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CURRENT ISSUE

Volume 88Issue 9May 2022

EDITOR IN CHIEF: Dr. Gemma Reguera

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Editor in Chief

AEM EiC Reguera
Dr. Gemma Reguera

Editor in Chief (2026) | Michigan State University

Gemma Reguera is a professor in the Department of Microbiology and Molecular Genetics at Michigan State University. Her work investigates energy conversion reactions catalyzed by microbes in natural and anthropogenic systems.

Editorial Board

  • Applied and Environmental MicrobiologyArticle
    Symbiotic Nitrogen Fixation and the Challenges to Its Extension to Nonlegumes

    ABSTRACT

    Access to fixed or available forms of nitrogen limits the productivity of crop plants and thus food production. Nitrogenous fertilizer production currently represents a significant expense for the efficient growth of various crops in the developed world. There are significant potential gains to be had from reducing dependence on nitrogenous fertilizers in agriculture in the developed world and in developing countries, and there is significant interest in research on biological nitrogen fixation and prospects for increasing its importance in an agricultural setting. Biological nitrogen fixation is the conversion of atmospheric N2 to NH3, a form that can be used by plants. However, the process is restricted to bacteria and archaea and does not occur in eukaryotes. Symbiotic nitrogen fixation is part of a mutualistic relationship in which plants provide a niche and fixed carbon to bacteria in exchange for fixed nitrogen. This process is restricted mainly to legumes in agricultural systems, and there is considerable interest in exploring whether similar symbioses can be developed in nonlegumes, which produce the bulk of human food. We are at a juncture at which the fundamental understanding of biological nitrogen fixation has matured to a level that we can think about engineering symbiotic relationships using synthetic biology approaches. This minireview highlights the fundamental advances in our understanding of biological nitrogen fixation in the context of a blueprint for expanding symbiotic nitrogen fixation to a greater diversity of crop plants through synthetic biology.

    REFERENCES

    1.
    Boyd ES, Peters JW. 2013. New insights into the evolutionary history of biological nitrogen fixation. Front Microbiol 4:201.
    2.
    Hardoim PR, van Overbeek LS, Berg G, Pirttilä AM, Compant S, Campisano A, Döring M, Sessitsch A. 2015. The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiol Mol Biol Rev 79:293–320.
    3.
    Santi C, Bogusz D, Franche C. 2013. Biological nitrogen fixation in non-legume plants. Ann Bot 111:743–767.
    4.
    Compant S, Clément C, Sessitsch A. 2010. Plant growth-promoting bacteria in the rhizo- and endosphere of plants: their role, colonization, mechanisms involved and prospects for utilization. Soil Biol Biochem 42:669–678.
    5.
    Schmid M, Hartmann A. 2007. Molecular phylogeny and ecology of root associated diazotrophic α- and β-proteobacteria, p 21–40. In Elmerich C, Newton W (ed), Associative and endophytic nitrogen-fixing bacteria and cyanobacterial associations. Springer-Verlag New York, Inc., New York, NY.
    6.
    Ahemad M, Kibret M. 2014. Mechanisms and applications of plant growth promoting rhizobacteria: current perspective. J King Saud Univ Sci 26:1–20.
    7.
    Steenhoudt O, Vanderleyden J. 2000. Azospirillum, a free-living nitrogen-fixing bacterium closely associated with grasses: genetic, biochemical and ecological aspects. FEMS Microbiol Rev 24:487–506.
    8.
    Peters GA, Meeks JC. 1989. The Azolla-Anabaena symbiosis: basic biology. Annu Rev Plant Physiol Plant Mol Biol 40:193–210.
    9.
    Pedraza RO. 2008. Recent advances in nitrogen-fixing acetic acid bacteria. Int J Food Microbiol 125:25–35.
    10.
    Nair DN, Padmavathy S. 2014. Impact of endophytic microorganisms on plants, environment and humans. Sci World J 2014:250693.
    11.
    Eskin N, Vessey K, Tian L. 2014. Research progress and perspectives of nitrogen fixing bacterium, Gluconacetobacter diazotrophicus, in monocot plants. Int J Agron 2014:1–13.
    12.
    Adams DG, Duggan PS. 2008. Cyanobacteria-bryophyte symbioses. J Exp Bot 59:1047–1058.
    13.
    Costa JL, Lindblad P. 2002. Cyanobacteria in symbiosis with cycads, p 195–205. In Rai AN, Bergman B, Rasmussen U (ed), Cyanobacteria in symbiosis. Springer, Dordrecht, The Netherlands.
    14.
    Bergman B, Osborne B. 2002. The Gunnera:Nostoc symbiosis. Biol Environ 102B:35–39.
    15.
    Long SR. 1996. Rhizobium symbiosis: Nod factors in perspective. Plant Cell 8:1885–1898.
    16.
    Oldroyd GED, Downie JA. 2008. Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu Rev Plant Biol 59:519–546.
    17.
    Davis EO, Evans IJ, Johnston AW. 1988. Identification of nodX, a gene that allows Rhizobium leguminosarum biovar viciae strain TOM to nodulate Afghanistan peas. Mol Gen Genet 212:531–535.
    18.
    Devine TE, Kuykendall LD, Breithaupt BH. 1980. Nodulation of soybeans carrying the nodulation-restrictive gene, rj1, by an incompatible Rhizobium japonicum strain upon mixed inoculation with a compatible strain. Can J Microbiol 26:179–182.
    19.
    Radutoiu S, Madsen LH, Madsen EB, Jurkiewicz A, Fukai E, Quistgaard EM, Albrektsen AS, James EK, Thirup S, Stougaard J. 2007. LysM domains mediate lipochitin-oligosaccharide recognition and Nfr genes extend the symbiotic host range. EMBO J 26:3923–3935.
    20.
    Sprent JI, James EK. 2007. Legume evolution: where do nodules and mycorrhizas fit in? Plant Physiol 144:575–581.
    21.
    Hirsch AM. 1992. Developmental biology of legume nodulation. New Phytol 122:211–237.
    22.
    Svistoonoff S, Hocher V, Gherbi H. 2014. Actinorhizal root nodule symbioses: what is signalling telling on the origins of nodulation? Curr Opin Plant Biol 20:11–18.
    23.
    Sytsma KJ, Morawetz J, Pires JC, Nepokroeff M, Conti E, Zjhra M, Hall JC, Chase MW. 2002. Urticalean rosids: circumscription, rosid ancestry, and phylogenetics based on rbcL, trnL-F, and ndhF sequences. Am J Bot 89:1531–1546.
    24.
    Behm JE, Geurts R, Kiers ET. Parasponia: a novel system for studying mutualism stability. Trends Plant Sci 19:757–763.
    25.
    Cárdenas L, Domínguez J, Quinto C, López-Lara IM, Lugtenberg BJ, Spaink HP, Rademaker GJ, Haverkamp J, Thomas-Oates JE. 1995. Isolation, chemical structures and biological activity of the lipo-chitin oligosaccharide nodulation signals from Rhizobium etli. Plant Mol Biol 29:453–464.
    26.
    Perret X, Staehelin C, Broughton WJ. 2000. Molecular basis of symbiotic promiscuity. Microbiol Mol Biol Rev 64:180–201.
    27.
    Finan TM, Hirsch AM, Leigh JA, Johansen E, Kuldau GA, Deegan S, Walker GC, Signer ER. 1985. Symbiotic mutants of Rhizobium meliloti that uncouple plant from bacterial differentiation. Cell 40:869–877.
    28.
    Leigh JA, Signer ER, Walker GC. 1985. Exopolysaccharide-deficient mutants of Rhizobium meliloti that form ineffective nodules. Proc Natl Acad Sci U S A 82:6231–6235.
    29.
    Cheng HP, Walker GC. 1998. Succinoglycan is required for initiation and elongation of infection threads during nodulation of alfalfa by Rhizobium meliloti. J Bacteriol 180:5183–5191.
    30.
    Dylan T, Ielpi L, Stanfield S, Kashyap L, Douglas C, Yanofsky M, Nester E, Helinski DR, Ditta G. 1986. Rhizobium meliloti genes required for nodule development are related to chromosomal virulence genes in Agrobacterium tumefaciens. Proc Natl Acad Sci U S A 83:4403–4407.
    31.
    Mithöfer A. 2002. Suppression of plant defence in rhizobia-legume symbiosis. Trends Plant Sci 7:440–444.
    32.
    Kawaharada Y, Kelly S, Nielsen MW, Hjuler CT, Gysel K, Muszynski A, Carlson RW, Thygesen MB, Sandal N, Asmussen MH, Vinther M, Andersen SU, Krusell L, Thirup S, Jensen KJ, Ronson CW, Blaise M, Radutoiu S, Stougaard J. 2015. Receptor-mediated exopolysaccharide perception controls bacterial infection. Nature 523:308–312.
    33.
    Persson T, Battenberg K, Demina IV, Vigil-Stenman T, Vanden Heuvel B, Pujic P, Facciotti MT, Wilbanks EG, O'Brien A, Fournier P, Cruz Hernandez MA, Mendoza Herrera A, Médigue C, Normand P, Pawlowski K, Berry AM. Candidatus Frankia datiscae Dg1, the actinobacterial microsymbiont of Datisca glomerata, expresses the canonical nod genes nodABC in symbiosis with its host plant. PLoS One 10:e0127630.
    34.
    Cérémonie H, Debellé F, Fernandez MP. 1999. Structural and functional comparison of Frankia root hair deforming factor and rhizobia Nod factor. Can J Bot 77:1293–1301.
    35.
    Wagner GM. 1997. Azolla: a review of its biology and utilization. Bot Rev 63:1–26.
    36.
    Jones DL, Nguyen C, Finlay RD. 2009. Carbon flow in the rhizosphere: carbon trading at the soil-root interface. Plant Soil 321:5–33.
    37.
    Günter N, Volker R. 2007. The release of root exudates as affected by the plant physiological status, p 23–72. In Pinton R, Varanini Z, Nannipieri P (ed), The rhizophere: biochemistry and organic substances at the soil-plant interface. CRC Press, Boca Raton, FL.
    38.
    Turner TR, James EK, Poole PS. 2013. The plant microbiome. Genome Biol 14:209.
    39.
    Turner TR, Ramakrishnan K, Walshaw J, Heavens D, Alston M, Swarbreck D, Osbourn A, Grant A, Poole PS. 2013. Comparative metatranscriptomics reveals kingdom level changes in the rhizosphere microbiome of plants. ISME J 7:2248–2258.
    40.
    Kamilova F, Validov S, Azarova T, Mulders I, Lugtenberg B. 2005. Enrichment for enhanced competitive plant root tip colonizers selects for a new class of biocontrol bacteria. Environ Microbiol 7:1809–1817.
    41.
    Kamilova F, Kravchenko LV, Shaposhnikov AI, Azarova T, Makarova N, Lugtenberg B. 2006. Organic acids, sugars, and l-tryptophane in exudates of vegetables growing on stonewool and their effects on activities of rhizosphere bacteria. Mol Plant Microbe Interact 19:250–256.
    42.
    van Egeraat AWSM. 1975. The possible role of homoserine in the development of Rhizobium leguminosarum in the rhizosphere of pea seedlings. Plant Soil 42:381–386.
    43.
    Vanderlinde EM, Hynes MF, Yost CK. 2014. Homoserine catabolism by Rhizobium leguminosarum bv. viciae 3841 requires a plasmid-borne gene cluster that also affects competitiveness for nodulation. Environ Microbiol 16:205–217.
    44.
    Ramachandran VK, East AK, Karunakaran R, Downie JA, Poole PS. 2011. Adaptation of Rhizobium leguminosarum to pea, alfalfa and sugar beet rhizospheres investigated by comparative transcriptomics. Genome Biol 12:R106.
    45.
    Baetz U, Martinoia E. 2014. Root exudates: the hidden part of plant defense. Trends Plant Sci 19:90–98.
    46.
    Neal AL, Ahmad S, Gordon-Weeks R, Ton J. 2012. Benzoxazinoids in root exudates of maize attract Pseudomonas putida to the rhizosphere. PLoS One 7:e35498.
    47.
    Fan J, Crooks C, Creissen G, Hill L, Fairhurst S, Doerner P, Lamb C. 2011. Pseudomonas sax genes overcome aliphatic isothiocyanate-mediated non-host resistance in Arabidopsis. Science 331:1185–1188.
    48.
    Soedarjo M, Borthakur D. 1997. Mimosine produced by the tree-legume Leucaena provides growth advantages to some Rhizobium strains that utilize it as a source of carbon and nitrogen, p 87–92. In Elkan GH, Upchurch RG (ed), Current issues in symbiotic nitrogen fixation. Springer, Dordrecht, The Netherlands.
    49.
    Cai T, Cai W, Zhang J, Zheng H, Tsou AM, Xiao L, Zhong Z, Zhu J. 2009. Host legume-exuded antimetabolites optimize the symbiotic rhizosphere. Mol Microbiol 73:507–517.
    50.
    Savka MA, Dessaux Y, Oger P, Rossbach S. 2002. Engineering bacterial competitiveness and persistence in the phytosphere. Mol Plant Microbe Interact 15:866–874.
    51.
    Murphy PJ, Wexler W, Grzemski W, Rao JP, Gordon D. 1995. Rhizopines—their role in symbiosis and competition. Soil Biol Biochem 27:525–529.
    52.
    Gordon DM, Ryder MH, Heinrich K, Murphy PJ. 1996. An experimental test of the rhizopine concept in Rhizobium meliloti. Appl Environ Microbiol 62:3991–3996.
    53.
    Oger P, Petit A, Dessaux Y. 1997. Genetically engineered plants producing opines alter their biological environment. Nat Biotechnol 15:369–372.
    54.
    Mondy S, Lenglet A, Beury-Cirou A, Libanga C, Ratet P, Faure D, Dessaux Y. 2014. An increasing opine carbon bias in artificial exudation systems and genetically modified plant rhizospheres leads to an increasing reshaping of bacterial populations. Mol Ecol 23:4846–4861.
    55.
    Oger P, Mansouri H, Dessaux Y. 2000. Effect of crop rotation and soil cover on alteration of the soil microflora generated by the culture of transgenic plants producing opines. Mol Ecol 9:881–890.
    56.
    Savka MA, Farrand SK. 1997. Modification of rhizobacterial populations by engineering bacterium utilization of a novel plant-produced resource. Nat Biotechnol 15:363–368.
    57.
    Kiers ET, Rousseau RA, West SA, Denison RF. 2003. Host sanctions and the legume-Rhizobium mutualism. Nature 425:78–81.
    58.
    Kiers ET, Duhamel M, Beesetty Y, Mensah JA, Franken O, Verbruggen E, Fellbaum CR, Kowalchuk GA, Hart MM, Bago A, Palmer TM, West SA, Vandenkoornhuyse P, Jansa J, Bücking H. 2011. Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333:880–882.
    59.
    Maróti G, Downie JA, Kondorosi É. 2015. Plant cysteine-rich peptides that inhibit pathogen growth and control rhizobial differentiation in legume nodules. Curr Opin Plant Biol 26:57–63.
    60.
    Czernic P, Gully D, Cartieaux F, Moulin L, Guefrachi I, Patrel D, Pierre O, Fardoux J, Chaintreuil C, Nguyen P, Gressent F, Da Silva C, Poulain J, Wincker P, Rofidal V, Hem S, Barrière Q, Arrighi J-F, Mergaert P, Giraud E. 2015. Convergent evolution of endosymbiont differentiation in Dalbergioid and inverted repeat-lacking clade legumes mediated by nodule-specific cysteine-rich peptides. Plant Physiol 169:1254–1265.
    61.
    Carro L, Pujic P, Trujillo M, Normand P. 2013. Micromonospora is a normal occupant of actinorhizal nodules. J Biosci 38:685–693.
    62.
    Meeks JC, Elhai J. 2002. Regulation of cellular differentiation in filamentous cyanobacteria in free-living and plant-associated symbiotic growth states. Microbiol Mol Biol Rev 66:94–121.
    63.
    Rai AN, Bergman B, Rasmussen U (ed). 2002. Cyanobacteria in symbiosis. Springer, Dordrecht, The Netherlands.
    64.
    Valverde C, Huss-Danell K. 2008. Carbon and nitrogen metabolism in actinorhizal nodules, p 167–198. In Pawlowski K, Newton WE (ed), Nitrogen-fixing actinorhizal symbioses. Springer, Dordrecht, The Netherlands.
    65.
    Colebatch G, Desbrosses G, Ott T, Krusell L, Montanari O, Kloska S, Kopka J, Udvardi MK. 2004. Global changes in transcription orchestrate metabolic differentiation during symbiotic nitrogen fixation in Lotus japonicus. Plant J 39:487–512.
    66.
    Benedito VA, Li H, Dai X, Wandrey M, He J, Kaundal R, Torres-Jerez I, Gomez SK, Harrison MJ, Tang Y, Zhao PX, Udvardi MK. 2010. Genomic inventory and transcriptional analysis of Medicago truncatula transporters. Plant Physiol 152:1716–1730.
    67.
    Kouchi H, Yoneyama T. 1984. Dynamics of carbon photosynthetically assimilated in nodulated soya bean plants under steady-state conditions 2. The incorporation of 13C into carbohydrates, organic acids, amino acids and some storage compounds. Ann Bot 53:883–896.
    68.
    Craig J, Barratt P, Tatge H, Déjardin A, Handley L, Gardner CD, Barber L, Wang T, Hedley C, Martin C, Smith AM. 1999. Mutations at the rug4 locus alter the carbon and nitrogen metabolism of pea plants through an effect on sucrose synthase. Plant J 17:353–362.
    69.
    Horst I, Welham T, Kelly S, Kaneko T, Sato S, Tabata S, Parniske M, Wang TL. 2007. TILLING mutants of Lotus japonicus reveal that nitrogen assimilation and fixation can occur in the absence of nodule-enhanced sucrose synthase. Plant Physiol 144:806–820.
    70.
    Udvardi M, Poole PS. 2013. Transport and metabolism in legume-rhizobia symbioses. Annu Rev Plant Biol 64:781–805.
    71.
    Limpens E, Moling S, Hooiveld G, Pereira PA, Bisseling T, Becker JD, Küster H. 2013. Cell- and tissue-specific transcriptome analyses of Medicago truncatula root nodules. PLoS One 8:e64377.
    72.
    Udvardi MK, Price GD, Gresshoff PM, Day DA. 1988. A dicarboxylate transporter on the peribacteroid membrane of soybean nodules. FEBS Lett 231:36–40.
    73.
    Yurgel SN, Kahn ML. 2004. Dicarboxylate transport by rhizobia. FEMS Microbiol Rev 28:489–501.
    74.
    Finan TM, Oresnik I, Bottacin A. 1988. Mutants of Rhizobium meliloti defective in succinate metabolism. J Bacteriol 170:3396–3403.
    75.
    Finan TM, McWhinne E, Driscoll B, Watson RJ. 1991. Complex symbiotic phenotypes result from gluconeogenic mutations in Rhizobium meliloti. Mol Plant Microbe Interact 4:386–392.
    76.
    Lodwig EM, Hosie AH, Bourdès A, Findlay K, Allaway D, Karunakaran R, Downie J, Poole PS. 2003. Amino-acid cycling drives nitrogen fixation in the legume-Rhizobium symbiosis. Nature 422:722–726.
    77.
    Mulley G, White JP, Karunakaran R, Prell J, Bourdes A, Bunnewell S, Hill L, Poole PS. 2011. Mutation of GOGAT prevents pea bacteroid formation and N2 fixation by globally downregulating transport of organic nitrogen sources. Mol Microbiol 80:149–167.
    78.
    Udvardi MK, Lister DL, Day DA. 1992. Isolation and characterization of a ntrC mutant of Bradyrhizobium (Parasponia) sp. ANU289. Microbiology 138:1019–1025.
    79.
    Patriarca EJ, Tatè R, Iaccarino M. 2002. Key role of bacterial NH4+ metabolism in Rhizobium-plant symbiosis. Microbiol Mol Biol Rev 66:203–222.
    80.
    Day DA, Kaiser BN, Thomson R, Udvardi MK, Moreau S, Puppo A. 2001. Nutrient transport across symbiotic membranes from legume nodules. Aust J Plant Physiol 28:669–676.
    81.
    Niemietz CM, Tyerman SD. 2000. Channel-mediated permeation of ammonia gas through the peribacteroid membrane of soybean nodules. FEBS Lett 465:110–114.
    82.
    Tyerman SD, Whitehead LF, Day DA. 1995. A channel-like transporter for NH4+ on the symbiotic interface of N2-fixing plants. Nature 378:629–632.
    83.
    Hwang JH, Ellingson SR, Roberts DM. 2010. Ammonia permeability of the soybean nodulin 26 channel. FEBS Lett 584:4339–4343.
    84.
    Masalkar P, Wallace IS, Hwang JH, Roberts DM. 2010. Interaction of cytosolic glutamine synthetase of soybean root nodules with the C-terminal domain of the symbiosome membrane nodulin 26 aquaglyceroporin. J Biol Chem 285:23880–23888.
    85.
    Eckardt NA. 2005. Insights into plant cellular mechanisms: of phosphate transporters and arbuscular mycorrhizal infection. Plant Cell 17:3213–3216.
    86.
    Kaiser BN, Moreau S, Castelli J, Thomson R, Lambert A, Bogliolo S, Puppo A, Day DA. 2003. The soybean NRAMP homologue, GmDMT1, is a symbiotic divalent metal transporter capable of ferrous iron transport. Plant J 35:295–304.
    87.
    Krusell L, Krause K, Ott T, Desbrosses G, Krämer U, Sato S, Nakamura Y, Tabata S, James EK, Sandal N, Stougaard J, Kawaguchi M, Miyamoto A, Suganuma N, Udvardi MK. 2005. The sulfate transporters SST1 is crucial for symbiotic nitrogen fixation in Lotus japonicus root nodules. Plant Cell 17:1625–1636.
    88.
    Bellenger JP, Wichard T, Kustka AB, Kraepiel AML. 2008. Uptake of molybdenum and vanadium by a nitrogen-fixing soil bacterium using siderophores. Nat Geosci 1:243–246.
    89.
    Delgado MJ, Tresierra-Ayala A, Talbi C, Bedmar EJ. 2006. Functional characterization of the Bradyrhizobium japonicum modA and modB genes involved in molybdenum transport. Microbiology 152:199–207.
    90.
    Campbell GRO, Taga ME, Mistry K, Lloret J, Anderson PJ, Roth JR, Walker GC. 2006. Sinorhizobium meliloti bluB is necessary for production of 5,6-dimethylbenzimidazole, the lower ligand of B12. Proc Natl Acad Sci U S A 103:4634–4639.
    91.
    Black KG, Parsons R, Osborne BA. 2002. Uptake and metabolism of glucose in the Nostoc-Gunnera symbiosis. New Phytol 153:297–305.
    92.
    Peters JW, Boyd ES, Hamilton TL, Rubio L. 2011. Biochemistry of Mo-nitrogenase, p 59–100. In Moir JWB (ed), Nitrogen cycling in bacteria: molecular analysis. Caister Academic Press, Norfolk, United Kingdom.
    93.
    Rubio LM, Ludden PW. 2008. Biosynthesis of the iron-molybdenum cofactor of nitrogenase. Annu Rev Microbiol 62:93–111.
    94.
    Edgren T, Nordlund S. 2004. The fixABCX genes in Rhodospirillum rubrum encode a putative membrane complex participating in electron transfer to nitrogenase. J Bacteriol 186:2052–2060.
    95.
    Boyd ES, Costas AM, Hamilton TL, Mus F, Peters JW. 2015. Evolution of molybdenum nitrogenase during the transition from anaerobic to aerobic metabolism. J Bacteriol 197:1690–1699.
    96.
    Ott T, van Dongen JT, Gunther C, Krusell L, Desbrosses G, Vigeolas H, Bock V, Czechowski T, Geigenberger P, Udvardi MK. 2005. Symbiotic leghemoglobins are crucial for nitrogen fixation in legume root nodules but not for general plant growth and development. Curr Biol 15:531–535.
    97.
    Dixon R, Kahn D. 2004. Genetic regulation of biological nitrogen fixation. Nat Rev Microbiol 2:621–631.
    98.
    Pitcher RS, Watmough NJ. 2004. The bacterial cytochrome cbb3 oxidases. Biochim Biophys Acta 1655:388–399.
    99.
    Preisig O, Anthamatten D, Hennecke H. 1993. Genes for a microaerobically induced oxidase complex in Bradyrhizobium japonicum are essential for a nitrogen-fixing endosymbiosis. Proc Natl Acad Sci U S A 90:3309–3313.
    100.
    Fay P. 1992. Oxygen relations of nitrogen fixation in cyanobacteria. Microbiol Rev 56:340–373.
    101.
    Murry MA, Horne AJ, Benemann JR. 1984. Physiological studies of oxygen protection mechanisms in the heterocysts of Anabaena cylindrica. Appl Environ Microbiol 47:449–454.
    102.
    Stal LJ, Krumbien WE. 1985. Nitrogenase activity in the non-heterocystous cyanobacterium Oscillatoria sp. grown under alternating light-dark cycles. Arch Microbiol 143:67–71.
    103.
    Poole RK, Hill S. 1997. Respiratory protection of nitrogenase activity in Azotobacter vinelandii—roles of the terminal oxidases. Biosci Rep 17:303–320.
    104.
    Maier RJ, Moshiri F. 2000. Role of the Azotobacter vinelandii nitrogenase-protective shethna protein in preventing oxygen-mediated cell death. J Bacteriol 182:3854–3857.
    105.
    Sabra W, Zeng A-P, Lünsdorf H, Deckwer W-D. 2000. Effect of oxygen on formation and structure of Azotobacter vinelandii alginate and its role protecting nitrogenase. Appl Environ Microbiol 66:4037–4044.
    106.
    Berry AM, Harriott OT, Moreau RA, Osman SF, Benson DR, Jones AD. 1993. Hopanoid lipids compose the Frankia vesicle envelope, presumptive barrier of oxygen diffusion to nitrogenase. Proc Natl Acad Sci U S A 90:6091–6094.
    107.
    Pawlowski K, Bisseling T. 1996. Rhizobial and actinorhizal symbioses: what are the shared features? Plant Cell 8:1899–1913.
    108.
    Oldroyd GE. 2013. Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nat Rev Microbiol 11:252–263.
    109.
    Oldroyd GE, Murray JD, Poole PS, Downie JA. 2011. The rules of engagement in the legume-rhizobial symbiosis. Annu Rev Genet 45:119–144.
    110.
    Curatti L, Rubio LM. 2014. Challenges to develop nitrogen-fixing cereals by direct nif-gene transfer. Plant Sci 225:130–137.
    111.
    Hawkesford MJ. 2014. Reducing the reliance on nitrogen fertilizer for wheat production. J Cereal Sci 59:276–283.
    112.
    Weber E, Engler C, Gruetzner R, Werner S, Marillonnet S. 2011. A modular cloning system for standardized assembly of multigene constructs. PLoS One 6:e16765.
    113.
    Gibson DG. 2011. Enzymatic assembly of overlapping DNA fragments. Methods Enzymol 498:349–361.
    114.
    Rogers C, Oldroyd GED. 2014. Synthetic biology approaches to engineering the nitrogen symbiosis in cereals. J Exp Bot 65:1939–1946.
    115.
    Martinez-Argudo I, Little R, Shearer N, Johnson P, Dixon R. 2004. The NifL-NifA system: a multidomain transcriptional regulatory complex that integrates environmental signals. J Bacteriol 186:601–610.
    116.
    Bode HB, Müller R. 2005. The impact of bacterial genomics on natural product research. Angew Chem Int Ed Engl 44:6828–6846.
    117.
    Hertweck C. 2009. Hidden biosynthetic treasures brought to light. Nat Chem Biol 5:450–452.
    118.
    Brakhage AA, Schroeckh V. 2011. Fungal secondary metabolites–strategies to activate silent gene clusters. Fungal Genet Biol 48:15–22.
    119.
    Temme K, Zhao D, Voigt CA. 2012. Refactoring the nitrogen fixation gene cluster from Klebsiella oxytoca. Proc Natl Acad Sci U S A 109:7085–7090.
    120.
    Fischbach M, Voigt CA. 2010. Prokaryotic gene clusters: a rich toolbox for synthetic biology. Biotechnol J 5:1277–1296.
    121.
    Jaschke PR, Lieberman EK, Rodriguez J, Sierra A, Endy D. 2012. A fully decompressed synthetic bacteriophage øX174 genome assembled and archived in yeast. Virology 434:278–284.
    122.
    Chan LY, Kosuri S, Endy D. 2005. Refactoring bacteriophage T7. Mol Syst Biol 1:2005.0018.
    123.
    Smanski MJ, Bhatia S, Zhao D, Park Y, Woodruff LBA, Giannoukos G, Ciulla D, Busby M, Calderon J, Nicol R, Gordon DB, Densmore D, Voigt CA. 2014. Functional optimization of gene clusters by combinatorial design and assembly. Nat Biotechnol 32:1241–1249.
    124.
    Wang X, Yang JG, Chen L, Wang JL, Cheng Q, Dixon R, Wang YP. 2013. Using synthetic biology to distinguish and overcome regulatory and functional barriers related to nitrogen fixation. PLoS One 8:e68677.
    125.
    Kosuri S, Church GM. 2014. Large-scale de novo DNA synthesis: technologies and applications. Nat Methods 11:499–507.
    126.
    Kodumal SJ, Patel KG, Reid R, Menzella HG, Welch M, Santi DV. 2004. Total synthesis of long DNA sequences: synthesis of a contiguous 32-kb polyketide synthase gene cluster. Proc Natl Acad Sci U S A 101:15573–15578.
    127.
    Annaluru N, Muller H, Mitchell LA, Ramalingam S, Stracquadanio G, Richardson SM, Dymond JS, Kuang Z, Scheifele LZ, Cooper EM, Cai Y, Zeller K, Agmon N, Han JS, Hadjithomas M, Tullman J, Caravelli K, Cirelli K, Guo Z, London V, Yeluru A, Murugan S, Kandavelou K, Agier N, Fischer G, Yang K, Martin JA, Bilgel M, Bohutski P, Boulier KM, Capaldo BJ, Chang J, Charoen K, Choi WJ, Deng P, DiCarlo JE, Doong J, Dunn J, Feinberg JI, Fernandez C, Floria CE, Gladowski D, Hadidi P, Ishizuka I, Jabbari J, Lau CY, Lee PA, Li S, Lin D, Linder ME, et al. 2014. Total synthesis of a functional designer eukaryotic chromosome. Science 344:55–58.
    128.
    Gibson DG, Glass JI, Lartigue C, Noskov VN, Chuang RY, Algire MA, Benders GA, Montague MG, Ma L, Moodie MM, Merryman C, Vashee S, Krishnakumar R, Assad-Garcia N, Andrews-Pfannkoch C, Denisova EA, Young L, Qi ZQ, Segall-Shapiro TH, Calvey CH, Parmar PP, Hutchison CA, III, Smith HO, Venter JC. 2010. Creation of a bacterial cell controlled by a chemically synthesized genome. Science 329:52–56.

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    Published In

    Applied and Environmental Microbiology
    Volume 82Number 131 July 2016
    Pages: 3698 - 3710
    Editor: R. M. Kelly, North Carolina State University
    PubMed: 27084023

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    Published online: 13 June 2016

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    Authors

    Florence Mus
    Department of Chemistry and Biochemistry, Montana State University, Bozeman, Montana, USA
    Matthew B. Crook
    Department of Bacteriology, University of Wisconsin—Madison, Madison, Wisconsin, USA
    Kevin Garcia
    Department of Bacteriology, University of Wisconsin—Madison, Madison, Wisconsin, USA
    Amaya Garcia Costas
    Department of Chemistry and Biochemistry, Montana State University, Bozeman, Montana, USA
    Barney A. Geddes
    Department of Plant Sciences, University of Oxford, Oxford, United Kingdom
    Evangelia D. Kouri
    Plant Biology Division, The Samuel Roberts Noble Foundation, Ardmore, Oklahoma, USA
    Ponraj Paramasivan
    John Innes Centre, Norwich Research Park, Norwich, United Kingdom
    Min-Hyung Ryu
    Department of Biological Engineering, Massachusetts Institute of Technology, Cambridge, Massachusetts, USA
    Giles E. D. Oldroyd
    John Innes Centre, Norwich Research Park, Norwich, United Kingdom
    Philip S. Poole
    Department of Plant Sciences, University of Oxford, Oxford, United Kingdom
    Michael K. Udvardi
    Plant Biology Division, The Samuel Roberts Noble Foundation, Ardmore, Oklahoma, USA
    Christopher A. Voigt
    Department of Biological Engineering, Massachusetts Institute of Technology, Cambridge, Massachusetts, USA
    Jean-Michel Ané
    Department of Bacteriology, University of Wisconsin—Madison, Madison, Wisconsin, USA
    John W. Peters
    Department of Chemistry and Biochemistry, Montana State University, Bozeman, Montana, USA

    Editor

    R. M. Kelly
    Editor
    North Carolina State University

    Notes

    Address correspondence to Jean-Michel Ané, [email protected], or John W. Peters, [email protected].

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  • Applied and Environmental MicrobiologyArticle
    Plastics: Environmental and Biotechnological Perspectives on Microbial Degradation

    ABSTRACT

    Plastics are widely used in the global economy, and each year, at least 350 to 400 million tons are being produced. Due to poor recycling and low circular use, millions of tons accumulate annually in terrestrial or marine environments. Today it has become clear that plastic causes adverse effects in all ecosystems and that microplastics are of particular concern to our health. Therefore, recent microbial research has addressed the question of if and to what extent microorganisms can degrade plastics in the environment. This review summarizes current knowledge on microbial plastic degradation. Enzymes available act mainly on the high-molecular-weight polymers of polyethylene terephthalate (PET) and ester-based polyurethane (PUR). Unfortunately, the best PUR- and PET-active enzymes and microorganisms known still have moderate turnover rates. While many reports describing microbial communities degrading chemical additives have been published, no enzymes acting on the high-molecular-weight polymers polystyrene, polyamide, polyvinylchloride, polypropylene, ether-based polyurethane, and polyethylene are known. Together, these polymers comprise more than 80% of annual plastic production. Thus, further research is needed to significantly increase the diversity of enzymes and microorganisms acting on these polymers. This can be achieved by tapping into the global metagenomes of noncultivated microorganisms and dark matter proteins. Only then can novel biocatalysts and organisms be delivered that allow rapid degradation, recycling, or value-added use of the vast majority of most human-made polymers.

    REFERENCES

    1.
    Geyer R, Jambeck JR, Law KL. 2017. Production, use, and fate of all plastics ever made. Sci Adv 3:e1700782.
    2.
    PlasticsEurope. 2018. PlasticsEurope, plastics—the facts 2018: an analysis of European plastics production, demand and waste data. PlasticsEurope, Brussels, Belgium.
    3.
    Ellen MacArthur Foundation. 2017. The new plastics economy: rethinking the future of plastics and catalysing action. Ellen MacArthur Foundation, Cowes, United Kingdom.
    4.
    Jambeck JR, Geyer R, Wilcox C, Siegler TR, Perryman M, Andrady A, Narayan R, Law KL. 2015. Marine pollution. Plastic waste inputs from land into the ocean. Science 347:768–771.
    5.
    Derraik J. 2002. The pollution of the marine environment by plastic debris: a review. Mar Pollut Bull 44:842–852.
    6.
    Cózar A, Echevarría F, González-Gordillo JI, Irigoien X, Úbeda B, Hernández-León S, Palma ÁT, Navarro S, García-de-Lomas J, Ruiz A, Fernández-de-Puelles ML, Duarte CM. 2014. Plastic debris in the open ocean. Proc Natl Acad Sci U S A 111:10239–10244.
    7.
    Lebreton L, Slat B, Ferrari F, Sainte-Rose B, Aitken J, Marthouse R, Hajbane S, Cunsolo S, Schwarz A, Levivier A, Noble K, Debeljak P, Maral H, Schoeneich-Argent R, Brambini R, Reisser J. 2018. Evidence that the Great Pacific Garbage Patch is rapidly accumulating plastic. Sci Rep 8:4666.
    8.
    Wei R, Zimmermann W. 2017. Microbial enzymes for the recycling of recalcitrant petroleum-based plastics: how far are we? Microb Biotechnol 10:1308.
    9.
    Day M, Wiles DM. 1972. Photochemical degradation of poly(ethylene terephthalate). II. Effect of wavelength and environment on the decomposition process. J Appl Polym Sci 16:191–202.
    10.
    Mohammadian M, Allen NS, Edge M, Jones K. 1991. Environmental degradation of poly (ethylene terephthalate). Textile Res J 61:690–696.
    11.
    Welzel K, Müller RJ, Deckwer WD. 2002. Enzymatischer Abbau von Polyester-Nanopartikeln. Chemie Ingenieur Technik 74:1496–1500.
    12.
    Smith M, Love DC, Rochman CM, Neff RA. 2018. Microplastics in seafood and the implications for human health. Curr Environ Health Rep 5:375–386.
    13.
    de Souza Machado AA, Kloas W, Zarfl C, Hempel S, Rillig MC. 2018. Microplastics as an emerging threat to terrestrial ecosystems. Glob Chang Biol 24:1405–1416.
    14.
    Gubbels E, Heitz T, Yamamoto M, Chilekar V, Zarbakhsh S, Gepraegs M, Köpnick H, Schmidt M, Brügging W, Rüter J, Kaminsky W. 2018. Polyesters. In Ullmann’s encyclopedia of industrial chemistry. Wiley-VCH, Weinheim, Germany.
    15.
    Acero EH, Ribitsch D, Steinkellner G, Gruber K, Greimel K, Eiteljoerg I, Trotscha E, Wei R, Zimmermann W, Zinn M, Cavaco-Paulo A, Freddi G, Schwab H, Guebitz G. 2011. Enzymatic surface hydrolysis of PET: effect of structural diversity on kinetic properties of cutinases from Thermobifida. Macromolecules 44:4632–4640.
    16.
    Kleeberg I, Hetz C, Kroppenstedt RM, Muller RJ, Deckwer WD. 1998. Biodegradation of aliphatic-aromatic copolyesters by Thermomonospora fusca and other thermophilic compost isolates. Appl Environ Microbiol 64:1731–1735.
    17.
    Hu X, Thumarat U, Zhang X, Tang M, Kawai F. 2010. Diversity of polyester-degrading bacteria in compost and molecular analysis of a thermoactive esterase from Thermobifida alba AHK119. Appl Microbiol Biotechnol 87:771–779.
    18.
    Wei R, Oeser T, Then J, Kuhn N, Barth M, Schmidt J, Zimmermann W. 2014. Functional characterization and structural modeling of synthetic polyester-degrading hydrolases from Thermomonospora curvata. AMB Express 4:44.
    19.
    Wei R, Oeser T, Zimmermann W. 2014. Synthetic polyester-hydrolyzing enzymes from thermophilic actinomycetes. Adv Appl Microbiol 89:267–305.
    20.
    Chen S, Tong X, Woodard RW, Du GC, Wu J, Chen J. 2008. Identification and characterization of bacterial cutinase. J Biol Chem 283:25854–25862.
    21.
    Zimmermann W, Billig S. 2011. Enzymes for the biofunctionalization of poly(ethylene terephthalate). Adv Biochem Eng Biotechnol 125:97–120.
    22.
    Ribitsch D, Acero EH, Greimel K, Dellacher A, Zitzenbacher S, Marold A, Rodriguez RD, Steinkellner G, Gruber K, Schwab H, Guebitz GM. 2012. A new esterase from Thermobifida halotolerans hydrolyses polyethylene terephthalate (PET) and polylactic acid (PLA). Polymers 4:617–629.
    23.
    Kawai F, Oda M, Tamashiro T, Waku T, Tanaka N, Yamamoto M, Mizushima H, Miyakawa T, Tanokura M. 2014. A novel Ca2+-activated, thermostabilized polyesterase capable of hydrolyzing polyethylene terephthalate from Saccharomonospora viridis AHK190. Appl Microbiol Biotechnol 98:10053–10064.
    24.
    Ollis DL, Cheah E, Cygler M, Dijkstra B, Frolow F, Franken SM, Harel M, Remington SJ, Silman I, Schrag J. 1992. The alpha/beta hydrolase fold. Protein Eng 5:197–211.
    25.
    Yoshida S, Hiraga K, Takehana T, Taniguchi I, Yamaji H, Maeda Y, Toyohara K, Miyamoto K, Kimura Y, Oda K. 2016. A bacterium that degrades and assimilates poly(ethylene terephthalate). Science 351:1196–1199.
    26.
    Austin HP, Allen MD, Donohoe BS, Rorrer NA, Kearns FL, Silveira RL, Pollard BC, Dominick G, Duman R, El Omari K, Mykhaylyk V, Wagner A, Michener WE, Amore A, Skaf MS, Crowley MF, Thorne AW, Johnson CW, Woodcock HL, McGeehan JE, Beckham GT. 2018. Characterization and engineering of a plastic-degrading aromatic polyesterase. Proc Natl Acad Sci U S A 115:E4350–E4357.
    27.
    Roth C, Wei R, Oeser T, Then J, Follner C, Zimmermann W, Strater N. 2014. Structural and functional studies on a thermostable polyethylene terephthalate degrading hydrolase from Thermobifida fusca. Appl Microbiol Biotechnol 98:7815–7823.
    28.
    Sulaiman S, You DJ, Kanaya E, Koga Y, Kanaya S. 2014. Crystal structure and thermodynamic and kinetic stability of metagenome-derived LC-cutinase. Biochemistry 53:1858–1869.
    29.
    Then J, Wei R, Oeser T, Gerdts A, Schmidt J, Barth M, Zimmermann W. 2016. A disulfide bridge in the calcium binding site of a polyester hydrolase increases its thermal stability and activity against polyethylene terephthalate. FEBS Open Bio 6:425–432.
    30.
    Ribitsch D, Heumann S, Trotscha E, Acero EH, Greimel K, Leber R, Birner-Gruenberger R, Deller S, Eiteljoerg I, Remler P, Weber T, Siegert P, Maurer KH, Donelli I, Freddi G, Schwab H, Guebitz GM. 2011. Hydrolysis of polyethyleneterephthalate by p-nitrobenzylesterase from Bacillus subtilis. Biotechnol Progress 27:951–960.
    31.
    Danso D, Schmeisser C, Chow J, Zimmermann W, Wei R, Leggewie C, Li X, Hazen T, Streit WR. 2018. New insights into the function and global distribution of polyethylene terephthalate (PET)-degrading bacteria and enzymes in marine and terrestrial metagenomes. Appl Environ Microbiol 84:e02773-17.
    32.
    Palm GJ, Reisky L, Böttcher D, Müller H, Michels EAP, Walczak MC, Berndt L, Weiss MS, Bornscheuer UT, Weber G. 2019. Structure of the plastic-degrading Ideonella sakaiensis MHETase bound to a substrate. Nat Commun 10:1717.
    33.
    Barth M, Oeser T, Wei R, Then J, Schmidt J, Zimmermann W. 2015. Effect of hydrolysis products on the enzymatic degradation of polyethylene terephthalate nanoparticles by a polyester hydrolase from Thermobifida fusca. Biochem Eng J 93:222–228.
    34.
    Carniel A, Valoni E, Nicomedes J, Gomes AD, de Castro AM. 2017. Lipase from Candida antarctica (CALB) and cutinase from Humicola insolens act synergistically for PET hydrolysis to terephthalic acid. Process Biochem 59:84–90.
    35.
    Wei R, Oeser T, Schmidt J, Meier R, Barth M, Then J, Zimmermann W. 2016. Engineered bacterial polyester hydrolases efficiently degrade polyethylene terephthalate due to relieved product inhibition. Biotechnol Bioeng 113:1658–1665.
    36.
    Haernvall K, Zitzenbacher S, Wallig K, Yamamoto M, Schick MB, Ribitsch D, Guebitz GM. 2017. Hydrolysis of ionic phthalic acid based polyesters by wastewater microorganisms and their enzymes. Environ Sci Technol 51:4596–4605.
    37.
    Bollinger A, Thies S, Katzke N, Jaeger KE. 25 June 2018. The biotechnological potential of marine bacteria in the novel lineage of Pseudomonas pertucinogena. Microb Biotechnol doi:
    38.
    Hajighasemi M, Tchigvintsev A, Nocek BP, Flick R, Popovic A, Hai T, Khusnutdinova AN, Brown G, Xu X, Cui H, Anstett J, Chernikova TN, Bruls T, Le Paslier D, Yakimov MM, Joachimiak A, Golyshina OV, Savchenko A, Golyshin PN, Edwards EA, Yakunin AF. 2018. Screening and characterization of novel polyesterases from environmental metagenomes with high hydrolytic activity against synthetic polyesters. Environ Sci Technol 52:12388–12401.
    39.
    Seymour RB, Kauffman GB. 1992. Polyurethanes: a class of modern versatile materials. J Chem Educ 69:909.
    40.
    Darby RT, Kaplan AM. 1968. Fungal susceptibility of polyurethanes. Appl Microbiol 16:900–905.
    41.
    Russell JR, Huang J, Anand P, Kucera K, Sandoval AG, Dantzler KW, Hickman D, Jee J, Kimovec FM, Koppstein D, Marks DH, Mittermiller PA, Núñez SJ, Santiago M, Townes MA, Vishnevetsky M, Williams NE, Vargas MPN, Boulanger L-A, Bascom-Slack C, Strobel SA. 2011. Biodegradation of polyester polyurethane by endophytic fungi. Appl Environ Microbiol 77:6076–6084.
    42.
    Howard GT, Crother B, Vicknair J. 2001. Cloning, nucleotide sequencing and characterization of a polyurethanase gene (pueB) from Pseudomonas chlororaphis. Int Biodeterior Biodegrad 47:141–149.
    43.
    Howard GT, Blake RC. 1998. Growth of Pseudomonas fluorescens on a polyester–polyurethane and the purification and characterization of a polyurethanase–protease enzyme. Int Biodeterior Biodegrad 42:213–220.
    44.
    Stern RV, Howard GT. 2000. The polyester polyurethanase gene (pueA) from Pseudomonas chlororaphis encodes a lipase. FEMS Microbiol Lett 185:163–168.
    45.
    Howard GT, Mackie RI, Cann IK, Ohene-Adjei S, Aboudehen KS, Duos BG, Childers GW. 2007. Effect of insertional mutations in the pueA and pueB genes encoding two polyurethanases in Pseudomonas chlororaphis contained within a gene cluster. J Appl Microbiol 103:2074–2083.
    46.
    Hung CS, Zingarelli S, Nadeau LJ, Biffinger JC, Drake CA, Crouch AL, Barlow DE, Russell JN, Jr, Crookes-Goodson WJ. 2016. Carbon catabolite repression and impranil polyurethane degradation in Pseudomonas protegens strain Pf-5. Appl Environ Microbiol 82:6080–6090.
    47.
    Peng YH, Shih YH, Lai YC, Liu YZ, Liu YT, Lin NC. 2014. Degradation of polyurethane by bacterium isolated from soil and assessment of polyurethanolytic activity of a Pseudomonas putida strain. Environ Sci Pollut Res Int 21:9529–9537.
    48.
    Akutsu Y, Nakajima-Kambe T, Nomura N, Nakahara T. 1998. Purification and properties of a polyester polyurethane-degrading enzyme from Comamonas acidovorans TB-35. Appl Environ Microbiol 64:62–67.
    49.
    Shigeno-Akutsu Y, Nakajima-Kambe T, Nomura N, Nakahara T. 1999. Purification and properties of culture-broth-secreted esterase from the polyurethane degrader Comamonas acidovorans TB-35. J Biosci Bioeng 88:484–487.
    50.
    Biffinger JC, Barlow DE, Cockrell AL, Cusick KD, Hervey WJ, Fitzgerald LA, Nadeau LJ, Hung CS, Crookes-Goodson WJ, Russell JN. 2015. The applicability of Impranil® DLN for gauging the biodegradation of polyurethanes. Polym Degradation Stab 120:178–185.
    51.
    Shah Z, Krumholz L, Aktas DF, Hasan F, Khattak M, Shah AA. 2013. Degradation of polyester polyurethane by a newly isolated soil bacterium, Bacillus subtilis strain MZA-75. Biodegradation 24:865–877.
    52.
    Rowe L, Howard GT. 2002. Growth of Bacillus subtilis on polyurethane and the purification and characterization of a polyurethanase-lipase enzyme. Int Biodeterior Biodegrad 50:33–40.
    53.
    Oceguera-Cervantes A, Carrillo-García A, López N, Bolaños-Nuñez S, Cruz-Gómez MJ, Wacher C, Loza-Tavera H. 2007. Characterization of the polyurethanolytic activity of two Alicycliphilus sp. strains able to degrade polyurethane and n-methylpyrrolidone. Appl Environ Microbiol 73:6214–6223.
    54.
    Schmidt J, Wei R, Oeser T, Dedavid e Silva L, Breite D, Schulze A, Zimmermann W. 2017. Degradation of polyester polyurethane by bacterial polyester hydrolases. Polymers 9:65.
    55.
    Martinez-Martinez M, Coscolin C, Santiago G, Chow J, Stogios PJ, Bargiela R, Gertler C, Navarro-Fernandez J, Bollinger A, Thies S, Mendez-Garcia C, Popovic A, Brown G, Chernikova TN, Garcia-Moyano A, Bjerga GEK, Perez-Garcia P, Hai T, Del Pozo MV, Stokke R, Steen IH, Cui H, Xu X, Nocek BP, Alcaide M, Distaso M, Mesa V, Pelaez AI, Sanchez J, Buchholz PCF, Pleiss J, Fernandez-Guerra A, Glockner FO, Golyshina OV, Yakimov MM, Savchenko A, Jaeger KE, Yakunin AF, Streit WR, Golyshin PN, Guallar V, Ferrer M, The Inmare Consortium. 2018. Determinants and prediction of esterase substrate promiscuity patterns. ACS Chem Biol 13:225–234.
    56.
    Zafar U, Houlden A, Robson GD. 2013. Fungal communities associated with the biodegradation of polyester polyurethane buried under compost at different temperatures. Appl Environ Microbiol 79:7313–7324.
    57.
    Gautam R, Bassi AS, Yanful EK. 2007. Candida rugosa lipase-catalyzed polyurethane degradation in aqueous medium. Biotechnol Lett 29:1081–1086.
    58.
    Álvarez-Barragán J, Domínguez-Malfavón L, Vargas-Suárez M, González-Hernández R, Aguilar-Osorio G, Loza-Tavera H. 2016. Biodegradative activities of selected environmental fungi on a polyester polyurethane varnish and polyether polyurethane foams. Appl Environ Microbiol 82:5225–5235.
    59.
    Mathur G, Prasad R. 2012. Degradation of polyurethane by Aspergillus flavus (ITCC 6051) isolated from soil. Appl Biochem Biotechnol 167:1595–1602.
    60.
    Khan S, Nadir S, Shah ZU, Shah AA, Karunarathna SC, Xu J, Khan A, Munir S, Hasan F. 2017. Biodegradation of polyester polyurethane by Aspergillus tubingensis. Environ Pollut 225:469–480.
    61.
    Nowlin T. 2014. Global polyethylene business overview. In Nowlin TE (ed), Business and technology of the global polyethylene industry. Wiley-VCH, Weinheim, Germany.
    62.
    Sen SK, Raut S. 2015. Microbial degradation of low density polyethylene (LDPE): a review. J Environ Chem Eng 3:462–473.
    63.
    Restrepo-Florez JM, Bassi A, Thompson MR. 2014. Microbial degradation and deterioration of polyethylene—a review. Int Biodeterior Biodegrad 88:83–90.
    64.
    Pathak VM, Navneet. 2017. Review on the current status of polymer degradation: a microbial approach. Bioresource Bioprocess 4:15.
    65.
    Ojha N, Pradhan N, Singh S, Barla A, Shrivastava A, Khatua P, Rai V, Bose S. 2017. Evaluation of HDPE and LDPE degradation by fungus, implemented by statistical optimization. Sci Rep 7:39515.
    66.
    Yamada-Onodera K, Mukumoto H, Katsuyaya Y, Saiganji A, Tani Y. 2001. Degradation of polyethylene by a fungus, Penicillium simplicissimum YK. Polym Degradation Stab 72:323–327.
    67.
    Bonhomme S, Cuer A, Delort A, Lemaire J, Sancelme M, Scott G. 2003. Environmental biodegradation of polyethylene. Polym Degradation Stab 81:441–452.
    68.
    Veethahavya KS, Rajath BS, Noobia S, Kumar BM. 2016. Biodegradation of low density polyethylene in aqueous media. Procedia Environ Sci 35:709–713.
    69.
    Vimala PP, Mathew L. 2016. Biodegradation of polyethylene using Bacillus subtilis. Procedia Technol 24:232–239.
    70.
    Yang J, Yang Y, Wu W-M, Zhao J, Jiang L. 2014. Evidence of polyethylene biodegradation by bacterial strains from the guts of plastic-eating waxworms. Environ Sci Technol 48:13776–13784.
    71.
    Yang Y, Yang J, Wu W-M, Zhao J, Song Y, Gao L, Yang R, Jiang L. 2015. Biodegradation and mineralization of polystyrene by plastic-eating mealworms: Part 1. Chemical and physical characterization and isotopic tests. Environ Sci Technol 49:12080–12086.
    72.
    Sowmya HV, Ramalingappa B, Krishnappa M, Thippeswamy B. 2015. Degradation of polyethylene by Penicillium simplicissimum isolated from local dumpsite of Shivamogga district. Environ Dev Sustain 17:731–745.
    73.
    Palmer R. 2001. Polyamides, plastics. In Encyclopedia of polymer science and technology. Wiley, Hoboken, NJ.
    74.
    Tosa T, Chibata I. 1965. Utilization of cyclic amides and formation of omega-amino acids by microorganisms. J Bacteriol 89:919–920.
    75.
    Takehara I, Kato DI, Takeo M, Negoro S. 2017. Draft genome sequence of the nylon oligomer-degrading bacterium Arthrobacter sp. strain KI72. Genome Announc 5:e00217-17.
    76.
    Negoro S, Taniguchi T, Kanaoka M, Kimura H, Okada H. 1983. Plasmid-determined enzymatic degradation of nylon oligomers. J Bacteriol 155:22–31.
    77.
    Negoro S, Kakudo S, Urabe I, Okada H. 1992. A new nylon oligomer degradation gene (nylC) on plasmid pOAD2 from a Flavobacterium sp. J Bacteriol 174:7948–7953.
    78.
    Kakudo S, Negoro S, Urabe I, Okada H. 1993. Nylon oligomer degradation gene, nylC, on plasmid pOAD2 from a Flavobacterium strain encodes endo-type 6-aminohexanoate oligomer hydrolase: purification and characterization of the nylC gene product. Appl Environ Microbiol 59:3978.
    79.
    Negoro S, Ohki T, Shibata N, Sasa K, Hayashi H, Nakano H, Yasuhira K, Kato D-i, Takeo M, Higuchi Y. 2007. Nylon-oligomer degrading enzyme/substrate complex: catalytic mechanism of 6-aminohexanoate-dimer hydrolase. J Mol Biol 370:142–156.
    80.
    Yasuhira K, Uedo Y, Shibata N, Negoro S, Takeo M, Higuchi Y. 2006. Crystallization and X-ray diffraction analysis of 6-aminohexanoate-cyclic-dimer hydrolase from Arthrobacter sp. KI72. Acta Crystallogr Sect F Struct Biol Cryst Commun 62:1209–1211.
    81.
    Ohki T, Mizuno N, Shibata N, Takeo M, Negoro S, Higuchi Y. 2005. Crystallization and X-ray diffraction analysis of 6-aminohexanoate-dimer hydrolase from Arthrobacter sp. KI72. Acta Crystallogr Sect F Struct Biol Cryst Commun 61:928–930.
    82.
    Nagai K, Yasuhira K, Tanaka Y, Kato D, Takeo M, Higuchi Y, Negoro S, Shibata N. 2013. Crystallization and X-ray diffraction analysis of nylon hydrolase (NylC) from Arthrobacter sp. KI72. Acta Crystallogr Sect F Struct Biol Cryst Commun 69:1151–1154.
    83.
    Kinoshita S, Terada T, Taniguchi T, Takene Y, Masuda S, Matsunaga N, Okada H. 1981. Purification and characterization of 6-aminohexanoic-acid-oligomer hydrolase of Flavobacterium sp. Ki72. Eur J Biochem 116:547–551.
    84.
    Yasuhira K, Tanaka Y, Shibata H, Kawashima Y, Ohara A, Kato D, Takeo M, Negoro S. 2007. 6-Aminohexanoate oligomer hydrolases from the alkalophilic bacteria Agromyces sp. strain KY5R and Kocuria sp. strain KY2. Appl Environ Microbiol 73:7099–7102.
    85.
    Negoro S, Ohki T, Shibata N, Mizuno N, Wakitani Y, Tsurukame J, Matsumoto K, Kawamoto I, Takeo M, Higuchi Y. 2005. X-ray crystallographic analysis of 6-aminohexanoate-dimer hydrolase: molecular basis for the birth of a nylon oligomer-degrading enzyme. J Biol Chem 280:39644–39652.
    86.
    Kinoshita S, Negoro S, Muramatsu M, Bisaria VS, Sawada S, Okada H. 1977. 6-Aminohexanoic acid cyclic dimer hydrolase. A new cyclic amide hydrolase produced by Achromobacter guttatus KI74. Eur J Biochem 80:489–495.
    87.
    Kinoshita S, Kageyama S, Iba K, Yamada Y, Okada H. 1975. Utilization of a cyclic dimer and linear oligomers of ε-aminocaproic acid by Achromobacter guttatus KI 72. Agric Biol Chem 39:1219–1223.
    88.
    Takehara I, Fujii T, Tanimoto Y, Kato DI, Takeo M, Negoro S. 2018. Correction to: Metabolic pathway of 6-aminohexanoate in the nylon oligomer-degrading bacterium Arthrobacter sp. KI72: identification of the enzymes responsible for the conversion of 6-aminohexanoate to adipate. Appl Microbiol Biotechnol 102:815.
    89.
    Takehara I, Fujii T, Tanimoto Y, Kato DI, Takeo M, Negoro S. 2018. Metabolic pathway of 6-aminohexanoate in the nylon oligomer-degrading bacterium Arthrobacter sp. KI72: identification of the enzymes responsible for the conversion of 6-aminohexanoate to adipate. Appl Microbiol Biotechnol 102:801–814.
    90.
    Sudhakar M, Priyadarshini C, Doble M, Sriyutha Murthy P, Venkatesan R. 2007. Marine bacteria mediated degradation of nylon 66 and 6. Int Biodeterior Biodegrad 60:144–151.
    91.
    Oppermann FB, Pickartz S, Steinbüchel A. 1998. Biodegradation of polyamides. Polym Degradation Stab 59:337–344.
    92.
    Deguchi T, Kitaoka Y, Kakezawa M, Nishida T. 1998. Purification and characterization of a nylon-degrading enzyme. Appl Environ Microbiol 64:1366–1371.
    93.
    Prijambada ID, Negoro S, Yomo T, Urabe I. 1995. Emergence of nylon oligomer degradation enzymes in Pseudomonas aeruginosa PAO through experimental evolution. Appl Environ Microbiol 61:2020–2022.
    94.
    Kanagawa K, Oishi M, Negoro S, Urabe I, Okada H. 1993. Characterization of the 6-aminohexanoate-dimer hydrolase from Pseudomonas sp. NK87. J Gen Microbiol 139:787–795.
    95.
    Maul J, Frushour BG, Kontoff JR, Eichenauer H, Ott K-H, Schade C. 2007. Polystyrene and styrene copolymers. In Ullmann’s encyclopedia of industrial chemistry. Wiley-VCH, Weinheim, Germany.
    96.
    Krueger MC, Hofmann U, Moeder M, Schlosser D. 2015. Potential of wood-rotting fungi to attack polystyrene sulfonate and its depolymerisation by Gloeophyllum trabeum via hydroquinone-driven fenton chemistry. PLoS One 10:e0131773.
    97.
    Milstein O, Gersonde R, Huttermann A, Chen MJ, Meister JJ. 1992. Fungal biodegradation of lignopolystyrene graft copolymers. Appl Environ Microbiol 58:3225–3232.
    98.
    Ho BT, Roberts TK, Lucas S. 2018. An overview on biodegradation of polystyrene and modified polystyrene: the microbial approach. Crit Rev Biotechnol 38:308–320.
    99.
    Chauhan D, Agrawal G, Deshmukh S, Roy SS, Priyadarshini R. 2018. Biofilm formation by Exiguobacterium sp. DR11 and DR14 alter polystyrene surface properties and initiate biodegradation. RSC Adv 8:37590–37599.
    100.
    Mooney A, Ward PG, O’Connor KE. 2006. Microbial degradation of styrene: biochemistry, molecular genetics, and perspectives for biotechnological applications. Appl Microbiol Biotechnol 72:1.
    101.
    Dobson ADW, O’Leary ND, O'Connor KE. 2002. Biochemistry, genetics and physiology of microbial styrene degradation. FEMS Microbiol Rev 26:403–417.
    102.
    Tischler D. 2015. Microbial styrene degradation, p 7–22. Springer International Publishing, Cham, Switzerland.
    103.
    Oelschlägel M, Zimmerling J, Tischler D. 2018. A review: the styrene metabolizing cascade of side-chain oxygenation as biotechnological basis to gain various valuable compounds. Front Microbiol 9:490.
    104.
    Tischler D, Eulberg D, Lakner S, Kaschabek SR, van Berkel WJH, Schlomann M. 2009. Identification of a novel self-sufficient styrene monooxygenase from Rhodococcus opacus 1CP. J Bacteriol 191:4996–5009.
    105.
    Velasco A, Alonso S, García JL, Perera J, Díaz E. 1998. Genetic and functional analysis of the styrene catabolic cluster of Pseudomonas sp. strain Y2. J Bacteriol 180:1063–1071.
    106.
    Morrison E, Kantz A, Gassner GT, Sazinsky MH. 2013. Structure and mechanism of styrene monooxygenase reductase: new insight into the FAD-transfer reaction. Biochemistry 52:6063–6075.
    107.
    Oelschlägel M, Gröning JAD, Tischler D, Kaschabek SR, Schlömann M. 2012. Styrene oxide isomerase of Rhodococcus opacus 1CP, a highly stable and considerably active enzyme. Appl Environ Microbiol 78:4330–4337.
    108.
    Crabo AG, Singh B, Nguyen T, Emami S, Gassner GT, Sazinsky MH. 2017. Structure and biochemistry of phenylacetaldehyde dehydrogenase from the Pseudomonas putida S12 styrene catabolic pathway. Arch Biochem Biophys 616:47–58.
    109.
    O'Leary ND, O'Mahony MM, Dobson AD. 2011. Regulation of phenylacetic acid uptake is sigma54 dependent in Pseudomonas putida CA-3. BMC Microbiol 11:229.
    110.
    O’Leary ND, Duetz WA, Dobson AD, O’Connor KE. 2002. Induction and repression of the sty operon in Pseudomonas putida CA-3 during growth on phenylacetic acid under organic and inorganic nutrient-limiting continuous culture conditions. FEMS Microbiol Lett 208:263–268.
    111.
    O’Leary ND, Mooney A, O'Mahony M, Dobson AD. 2014. Functional characterization of a StyS sensor kinase reveals distinct domains associated with intracellular and extracellular sensing of styrene in P. putida CA-3. Bioengineered 5:114–122.
    112.
    Sheldon RA, Van Bekkum H. 2008. Fine chemicals through heterogeneous catalysis. John Wiley & Sons, Hoboken, NJ.
    113.
    O’Leary ND, O’Connor KE, Ward P, Goff M, Dobson AD. 2005. Genetic characterization of accumulation of polyhydroxyalkanoate from styrene in Pseudomonas putida CA-3. Appl Environ Microbiol 71:4380–4387.
    114.
    Ward PG, Goff M, Donner M, Kaminsky W, O’Connor KE. 2006. A two step chemo-biotechnological conversion of polystyrene to a biodegradable thermoplastic. Environ Sci Technol 40:2433–2437.
    115.
    Savoldelli J, Tomback D, Savoldelli H. 2017. Breaking down polystyrene through the application of a two-step thermal degradation and bacterial method to produce usable byproducts. Waste Manage 60:123–126.
    116.
    Fischer I, Schmitt WF, Porth H, Allsopp MW, Vianello G. 2014. Poly(vinyl chloride). In Ullmann’s encyclopedia of industrial chemistry. Wiley‐VCH, Weinheim, Germany.
    117.
    Karger-Kocsis J, Bárány T. 2019. Polypropylene handbook. Springer Nature Switzerland, Basel, Switzerland.
    118.
    Cacciari I, Quatrini P, Zirletta G, Mincione E, Vinciguerra V, Lupattelli P, Giovannozzi Sermanni G. 1993. Isotactic polypropylene biodegradation by a microbial community: physicochemical characterization of metabolites produced. Appl Environ Microbiol 59:3695–3700.
    119.
    Iakovlev VV, Guelcher SA, Bendavid R. 2017. Degradation of polypropylene in vivo: a microscopic analysis of meshes explanted from patients. J Biomed Mater Res B Appl Biomater 105:237–248.
    120.
    Bombelli P, Howe CJ, Bertocchini F. 2017. Polyethylene bio-degradation by caterpillars of the wax moth Galleria mellonella. Curr Biol 27:R292–R293.
    121.
    Weber C, Pusch S, Opatz T. 2017. Polyethylene bio-degradation by caterpillars? Curr Biol 27:R744–R745.
    122.
    Yang Y, Chen J, Wu W-M, Zhao J, Yang J. 2015. Complete genome sequence of Bacillus sp. YP1, a polyethylene-degrading bacterium from waxworm’s gut. J Biotechnol 200:77–78.
    123.
    Brandon AM, Gao S-H, Tian R, Ning D, Yang S-S, Zhou J, Wu W-M, Criddle CS. 2018. Biodegradation of polyethylene and plastic mixtures in mealworms (larvae of Tenebrio molitor) and effects on the gut microbiome. Environ Sci Technol 52:6526–6533.
    124.
    Notredame C, Higgins DG, Heringa J. 2000. T-Coffee: a novel method for fast and accurate multiple sequence alignment. J Mol Biol 302:205–217.
    125.
    Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. 2013. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30:2725–2729.

    Information & Contributors

    Information

    Published In

    Applied and Environmental Microbiology
    Volume 85Number 191 October 2019
    eLocator: e01095-19
    Editor: Harold L. Drake, University of Bayreuth
    PubMed: 31324632

    History

    Published online: 17 September 2019

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    KEYWORDS

    1. PET
    2. cutinase
    3. microbial plastic degradation
    4. polyamides
    5. polyethylene
    6. polyethylene terephthalate
    7. polypropylene
    8. polystyrene
    9. polyurethane
    10. polyvinylchloride

    Contributors

    Authors

    Department of Microbiology and Biotechnology, University of Hamburg, Hamburg, Germany
    Department of Microbiology and Biotechnology, University of Hamburg, Hamburg, Germany
    Department of Microbiology and Biotechnology, University of Hamburg, Hamburg, Germany

    Editor

    Harold L. Drake
    Editor
    University of Bayreuth

    Notes

    Address correspondence to Wolfgang R. Streit, [email protected].

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  • Applied and Environmental MicrobiologyArticle
    Introducing mothur: Open-Source, Platform-Independent, Community-Supported Software for Describing and Comparing Microbial Communities

    Introducing mothur: Open-Source, Platform-Independent, Community-Supported Software for Describing and Comparing Microbial Communities

    ABSTRACT

    mothur aims to be a comprehensive software package that allows users to use a single piece of software to analyze community sequence data. It builds upon previous tools to provide a flexible and powerful software package for analyzing sequencing data. As a case study, we used mothur to trim, screen, and align sequences; calculate distances; assign sequences to operational taxonomic units; and describe the α and β diversity of eight marine samples previously characterized by pyrosequencing of 16S rRNA gene fragments. This analysis of more than 222,000 sequences was completed in less than 2 h with a laptop computer.

    REFERENCES

    1.
    Antonopoulos, D. A., S. M. Huse, H. G. Morrison, T. M. Schmidt, M. L. Sogin, and V. B. Young.2009. Reproducible community dynamics of the gastrointestinal microbiota following antibiotic perturbation. Infect. Immun.77:2367-2375.
    2.
    Borneman, J.1999. Culture-independent identification of microorganisms that respond to specified stimuli. Appl. Environ. Microbiol.65:3398-3400.
    3.
    Cole, J. R., Q. Wang, E. Cardenas, J. Fish, B. Chai, et al.2009. The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res.37:D141-D145.
    4.
    DeSantis, T. Z., P. Hugenholtz, N. Larsen, M. Rojas, E. L. Brodie, K. Keller, T. Huber, D. Dalevi, P. Hu, and G. L. Andersen.2006. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl. Environ. Microbiol.72:5069-5072.
    5.
    DeSantis, T. Z., Jr., P. Hugenholtz, K. Keller, E. L. Brodie, N. Larsen, et al.2006. NAST: a multiple sequence alignment server for comparative analysis of 16S rRNA genes. Nucleic Acids Res.34:W394-W939.
    6.
    Felsenstein, J.1989. PHYLIP—Phylogeny Inference Package. Cladistics5:164-166.
    7.
    Gamma, E., R. Helm, R. Johnson, and J. M. Vlissides.1995. Design patterns: elements of reusable object-oriented software. Addison-Wesley, Reading, MA.
    8.
    Hall, J. R., K. R. Mitchell, O. Jackson-Weaver, A. S. Kooser, B. R. Cron, L. J. Crossey, and C. D. Takacs-Vesbach.2008. Molecular characterization of the diversity and distribution of a thermal spring microbial community by using rRNA and metabolic genes. Appl. Environ. Microbiol.74:4910-4922.
    9.
    Hartmann, M., and F. Widmer.2006. Community structure analyses are more sensitive to differences in soil bacterial communities than anonymous diversity indices. Appl. Environ. Microbiol.72:7804-7812.
    10.
    Li, W., and A. Godzik.2006. CD-HIT: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics22:1658-1659.
    11.
    Lozupone, C., M. Hamady, and R. Knight.2006. UniFrac—an online tool for comparing microbial community diversity in a phylogenetic context. BMC Bioinformatics7:371.
    12.
    Lozupone, C., and R. Knight.2005. UniFrac: a new phylogenetic method for comparing microbial communities. Appl. Environ. Microbiol.71:8228-8235.
    13.
    Ludwig, W., O. Strunk, R. Westram, L. Richter, H. Meier, et al.2004. ARB: a software environment for sequence data. Nucleic Acids Res.32:1363-1371.
    14.
    Maddison, W. P., and M. Slatkin.1991. Null models for the number of evolutionary steps in a character on a phylogenetic tree. Evolution45:1184-1197.
    15.
    Martin, A. P.2002. Phylogenetic approaches for describing and comparing the diversity of microbial communities. Appl. Environ. Microbiol.68:3673-3682.
    16.
    McCaig, A. E., L. A. Glover, and J. I. Prosser.1999. Molecular analysis of bacterial community structure and diversity in unimproved and improved upland grass pastures. Appl. Environ. Microbiol.65:1721-1730.
    17.
    McConnell, S.2004. Code complete, 2nd ed. Microsoft Press, Redmond, WA.
    18.
    Pace, N. R., D. A. Stahl, D. J. Lane, and G. J. Olsen.1985. Analyzing natural microbial populations by rRNA sequences. ASM News51:4-12.
    19.
    Pilone, D., and R. Miles.2008. Head first software development. O'Reilly, Sebastopol, CA.
    20.
    Pruesse, E., C. Quast, K. Knittel, B. M. Fuchs, W. Ludwig, et al.2007. SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res.35:7188-7196.
    21.
    Schloss, P. D.2008. Evaluating different approaches that test whether microbial communities have the same structure. ISME J.2:265-275.
    22.
    Schloss, P. D., and J. Handelsman.2005. Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl. Environ. Microbiol.71:1501-1506.
    23.
    Schloss, P. D., and J. Handelsman.2006. Introducing SONS, a tool that compares the membership of microbial communities. Appl. Environ. Microbiol.72:6773-6779.
    24.
    Schloss, P. D., and J. Handelsman.2006. Introducing TreeClimber, a test to compare microbial community structure. Appl. Environ. Microbiol.72:2379-2384.
    25.
    Schloss, P. D., B. R. Larget, and J. Handelsman.2004. Integration of microbial ecology and statistics: a test to compare gene libraries. Appl. Environ. Microbiol.70:5485-5492.
    26.
    Singleton, D. R., M. A. Furlong, S. L. Rathbun, and W. B. Whitman.2001. Quantitative comparisons of 16S rRNA gene sequence libraries from environmental samples. Appl. Environ. Microbiol.67:4374-4376.
    27.
    Sogin, M. L., H. G. Morrison, J. A. Huber, D. M. Welch, S. M. Huse, et al.2006. Microbial diversity in the deep sea and the underexplored “rare biosphere.” Proc. Natl. Acad. Sci. USA103:12115-12120.
    28.
    Turnbaugh, P. J., M. Hamady, T. Yatsunenko, B. L. Cantarel, A. Duncan, et al.2009. A core gut microbiome in obese and lean twins. Nature457:480-484.
    29.
    Turnbaugh, P. J., R. E. Ley, M. Hamady, C. M. Fraser-Liggett, R. Knight, et al.2007. The human microbiome project. Nature449:804-810.

    Information & Contributors

    Information

    Published In

    Applied and Environmental Microbiology
    Volume 75Number 231 December 2009
    Pages: 7537 - 7541
    PubMed: 19801464

    History

    Received: 30 June 2009
    Accepted: 26 September 2009
    Published online: 1 December 2009

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    Contributors

    Authors

    Patrick D. Schloss [email protected]
    Department of Microbiology, University of Massachusetts, Amherst, Massachusetts
    Department of Microbiology and Immunology, University of Michigan, Ann Arbor, Michigan
    Sarah L. Westcott
    Department of Microbiology, University of Massachusetts, Amherst, Massachusetts
    Department of Microbiology and Immunology, University of Michigan, Ann Arbor, Michigan
    Thomas Ryabin
    Department of Microbiology, University of Massachusetts, Amherst, Massachusetts
    Justine R. Hall
    Department of Biology, University of New Mexico, Albuquerque, New Mexico
    Martin Hartmann
    Department of Microbiology and Immunology, University of British Columbia, Vancouver, BC, Canada
    Emily B. Hollister
    Department of Soil and Crop Sciences, Texas A&M University, College Station, Texas
    Ryan A. Lesniewski
    Department of Soil, Water, and Climate, University of Minnesota, St. Paul, Minnesota
    Brian B. Oakley
    Department of Biological Sciences, University of Warwick, Coventry, United Kingdom
    Donovan H. Parks
    Faculty of Computer Science, Dalhousie University, Halifax, NS, Canada
    Courtney J. Robinson
    Department of Microbiology and Immunology, University of Michigan, Ann Arbor, Michigan
    Jason W. Sahl
    Environmental Science and Engineering, Colorado School of Mines, Golden, Colorado
    Blaz Stres
    Department of Animal Science, University of Ljubljana, Ljubljana, Slovenia
    Gerhard G. Thallinger
    Institute for Genomics and Bioinformatics, Graz University of Technology, Graz, Austria
    David J. Van Horn
    Department of Microbiology and Immunology, University of Michigan, Ann Arbor, Michigan
    Carolyn F. Weber
    Department of Biological Sciences, Louisiana State University, Baton Rouge, Lousiana

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  • Applied and Environmental MicrobiologyArticle
    Effects of Air Temperature and Relative Humidity on Coronavirus Survival on Surfaces

    Effects of Air Temperature and Relative Humidity on Coronavirus Survival on Surfaces

    ABSTRACT

    Assessment of the risks posed by severe acute respiratory syndrome (SARS) coronavirus (SARS-CoV) on surfaces requires data on survival of this virus on environmental surfaces and on how survival is affected by environmental variables, such as air temperature (AT) and relative humidity (RH). The use of surrogate viruses has the potential to overcome the challenges of working with SARS-CoV and to increase the available data on coronavirus survival on surfaces. Two potential surrogates were evaluated in this study; transmissible gastroenteritis virus (TGEV) and mouse hepatitis virus (MHV) were used to determine effects of AT and RH on the survival of coronaviruses on stainless steel. At 4°C, infectious virus persisted for as long as 28 days, and the lowest level of inactivation occurred at 20% RH. Inactivation was more rapid at 20°C than at 4°C at all humidity levels; the viruses persisted for 5 to 28 days, and the slowest inactivation occurred at low RH. Both viruses were inactivated more rapidly at 40°C than at 20°C. The relationship between inactivation and RH was not monotonic, and there was greater survival or a greater protective effect at low RH (20%) and high RH (80%) than at moderate RH (50%). There was also evidence of an interaction between AT and RH. The results show that when high numbers of viruses are deposited, TGEV and MHV may survive for days on surfaces at ATs and RHs typical of indoor environments. TGEV and MHV could serve as conservative surrogates for modeling exposure, the risk of transmission, and control measures for pathogenic enveloped viruses, such as SARS-CoV and influenza virus, on health care surfaces.

    REFERENCES

    1.
    Abad, F., R. Pinto, and A. Bosch.1994. Survival of enteric viruses on environmental fomites. Appl. Environ. Microbiol.60:3704-3710.
    2.
    Reference deleted.
    3.
    Bean, B., B. Moore, B. Sterner, L. Peterson, D. Gerding, and H. Balfour, Jr.1982. Survival of influenza viruses on environmental surfaces. J. Infect. Dis.146:47-51.
    4.
    Blachere, F., W. Lindsley, T. Pearce, S. Anderson, M. Fisher, R. Khakoo, B. Meade, O. Lander, S. Davis, and R. Thewlis.2009. Measurement of airborne influenza virus in a hospital emergency department. Clin. Infect. Dis.48:438-440.
    5.
    Reference deleted.
    6.
    Booth, T., B. Kournikakis, N. Bastien, J. Ho, D. Kobasa, L. Stadnyk, Y. Li, M. Spence, S. Paton, and B. Henry.2005. Detection of airborne severe acute respiratory syndrome (SARS) coronavirus and environmental contamination in SARS outbreak units. J. Infect. Dis.191:1472-1477.
    7.
    Casanova, L., W. Rutala, D. Weber, and M. Sobsey.2009. Survival of surrogate coronaviruses in water. Water Res.43:1893-1898.
    8.
    Chu, C., V. Cheng, I. Hung, K. Chan, B. Tang, T. Tsang, K. Chan, and K. Yuen.2005. Viral load distribution in SARS outbreak. Emerg. Infect. Dis.11:1882-1886.
    9.
    Cox, C.1993. Roles of water molecules in bacteria and viruses. Origins Life Evol. Biosph.23:29-36.
    10.
    Dowell, S., J. Simmerman, D. Erdman, J. Wu, A. Chaovavanich, M. Javadi, J. Yang, L. Anderson, S. Tong, and M. Ho.2004. Severe acute respiratory syndrome coronavirus on hospital surfaces. Clin. Infect. Dis.39:652-657.
    11.
    Harper, G.1961. Airborne micro-organisms: survival tests with four viruses. J. Hyg.59:479-486.
    12.
    Harper, G.1963. The influence of environment on the survival of airborne virus particles in the laboratory. Arch. Virol.13:64-71.
    13.
    Hemmes, J., K. C. Winkler, and S. M. Kool.1960. Virus survival as a seasonal factor in influenza and poliomyelitis. Nature188:430-431.
    14.
    Hung, I. F., V. C. Cheng, A. K. Wu, B. S. Tang, K. H. Chan, C. M. Chu, M. M. Wong, W. T. Hui, L. L. Poon, D. M. Tse, K. S. Chan, P. C. Woo, S. K. Lau, J. S. Peiris, and K. Y. Yuen.2004. Viral loads in clinical specimens and SARS manifestations. Emerg. Infect. Dis.10:1550-1557.
    15.
    Ijaz, M., A. Brunner, S. Sattar, R. Nair, and C. Johnson-Lussenburg.1985. Survival characteristics of airborne human coronavirus 229E. J. Gen. Virol.66:2743-2748.
    16.
    Jackwood, M. W.2006. The relationship of severe acute respiratory syndrome coronavirus with avian and other coronaviruses. Avian Dis.50:315-320.
    17.
    Kim, S., M. Ramakrishnan, P. Raynor, and S. Goyal.2007. Effects of humidity and other factors on the generation and sampling of a coronavirus aerosol. Aerobiologia23:239-248.
    18.
    Reference deleted.
    19.
    Mbithi, J., V. Springthorpe, and S. Sattar.1991. Effect of relative humidity and air temperature on survival of hepatitis A virus on environmental surfaces. Appl. Environ. Microbiol.57:1394-1399.
    20.
    McDonald, L., A. Simor, S. IhJen, S. Maloney, M. Ofner, C. KowTong, J. Lando, A. McGeer, L. MinLing, and D. Jernigan.2004. SARS in healthcare facilities, Toronto and Taiwan. Emerg. Infect. Dis.10:777-781.
    21.
    Noyce, J., H. Michels, and C. Keevil.2007. Inactivation of influenza A virus on copper versus stainless steel surfaces? Appl. Environ. Microbiol.73:2748-2750.
    22.
    Peiris, J., S. Lai, L. Poon, Y. Guan, L. Yam, W. Lim, J. Nicholls, W. Yee, W. Yan, and M. Cheung.2003. Coronavirus as a possible cause of severe acute respiratory syndrome. Lancet361:1319-1325.
    23.
    Rabenau, H. F., J. Cinatl, B. Morgenstern, G. Bauer, W. Preiser, and H. W. Doerr.2005. Stability and inactivation of SARS coronavirus. Med. Microbiol. Immunol.194:1-6.
    24.
    Reference deleted.
    25.
    Sattar, S.2004. Microbicides and the environmental control of nosocomial viral infections. J. Hosp. Infect.56(Suppl. 2):S64-S69.
    26.
    Schaffer, F., M. Soergel, and D. Straube.1976. Survival of airborne influenza virus: effects of propagating host, relative humidity, and composition of spray fluids. Arch. Virol.51:263-273.
    27.
    Shechmeister, I.1950. Studies on the experimental epidemiology of respiratory infections. III. Certain aspects of the behavior of type A influenza virus as an air-borne cloud. J. Infect. Dis.87:128-132.
    28.
    Sizun, J., M. Yu, and P. Talbot.2000. Survival of human coronaviruses 229E and OC43 in suspension and after drying on surfaces: a possible source of hospital-acquired infections. J. Hosp. Infect.46:55-60.
    29.
    Tennant, B., R. Gaskell, and C. Gaskell.1994. Studies on the survival of canine coronavirus under different environmental conditions. Vet. Microbiol.42:255-259.
    30.
    Thompson, S., M. Flury, M. Yates, and W. Jury.1998. Role of the air-water-solid interface in bacteriophage sorption experiments. Appl. Environ. Microbiol.64:304-309.
    31.
    Thompson, S., and M. Yates.1999. Bacteriophage inactivation at the air-water-solid interface in dynamic batch systems. Appl. Environ. Microbiol.65:1186.
    32.
    Reference deleted.
    33.
    Trouwborst, T., S. Kuyper, J. C. de Jong, and A. Plantinga.1974. Inactivation of some bacterial and animal viruses by exposure to liquid-air interfaces. J. Gen. Virol.24:155-165.
    34.
    Wong, S. C., J. K. Chan, K. C. Lee, E. S. Lo, and D. N. Tsang.2005. Development of a quantitative assay for SARS coronavirus and correlation of GAPDH mRNA with SARS coronavirus in clinical specimens. J. Clin. Pathol.58:276-280.
    35.
    World Health Organization.2003. First data on stability and resistance of SARS coronavirus compiled by members of WHO laboratory network. World Health Organization, Geneva, Switzerland. http://www.who.int/csr/sars/survival_2003_05_04/en/index.html.

    Information & Contributors

    Information

    Published In

    Applied and Environmental Microbiology
    Volume 76Number 91 May 2010
    Pages: 2712 - 2717
    PubMed: 20228108

    History

    Received: 23 September 2009
    Accepted: 26 February 2010
    Published online: 1 May 2010

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    Contributors

    Authors

    Lisa M. Casanova [email protected]
    Department of Environmental Sciences and Engineering, Gillings School of Global Public Health, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina
    Soyoung Jeon
    Department of Statistics and Operations Research, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina
    William A. Rutala
    Department of Medicine, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina
    David J. Weber
    Department of Medicine, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina
    Mark D. Sobsey
    Department of Environmental Sciences and Engineering, Gillings School of Global Public Health, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina

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  • Applied and Environmental MicrobiologyArticle
    Biodegradation of Polyester Polyurethane by Endophytic Fungi

    ABSTRACT

    Bioremediation is an important approach to waste reduction that relies on biological processes to break down a variety of pollutants. This is made possible by the vast metabolic diversity of the microbial world. To explore this diversity for the breakdown of plastic, we screened several dozen endophytic fungi for their ability to degrade the synthetic polymer polyester polyurethane (PUR). Several organisms demonstrated the ability to efficiently degrade PUR in both solid and liquid suspensions. Particularly robust activity was observed among several isolates in the genus Pestalotiopsis, although it was not a universal feature of this genus. Two Pestalotiopsis microspora isolates were uniquely able to grow on PUR as the sole carbon source under both aerobic and anaerobic conditions. Molecular characterization of this activity suggests that a serine hydrolase is responsible for degradation of PUR. The broad distribution of activity observed and the unprecedented case of anaerobic growth using PUR as the sole carbon source suggest that endophytes are a promising source of biodiversity from which to screen for metabolic properties useful for bioremediation.

    REFERENCES

    1.
    Akutsu Y., Nakajima-Kambe T., Nomura N., and Nakahara T.. 1998. Purification and properties of a polyester-polyurethane degrading enzyme from Comamonas acidovorans TB-35. Appl. Environ. Microbiol. 64:62–67.
    2.
    Allen B. A., Hilliard N. P., and Howard G. T.. 1999. Purification and characterization of a soluble polyurethane degrading enzyme from Comamonas acidovorans. Int. Biodeterior. Biodegrad. 43:37–41.
    3.
    Bacon C. and White J.. 2000. Microbial endophytes. Marcel Dekker, New York, NY.
    4.
    Cosgrove L., McGeechan P. L., Robson G. D., and Handley P. S.. 2007. Fungal communities associated with degradation of polyester polyurethane in soil. Appl. Environ. Microbiol. 73:5817–5824.
    5.
    Crabbe J. R., Campbell J. R., Thompson L., Walz S. L., and Schultz W. W.. 1994. Biodegradation of a colloidal ester-based polyurethane by soil fungi. Int. Biodeterior. Biodegrad. 33:103–113.
    6.
    Darby R. T. and Kaplan A. T.. 1968. Fungal susceptibility of polyurethanes. Appl. Microbiol. 16:900–905.
    7.
    Filip Z.. 1979. Polyurethane as the sole nutrient source for Aspergillus niger and Cladosporium herbarum. Eur. J. Appl. Microbiol. Biotechnol. 7:277–280.
    8.
    Gautam R., Bassi A. S., and Yanful E. K.. 2007. Candida rugosa lipase-catalyzed polyurethane degradation in aqueous medium. Biotechnol. Lett. 29:1081–1086.
    9.
    Hanauer D. I., Jacobs-Sera D., and Pedulla M. L.. 2006. Teaching scientific inquiry. Science 314:1880–1881.
    10.
    Howard G. T.. 2002. Biodegradation of polyurethane: a review. Int. Biodeterior. Biodegrad. 49:245–252.
    11.
    Howard G. T. and Blake R. C.. 1998. Growth of Pseudomonas fluorescens on a polyester-polyurethane and the purification and characterization of a polyurethanase-protease enzyme. Int. Biodeterior. Biodegrad. 42:213–220.
    12.
    Howard G. T. and Hilliard N. P.. 1999. Use of Coomassie blue-polyurethane interaction in screening of polyurethanase proteins and polyurethanolytic bacteria. Int. Biodeterior. Biodegrad. 43:23–30.
    13.
    Howard G. T., Ruiz C., and Hilliard N. P.. 1999. Growth of Pseudomonas chlororaphis on a polyester-polyurethane and the purification and characterization of a polyurethanase-esterase enzyme. Int. Biodeterior. Biodegrad. 43:7–12.
    14.
    Howard G. T., Vicknair J., and Mackie R. I.. 2001. Sensitive plate assay for screening and detection of bacterial polyurethanase activity. Lett. Appl. Microbiol. 32:211–214.
    15.
    Kay M. J., Morton L. H. G., and Prince E. L.. 1991. Bacterial degradation of polyester polyurethane. Int. Biodeterior. Biodegrad. 27:205–222.
    16.
    Kay M. J., McCabe R. W., and Morton L. H. G.. 1993. Chemical and physical changes occurring in polyester polyurethane during biodegradation. Int. Biodeterior. Biodegrad. 31:209–225.
    17.
    Nakajima-Kambe T., Shigeno-Akutsu Y., Nomura N., Onuma F., and Nakahara T.. 1999. Microbial degradation of polyurethane, polyester polyurethanes, and polyether polyurethanes. Appl. Microbiol. Biotechnol. 51:134–140.
    18.
    Oceguera-Cervantes A. et al. 2007. Characterization of the polyurethanolytic activity of two Alicycliphilus sp. strains able to degrade polyurethane and N-methylpyrrolidone. Appl. Environ. Microbiol. 73:6214–6223.
    19.
    Pathirana R. A. and Seal K. J.. 1984. Studies on polyurethane deteriorating fungi. Int. Biodeterior. Biodegrad. 20:163–168.
    20.
    Patricelli M. P., Giang D. K., Stamp L. M., and Burbaum J. J.. 2001. Direct visualization of serine hydrolase activities in complex proteomes using fluorescent active site-directed probes. Proteomics 1:1067–1071.
    21.
    PlasticsEurope. 1 2008. The compelling facts about plastics, an analysis of plastics production, demand and recovery for 2006 in Europe. PlasticsEurope, Brussels, Belgium. http://www.plasticsrecyclers.eu/docs/press%20release/080123CfaPpdfVersion.pdf.
    22.
    Ramirez-Coronel M. A., Viniegra-Gonzalez G., Darvill A., and Augur C.. 2003. A novel tannase from Aspergillus niger with β-glucosidase activity. Microbiology 149:2941–2946.
    23.
    Rowe L. and Howard G. T.. 2002. Growth of Bacillus subtilis on polyurethane and the purification and characterization of a polyurethanase-lipase enzyme. Int. Biodeterior. Biodegrad. 50:33–40.
    24.
    Shah A. A., Hassan F., Hameed A., and Ahmed S.. 2008. Biological degradation of plastics: a comprehensive review. Biotechnol. Adv. 26:246–265.
    25.
    Smith S. A. et al. 2008. Bioactive endophytes warrant intensified exploration and conservation. PLoS One 3:e3052.
    26.
    Stern R. V. and Howard G. T.. 2000. The polyester polyurethane gene (pueA) from Pseudomonas clororaphis encodes lipase. FEMS Microbiol. Lett. 185:163–168.
    27.
    Strobel G. et al. 1996. Taxol from Pestalotiopsis microspora, an endophytic fungus of Taxus wallachiana. Microbiology 142:435–440.
    28.
    Strobel S. A. and Strobel G.. 2007. Plant endophytes as a platform for discovery-based undergraduate science education. Nat. Chem. Biol. 3:356–359.
    29.
    Uchida J. Y.. 2004. Pestalotiopsis diseases, p. 27–28. In Elliott M. L., Broschat T. K., Uchida J. Y., and Simone G. W. (ed.), Diseases and disorders of ornamental palms. American Phytopathological Society, St. Paul, MN.
    30.
    White T. J., Bruns T., Lee S., and Taylor J. W.. 1990. Amplification and direct sequencing of fungal rRNA genes for phylogenetics, p. 315–322. In Innis M. A., Gelfand D. H., Sninsky J. J., and White T. J. (ed.), PCR protocols: a guide to methods and applications. Academic Press, Inc., New York, NY.

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    Information

    Published In

    Applied and Environmental Microbiology
    Volume 77Number 171 September 2011
    Pages: 6076 - 6084
    PubMed: 21764951

    History

    Received: 7 March 2011
    Accepted: 21 June 2011
    Published online: 24 August 2011

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    Authors

    Jonathan R. Russell
    Department of Molecular Biophysics and Biochemistry, Yale University, New Haven, Connecticut 06520
    Jeffrey Huang
    Department of Molecular Biophysics and Biochemistry, Yale University, New Haven, Connecticut 06520
    Pria Anand
    Department of Molecular Biophysics and Biochemistry, Yale University, New Haven, Connecticut 06520
    Kaury Kucera
    Department of Molecular Biophysics and Biochemistry, Yale University, New Haven, Connecticut 06520
    Amanda G. Sandoval
    Department of Molecular Biophysics and Biochemistry, Yale University, New Haven, Connecticut 06520
    Kathleen W. Dantzler
    Department of Molecular Biophysics and Biochemistry, Yale University, New Haven, Connecticut 06520
    DaShawn Hickman
    Department of Molecular Biophysics and Biochemistry, Yale University, New Haven, Connecticut 06520
    Justin Jee
    Department of Molecular Biophysics and Biochemistry, Yale University, New Haven, Connecticut 06520
    Farrah M. Kimovec
    Department of Molecular Biophysics and Biochemistry, Yale University, New Haven, Connecticut 06520
    David Koppstein
    Department of Molecular Biophysics and Biochemistry, Yale University, New Haven, Connecticut 06520
    Daniel H. Marks
    Department of Molecular Biophysics and Biochemistry, Yale University, New Haven, Connecticut 06520
    Paul A. Mittermiller
    Department of Molecular Biophysics and Biochemistry, Yale University, New Haven, Connecticut 06520
    Salvador Joel Núñez
    Department of Molecular Biophysics and Biochemistry, Yale University, New Haven, Connecticut 06520
    Marina Santiago
    Department of Molecular Biophysics and Biochemistry, Yale University, New Haven, Connecticut 06520
    Maria A. Townes
    Department of Molecular Biophysics and Biochemistry, Yale University, New Haven, Connecticut 06520
    Michael Vishnevetsky
    Department of Molecular Biophysics and Biochemistry, Yale University, New Haven, Connecticut 06520
    Neely E. Williams
    Department of Molecular Biophysics and Biochemistry, Yale University, New Haven, Connecticut 06520
    Mario Percy Núñez Vargas
    Universidad Nacional San Antõnio Abad del Cusco, Peru Escuela Post Grado, Facultad de Biologia, Andes Amazon Guianas Herbario Vargas (CUZ), Cusco, Peru
    Lori-Ann Boulanger
    Department of Molecular Biophysics and Biochemistry, Yale University, New Haven, Connecticut 06520
    Carol Bascom-Slack
    Department of Molecular Biophysics and Biochemistry, Yale University, New Haven, Connecticut 06520
    Scott A. Strobel [email protected]
    Department of Molecular Biophysics and Biochemistry, Yale University, New Haven, Connecticut 06520

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    Naïve Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy

    Naïve Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy

    ABSTRACT

    The Ribosomal Database Project (RDP) Classifier, a naïve Bayesian classifier, can rapidly and accurately classify bacterial 16S rRNA sequences into the new higher-order taxonomy proposed in Bergey's Taxonomic Outline of the Prokaryotes (2nd ed., release 5.0, Springer-Verlag, New York, NY, 2004). It provides taxonomic assignments from domain to genus, with confidence estimates for each assignment. The majority of classifications (98%) were of high estimated confidence (≥95%) and high accuracy (98%). In addition to being tested with the corpus of 5,014 type strain sequences from Bergey's outline, the RDP Classifier was tested with a corpus of 23,095 rRNA sequences as assigned by the NCBI into their alternative higher-order taxonomy. The results from leave-one-out testing on both corpora show that the overall accuracies at all levels of confidence for near-full-length and 400-base segments were 89% or above down to the genus level, and the majority of the classification errors appear to be due to anomalies in the current taxonomies. For shorter rRNA segments, such as those that might be generated by pyrosequencing, the error rate varied greatly over the length of the 16S rRNA gene, with segments around the V2 and V4 variable regions giving the lowest error rates. The RDP Classifier is suitable both for the analysis of single rRNA sequences and for the analysis of libraries of thousands of sequences. Another related tool, RDP Library Compare, was developed to facilitate microbial-community comparison based on 16S rRNA gene sequence libraries. It combines the RDP Classifier with a statistical test to flag taxa differentially represented between samples. The RDP Classifier and RDP Library Compare are available online at http://rdp.cme.msu.edu/.

    REFERENCES

    1.
    Ash, C., J. A. E. Farrow, S. Wallbanks, and M. D. Collins.1991. Phylogenetic heterogeneity of the genus bacillus revealed by comparative analysis of small subunit ribosomal RNA sequences. Lett. Appl. Microbiol.13:202-206.
    2.
    Audic, S., and J. M. Claverie.1997. The significance of digital gene expression profiles. Genome Res.7:986-995.
    3.
    Benson, D. A., I. Karsch-Mizrachi, D. J. Lipman, J. Ostell, B. A. Rapp, and D. L. Wheeler.2000. GenBank. Nucleic Acids Res.28:15-18.
    4.
    Brown, M. P. S.1999. RNA modeling using stochastic context-free grammars. Ph.D. thesis. University of California, Santa Cruz.
    5.
    Bruno, W. J., N. D. Socci, and A. L. Halpern.2000. Weighted neighbor joining: a likelihood-based approach to distance-based phylogeny reconstruction. Mol. Biol. Evol.17:189-197.
    6.
    Cannone, J. J., S. Subramanian, M. N. Schnare, J. R. Collett, L. M. D'Souza, Y. Du, B. Feng, N. Lin, L. V. Madabusi, K. M. Muller, N. Pande, Z. Shang, N. Yu, and R. R. Gutell.2002. The comparative RNA web (CRW) site: an online database of comparative sequence and structure information for ribosomal, intron, and other RNAs. BMC Bioinformatics3:2.
    7.
    Christensen, H. B.1992. Introduction to statistics: a calculus-based approach, 1st ed., p. 510-512. Harcourt Brace Jovanovich, Inc., Orlando, FL.
    8.
    Cole, J. R., B. Chai, R. J. Farris, Q. Wang, S. A. Kulam, D. M. McGarrell, G. M. Garrity, and J. M. Tiedje.2005. The Ribosomal Database Project (RDP-II): sequences and tools for high-throughput rRNA analysis. Nucleic Acids Res.33:D294-D296.
    9.
    Connor, C. J., H. Luo, B. B. M. Gardener, and H. H. Wang.2005. Development of a real-time PCR-based system targeting the 16S rRNA gene sequence for rapid detection of Alicyclobacillus spp. in juice products. Int. J. Food Microbiol.99:229-235.
    10.
    DeSantis, T. Z., I. Dubosarskiy, S. R. Murray, and G. L. Andersen.2003. Comprehensive aligned sequence construction for automated design of effective probes (CASCADE-P) using 16S rDNA. Bioinformatics19:1461-1468.
    11.
    Domingos, P., and M. Pazzani.1997. On the optimality of the simple Bayesian classifier under zero-one loss. Machine Learning29:103-130.
    12.
    Garrity, G. M., J. A. Bell, and D. B. Searles.2001. Taxonomic outline of the prokaryotes. Bergey's manual of systematic bacteriology, 2nd ed., release 1.0. Springer-Verlag, New York, NY.
    13.
    Garrity, G. M., J. A. Bell, and T. G. Lilburn.2004. Taxonomic outline of the procaryotes. Bergey's manual of systematic bacteriology, 2nd ed., release 5.0. Springer-Verlag, New York, NY.
    14.
    Karavaiko, G. I., T. I. Bogdanova, T. P. Tourova, T. F. Kondrat′eva, I. A. Tsaplina, M. A. Egorova, E. N. Krasil'nikova, and L. M. Zakharchuk.2005. Reclassification of ‘Sulfobacillus thermosulfidooxidans subsp. thermotolerans’ strain K1 as Alicyclobacillus tolerans sp. nov. and Sulfobacillus disulfidooxidans Dufresne et al. 1996 as Alicyclobacillus disulfidooxidans comb. nov., and emended description of the genus Alicyclobacillus. Int. J. Syst. Evol. Microbiol.55:941-947.
    15.
    Karavaĭko, G. I., T. P. Turova, I. A. Tsaplina, and T. I. Bogdanova.2000. The phylogenetic position of aerobic, moderately thermophilic bacteria of the Sulfobacillus species, oxidizing Fe2+, S0 and sulfide minerals. Mikrobiologiia69:857-860.
    16.
    Li, Y. H., and A. K. Jain.1998. Classification of text documents. Comput. J.41:537-546.
    17.
    Lozupone, C., and R. Knight.2005. UniFrac: a new phylogenetic method for comparing microbial communities. Appl. Environ. Microbiol.71:8228-8235.
    18.
    Maidak, B. L., N. Larsen, M. J. McCaughey, R. Overbeek, G. J. Olsen, K. Fogel, J. Blandy, and C. R. Woese.1994. The Ribosomal Database Project. Nucleic Acids Res.22:3485-3487.
    19.
    Martin, A. P.2002. Phylogenetic approaches for describing and comparing the diversity of microbial communities. Appl. Environ. Microbiol.68:3673-3682.
    20.
    Neefs, J. M., Y. Van de Peer, P. De Rijk, S. Chapelle, and R. De Wachter.1993. Compilation of small ribosomal subunit RNA structures. Nucleic Acids Res.21:3025-3049.
    21.
    Sandberg, R., G. Winberg, C. I. Branden, A. Kaske, I. Ernberg, and J. Coster.2001. Capturing whole-genome characteristics in short sequences using a naive Bayesian classifier. Genome Res.11:1404-1409.
    22.
    Singleton, D. R., M. A. Furlong, S. L. Rathbun, and W. B. Whitman.2001. Quantitative comparisons of 16S rRNA gene sequence libraries from environmental samples. Appl. Environ. Microbiol.67:4374-4376.
    23.
    Sogin, M. L., H. G. Morrison, J. A. Huber, D. M. Welch, S. M. Huse, P. R. Neal, J. M. Arrieta, and G. J. Herndl.2006. Microbial diversity in the deep sea and the underexplored “rare biosphere.” Proc. Natl. Acad. Sci. USA103:12115-12120.
    24.
    Stackebrandt, E., W. Frederiksen, G. M. Garrity, P. A. D. Grimont, P. Kämpfer, M. C. J. Maiden, X. Nesme, R. Rosselló-Mora, J. Swings, H. G. Trüper, L. Vauterin, A. C. Ward, and W. B. Whitman.2002. Report of the ad hoc committee for the re-evaluation of the species definition in bacteriology. Int. J. Syst. Evol. Microbiol.52:1043-1047.
    25.
    Turova, T. P., A. B. Poltoraus, I. A. Lebedeva, E. S. Bulygina, I. A. Tsaplina, T. I. Bogdanova, and G. I. Karavaiko.1995. Determination of the phylogenetic position of Sulfobacillus thermosulfidooxidans on the basis of analysis of the 5S and 16S ribosomal RNA. Mikrobiologiia64:366-374.
    26.
    Wheeler, D. L., C. Chappey, A. E. Lash, D. D. Leipe, T. L. Madden, G. D. Schuler, T. A. Tatusova, and B. A. Rapp.2000. Database resources of the National Center for Biotechnology Information. Nucleic Acids Res.28:10-14.
    27.
    Wisotzkey, J. D., P. Jurtshuk, G. E. Fox, G. Deinhard, and K. Poralla.1992. Comparative sequence analyses on the 16S rRNA (rDNA) of Bacillus acidocaldarius,Bacillus acidoterrestris, and Bacillus cycloheptanicus and proposal for creation of a new genus, Alicyclobacillus gen. nov. Int. J. Syst. Bacteriol.42:263-269.
    28.
    Woese, C. R., O. Kandler, and M. L. Wheelis.1990. Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc. Natl. Acad. Sci. USA87:4576-4579.

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    Published In

    Applied and Environmental Microbiology
    Volume 73Number 1615 August 2007
    Pages: 5261 - 5267
    PubMed: 17586664

    History

    Received: 10 January 2007
    Accepted: 18 June 2007
    Published online: 15 August 2007

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    Contributors

    Authors

    Qiong Wang
    Center for Microbial Ecology
    George M. Garrity
    Center for Microbial Ecology
    Department of Microbiology and Molecular Genetics, Michigan State University, East Lansing, Michigan 48824
    James M. Tiedje
    Center for Microbial Ecology
    Department of Microbiology and Molecular Genetics, Michigan State University, East Lansing, Michigan 48824
    James R. Cole [email protected]
    Center for Microbial Ecology

    Notes

    Supplemental material for this article may be found at http://aem.asm.org/.

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    Development of a Dual-Index Sequencing Strategy and Curation Pipeline for Analyzing Amplicon Sequence Data on the MiSeq Illumina Sequencing Platform

    Development of a Dual-Index Sequencing Strategy and Curation Pipeline for Analyzing Amplicon Sequence Data on the MiSeq Illumina Sequencing Platform

    ABSTRACT

    Rapid advances in sequencing technology have changed the experimental landscape of microbial ecology. In the last 10 years, the field has moved from sequencing hundreds of 16S rRNA gene fragments per study using clone libraries to the sequencing of millions of fragments per study using next-generation sequencing technologies from 454 and Illumina. As these technologies advance, it is critical to assess the strengths, weaknesses, and overall suitability of these platforms for the interrogation of microbial communities. Here, we present an improved method for sequencing variable regions within the 16S rRNA gene using Illumina's MiSeq platform, which is currently capable of producing paired 250-nucleotide reads. We evaluated three overlapping regions of the 16S rRNA gene that vary in length (i.e., V34, V4, and V45) by resequencing a mock community and natural samples from human feces, mouse feces, and soil. By titrating the concentration of 16S rRNA gene amplicons applied to the flow cell and using a quality score-based approach to correct discrepancies between reads used to construct contigs, we were able to reduce error rates by as much as two orders of magnitude. Finally, we reprocessed samples from a previous study to demonstrate that large numbers of samples could be multiplexed and sequenced in parallel with shotgun metagenomes. These analyses demonstrate that our approach can provide data that are at least as good as that generated by the 454 platform while providing considerably higher sequencing coverage for a fraction of the cost.

    REFERENCES

    1.
    Hugenholtz P, Pitulle C, Hershberger KL, and Pace NR. 1998. Novel division level bacterial diversity in a Yellowstone hot spring. J. Bacteriol. 180:366–376.
    2.
    The Human Microbiome Consortium. 2012. Structure, function and diversity of the healthy human microbiome. Nature 486:207–214.
    3.
    Sogin ML, Morrison HG, Huber JA, Welch DM, Huse SM, Neal PR, Arrieta JM, and Herndl GJ. 2006. Microbial diversity in the deep sea and the underexplored “rare biosphere.”. Proc. Natl. Acad. Sci. U. S. A. 103:12115–12120.
    4.
    Junemann S, Prior K, Szczepanowski R, Harks I, Ehmke B, Goesmann A, Stoye J, and Harmsen D. 2012. Bacterial community shift in treated periodontitis patients revealed by Ion Torrent 16S rRNA gene amplicon sequencing. PLoS One 7:e41606.
    5.
    Fichot EB and Norman RS. 2013. Microbial phylogenetic profiling with the Pacific Biosciences sequencing platform. Microbiome 1:10.
    6.
    Gloor GB, Hummelen R, Macklaim JM, Dickson RJ, Fernandes AD, MacPhee R, and Reid G. 2010. Microbiome profiling by Illumina sequencing of combinatorial sequence-tagged PCR products. PLoS One 5:e15406.
    7.
    Huse SM, Welch DM, Morrison HG, and Sogin ML. 2010. Ironing out the wrinkles in the rare biosphere through improved OTU clustering. Environ. Microbiol. 12:1889–1898.
    8.
    Kunin V, Engelbrektson A, Ochman H, and Hugenholtz P. 2010. Wrinkles in the rare biosphere: pyrosequencing errors can lead to artificial inflation of diversity estimates. Environ. Microbiol. 12:118–123.
    9.
    Quince C, Lanzen A, Davenport RJ, and Turnbaugh PJ. 2011. Removing noise from pyrosequenced amplicons. BMC Bioinformatics 12:38.
    10.
    Schloss PD, Gevers D, and Westcott SL. 2011. Reducing the effects of PCR amplification and sequencing artifacts on 16S rRNA-based studies. PLoS One 6:e27310.
    11.
    Wang Q, Garrity GM, Tiedje JM, and Cole JR. 2007. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 73:5261–5267.
    12.
    Bentley DR, Balasubramanian S, Swerdlow HP, Smith GP, Milton J, Brown CG, Hall KP, Evers DJ, Barnes CL, Bignell HR, Boutell JM, Bryant J, Carter RJ, Keira Cheetham R, Cox AJ, Ellis DJ, Flatbush MR, Gormley NA, Humphray SJ, Irving LJ, Karbelashvili MS, Kirk SM, Li H, Liu X, Maisinger KS, Murray LJ, Obradovic B, Ost T, Parkinson ML, Pratt MR, Rasolonjatovo IM, Reed MT, Rigatti R, Rodighiero C, Ross MT, Sabot A, Sankar SV, Scally A, Schroth GP, Smith ME, Smith VP, Spiridou A, Torrance PE, Tzonev SS, et al. 2008. Accurate whole human genome sequencing using reversible terminator chemistry. Nature 456:53–59.
    13.
    Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, Owens SM, Betley J, Fraser L, Bauer M, Gormley N, Gilbert JA, Smith G, and Knight R. 2012. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J. 6:1621–1624.
    14.
    Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, Fierer N, and Knight R. 2011. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc. Natl. Acad. Sci. U. S. A. 108(Suppl. 1):4516–4522.
    15.
    Werner JJ, Zhou D, Caporaso JG, Knight R, and Angenent LT. 2012. Comparison of Illumina paired-end and single-direction sequencing for microbial 16S rRNA gene amplicon surveys. ISME J. 6:1273–1276.
    16.
    Bokulich NA, Subramanian S, Faith JJ, Gevers D, Gordon JI, Knight R, Mills DA, and Caporaso JG. 2013. Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nat. Methods 10:57–59.
    17.
    Masella AP, Bartram AK, Truszkowski JM, Brown DG, and Neufeld JD. 2012. PANDAseq: paired-end assembler for Illumina sequences. BMC Bioinformatics 13:31.
    18.
    Schloss PD, Schubert AM, Zackular JP, Iverson KD, Young VB, and Petrosino JF. 2012. Stabilization of the murine gut microbiome following weaning. Gut Microbes 3:383–393.
    19.
    Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J, and Glockner FO. 2007. SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res. 35:7188–7196.
    20.
    Haas BJ, Gevers D, Earl AM, Feldgarden M, Ward DV, Giannoukos G, Ciulla D, Tabbaa D, Highlander SK, Sodergren E, Methé B, DeSantis TZ, Human Microbiome Consortium, Petrosino JF, Knight R, and Birren BW. 2011. Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Res. 21:494–504.
    21.
    Simpson JT, Wong K, Jackman SD, Schein JE, Jones SJ, and Birol I. 2009. ABySS: a parallel assembler for short read sequence data. Genome Res. 19:1117–1123.
    22.
    Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, and Weber CF. 2009. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75:7537–7541.
    23.
    Schloss PD. 2010. The effects of alignment quality, distance calculation method, sequence filtering, and region on the analysis of 16S rRNA gene-based studies. PLoS Comput. Biol. 6:e1000844.
    24.
    Schloss PD. 2009. A high-throughput DNA sequence aligner for microbial ecology studies. PLoS One 4:e8230.
    25.
    Schloss PD. 2013. Secondary structure improves OTU assignments of 16S rRNA gene sequences. ISME J. 7:457–460.
    26.
    Edgar RC, Haas BJ, Clemente JC, Quince C, and Knight R. 2011. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200.
    27.
    Schloss PD and Westcott SL. 2011. Assessing and improving methods used in operational taxonomic unit-based approaches for 16S rRNA gene sequence analysis. Appl. Environ. Microbiol. 77:3219–3226.
    28.
    Yue JC and Clayton MK. 2005. A similarity measure based on species proportions. Commun. Stat. Theory Methods 34:2123–2131.

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    Information

    Published In

    Applied and Environmental Microbiology
    Volume 79Number 171 September 2013
    Pages: 5112 - 5120
    PubMed: 23793624

    History

    Received: 1 April 2013
    Accepted: 13 June 2013
    Published online: 7 August 2013

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    Authors

    James J. Kozich
    Department of Microbiology and Immunology, University of Michigan, Ann Arbor, Michigan, USA
    Sarah L. Westcott
    Department of Microbiology and Immunology, University of Michigan, Ann Arbor, Michigan, USA
    Nielson T. Baxter
    Department of Microbiology and Immunology, University of Michigan, Ann Arbor, Michigan, USA
    Sarah K. Highlander
    Department of Molecular Virology and Microbiology, Baylor College of Medicine, Houston, Texas, USA
    Patrick D. Schloss
    Department of Microbiology and Immunology, University of Michigan, Ann Arbor, Michigan, USA

    Notes

    Address correspondence to Patrick D. Schloss, [email protected].

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  • Applied and Environmental MicrobiologyArticle
    Multigene Editing in the Escherichia coli Genome via the CRISPR-Cas9 System

    Multigene Editing in the Escherichia coli Genome via the CRISPR-Cas9 System

    ABSTRACT

    An efficient genome-scale editing tool is required for construction of industrially useful microbes. We describe a targeted, continual multigene editing strategy that was applied to the Escherichia coli genome by using the Streptococcus pyogenes type II CRISPR-Cas9 system to realize a variety of precise genome modifications, including gene deletion and insertion, with a highest efficiency of 100%, which was able to achieve simultaneous multigene editing of up to three targets. The system also demonstrated successful targeted chromosomal deletions in Tatumella citrea, another species of the Enterobacteriaceae, with highest efficiency of 100%.

    REFERENCES

    1.
    Ingram LO, Gomez PF, Lai X, Moniruzzaman M, Wood BE, Yomano LP, York SW. 1998. Metabolic engineering of bacteria for ethanol production. Biotechnol Bioeng 58:204–214.
    2.
    Atsumi S, Hanai T, Liao JC. 2008. Non-fermentative pathways for synthesis of branched-chain higher alcohols as biofuels. Nature 451:86–89.
    3.
    Steen EJ, Kang Y, Bokinsky G, Hu Z, Schirmer A, McClure A, Del Cardayre SB, Keasling JD. 2010. Microbial production of fatty-acid-derived fuels and chemicals from plant biomass. Nature 463:559–562.
    4.
    Leuchtenberger W, Huthmacher K, Drauz K. 2005. Biotechnological production of amino acids and derivatives: current status and prospects. Appl Microbiol Biotechnol 69:1–8.
    5.
    Bongaerts J, Kramer M, Muller U, Raeven L, Wubbolts M. 2001. Metabolic engineering for microbial production of aromatic amino acids and derived compounds. Metab Eng 3:289–300.
    6.
    Martin VJ, Pitera DJ, Withers ST, Newman JD, Keasling JD. 2003. Engineering a mevalonate pathway in Escherichia coli for production of terpenoids. Nat Biotechnol 21:796–802.
    7.
    McDaniel R, Thamchaipenet A, Gustafsson C, Fu H, Betlach M, Ashley G. 1999. Multiple genetic modifications of the erythromycin polyketide synthase to produce a library of novel “unnatural” natural products. Proc Natl Acad Sci U S A 96:1846–1851.
    8.
    Yim H, Haselbeck R, Niu W, Pujol-Baxley C, Burgard A, Boldt J, Khandurina J, Trawick JD, Osterhout RE, Stephen R, Estadilla J, Teisan S, Schreyer HB, Andrae S, Yang TH, Lee SY, Burk MJ, Van Dien S. 2011. Metabolic engineering of Escherichia coli for direct production of 1,4-butanediol. Nat Chem Biol 7:445–452.
    9.
    Nakamura CE, Whited GM. 2003. Metabolic engineering for the microbial production of 1,3-propanediol. Curr Opin Biotechnol 14:454–459.
    10.
    Esvelt KM, Wang HH. 2013. Genome-scale engineering for systems and synthetic biology. Mol Syst Biol 9:641.
    11.
    Enyeart PJ, Chirieleison SM, Dao MN, Perutka J, Quandt EM, Yao J, Whitt JT, Keatinge-Clay AT, Lambowitz AM, Ellington AD. 2013. Generalized bacterial genome editing using mobile group II introns and Cre-lox. Mol Syst Biol 9:685.
    12.
    Yu BJ, Kang KH, Lee JH, Sung BH, Kim MS, Kim SC. 2008. Rapid and efficient construction of markerless deletions in the Escherichia coli genome. Nucleic Acids Res 36:e84.
    13.
    Datsenko KA, Wanner BL. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 97:6640–6645.
    14.
    Yu D, Ellis HM, Lee EC, Jenkins NA, Copeland NG, Court DL. 2000. An efficient recombination system for chromosome engineering in Escherichia coli. Proc Natl Acad Sci U S A 97:5978–5983.
    15.
    Zhang Y, Buchholz F, Muyrers JP, Stewart AF. 1998. A new logic for DNA engineering using recombination in Escherichia coli. Nat Genet 20:123–128.
    16.
    Sharan SK, Thomason LC, Kuznetsov SG, Court DL. 2009. Recombineering: a homologous recombination-based method of genetic engineering. Nat Protoc 4:206–223.
    17.
    Warner JR, Reeder PJ, Karimpour-Fard A, Woodruff LB, Gill RT. 2010. Rapid profiling of a microbial genome using mixtures of barcoded oligonucleotides. Nat Biotechnol 28:856–862.
    18.
    Costantino N, Court DL. 2003. Enhanced levels of lambda Red-mediated recombinants in mismatch repair mutants. Proc Natl Acad Sci U S A 100:15748–15753.
    19.
    Posfai G, Kolisnychenko V, Bereczki Z, Blattner FR. 1999. Markerless gene replacement in Escherichia coli stimulated by a double-strand break in the chromosome. Nucleic Acids Res 27:4409–4415.
    20.
    Yang J, Sun B, Huang H, Jiang Y, Diao L, Chen B, Xu C, Wang X, Liu J, Jiang W, Yang S. 2014. High-efficiency scarless genetic modification in Escherichia coli using lambda-red recombination and I-SceI cleavage. Appl Environ Microbiol 80:3826–3834.
    21.
    Karberg M, Guo H, Zhong J, Coon R, Perutka J, Lambowitz AM. 2001. Group II introns as controllable gene targeting vectors for genetic manipulation of bacteria. Nat Biotechnol 19:1162–1167.
    22.
    Wang HH, Church GM. 2011. Multiplexed genome engineering and genotyping methods applications for synthetic biology and metabolic engineering. Methods Enzymol 498:409–426.
    23.
    Wang HH, Isaacs FJ, Carr PA, Sun ZZ, Xu G, Forest CR, Church GM. 2009. Programming cells by multiplex genome engineering and accelerated evolution. Nature 460:894–898.
    24.
    Jiang W, Bikard D, Cox D, Zhang F, Marraffini LA. 2013. RNA-guided editing of bacterial genomes using CRISPR-Cas systems. Nat Biotechnol 31:233–239.
    25.
    DiCarlo JE, Norville JE, Mali P, Rios X, Aach J, Church GM. 2013. Genome engineering in Saccharomyces cerevisiae using CRISPR-Cas systems. Nucleic Acids Res 41:4336–4343.
    26.
    Cobb RE, Wang Y, Zhao H. 8 December 2014. High-efficiency multiplex genome editing of Streptomyces species using an engineered CRISPR/Cas system. ACS Synth Biol.
    27.
    Shan Q, Wang Y, Li J, Zhang Y, Chen K, Liang Z, Zhang K, Liu J, Xi JJ, Qiu JL, Gao C. 2013. Targeted genome modification of crop plants using a CRISPR-Cas system. Nat Biotechnol 31:686–688.
    28.
    Wang Y, Li Z, Xu J, Zeng B, Ling L, You L, Chen Y, Huang Y, Tan A. 2013. The CRISPR/Cas System mediates efficient genome engineering in Bombyx mori. Cell Res 23:1414–1416.
    29.
    Yu Z, Ren M, Wang Z, Zhang B, Rong YS, Jiao R, Gao G. 2013. Highly efficient genome modifications mediated by CRISPR/Cas9 in Drosophila. Genetics 195:289–291.
    30.
    Cong L, Ran FA, Cox D, Lin S, Barretto R, Habib N, Hsu PD, Wu X, Jiang W, Marraffini LA, Zhang F. 2013. Multiplex genome engineering using CRISPR/Cas systems. Science 339:819–823.
    31.
    Mali P, Yang L, Esvelt KM, Aach J, Guell M, DiCarlo JE, Norville JE, Church GM. 2013. RNA-guided human genome engineering via Cas9. Science 339:823–826.
    32.
    Zhang Q, Rho M, Tang H, Doak TG, Ye Y. 2013. CRISPR-Cas systems target a diverse collection of invasive mobile genetic elements in human microbiomes. Genome Biol 14:R40.
    33.
    Deltcheva E, Chylinski K, Sharma CM, Gonzales K, Chao Y, Pirzada ZA, Eckert MR, Vogel J, Charpentier E. 2011. CRISPR RNA maturation by trans-encoded small RNA and host factor RNase III. Nature 471:602–607.
    34.
    Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E. 2012. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337:816–821.
    35.
    Qi LS, Larson MH, Gilbert LA, Doudna JA, Weissman JS, Arkin AP, Lim WA. 2013. Repurposing CRISPR as an RNA-guided platform for sequence-specific control of gene expression. Cell 152:1173–1183.
    36.
    Pujol CJ, Kado CI. 2000. Genetic and biochemical characterization of the pathway in Pantoea citrea leading to pink disease of pineapple. J Bacteriol 182:2230–2237.
    37.
    Cha JS, Pujol C, Kado CI. 1997. Identification and characterization of a Pantoea citrea gene encoding glucose dehydrogenase that is essential for causing pink disease of pineapple. Appl Environ Microbiol 63:71–76.
    38.
    Ochman H, Gerber AS, Hartl DL. 1988. Genetic applications of an inverse polymerase chain reaction. Genetics 120:621–623.
    39.
    Shetty RP, Endy D, Knight TF, Jr. 2008. Engineering BioBrick vectors from BioBrick parts. J Biol Eng 2:5.
    40.
    Guzman LM, Belin D, Carson MJ, Beckwith J. 1995. Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol 177:4121–4130.
    41.
    Chayot R, Montagne B, Mazel D, Ricchetti M. 2010. An end-joining repair mechanism in Escherichia coli. Proc Natl Acad Sci U S A 107:2141–2146.
    42.
    Koboldt DC, Steinberg KM, Larson DE, Wilson RK, Mardis ER. 2013. The next-generation sequencing revolution and its impact on genomics. Cell 155:27–38.
    43.
    Dodge TC, Valle F, Rashid MH. February 2005. Metabolically engineered bacterial strains having enhanced 2-keto-d-gluconate accumulation. US patent WO2005012486-A2.
    44.
    Banta S, Boston M, Jarnagin A, Anderson S. 2002. Mathematical modeling of in vitro enzymatic production of 2-keto-l-gulonic acid using NAD(H) or NADP(H) as cofactors. Metab Eng 4:273–284.
    45.
    Wilson TE, Topper LM, Palmbos PL. 2003. Non-homologous end-joining: bacteria join the chromosome breakdance. Trends Biochem Sci 28:62–66.
    46.
    Malyarchuk S, Wright D, Castore R, Klepper E, Weiss B, Doherty AJ, Harrison L. 2007. Expression of Mycobacterium tuberculosis Ku and ligase D in Escherichia coli results in RecA and RecB-independent DNA end-joining at regions of microhomology. DNA Repair (Amst) 6:1413–1424.
    47.
    Siegele DA, Hu JC. 1997. Gene expression from plasmids containing the araBAD promoter at subsaturating inducer concentrations represents mixed populations. Proc Natl Acad Sci U S A 94:8168–8172.
    48.
    Cradick TJ, Fine EJ, Antico CJ, Bao G. 2013. CRISPR/Cas9 systems targeting beta-globin and CCR5 genes have substantial off-target activity. Nucleic Acids Res 41:9584–9592.
    49.
    Fu Y, Foden JA, Khayter C, Maeder ML, Reyon D, Joung JK, Sander JD. 2013. High-frequency off-target mutagenesis induced by CRISPR-Cas nucleases in human cells. Nat Biotechnol 31:822–826.
    50.
    Ran FA, Hsu PD, Lin CY, Gootenberg JS, Konermann S, Trevino AE, Scott DA, Inoue A, Matoba S, Zhang Y, Zhang F. 2013. Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell 154:1380–1389.
    51.
    Anders C, Niewoehner O, Duerst A, Jinek M. 2014. Structural basis of PAM-dependent target DNA recognition by the Cas9 endonuclease. Nature 513:569–573.
    52.
    Martinez E, Bartolome B, de la Cruz F. 1988. pACYC184-derived cloning vectors containing the multiple cloning site and lacZ alpha reporter gene of pUC8/9 and pUC18/19 plasmids. Gene 68:159–162.
    53.
    Amann E, Ochs B, Abel KJ. 1988. Tightly regulated tac promoter vectors useful for the expression of unfused and fused proteins in Escherichia coli. Gene 69:301–315.
    54.
    Gust B, Challis GL, Fowler K, Kieser T, Chater KF. 2003. PCR-targeted Streptomyces gene replacement identifies a protein domain needed for biosynthesis of the sesquiterpene soil odor geosmin. Proc Natl Acad Sci U S A 100:1541–1546.

    Information & Contributors

    Information

    Published In

    Applied and Environmental Microbiology
    Volume 81Number 71 April 2015
    Pages: 2506 - 2514
    Editor: R. M. Kelly
    PubMed: 25636838

    History

    Received: 10 December 2014
    Accepted: 17 January 2015
    Published online: 12 March 2015

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    Contributors

    Authors

    Yu Jiang
    Key Laboratory of Synthetic Biology, Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai, China
    Shanghai Research Center of Industrial Biotechnology, Shanghai, China
    Biao Chen
    Key Laboratory of Synthetic Biology, Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai, China
    Shanghai Research Center of Industrial Biotechnology, Shanghai, China
    Chunlan Duan
    Key Laboratory of Synthetic Biology, Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai, China
    Bingbing Sun
    Key Laboratory of Synthetic Biology, Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai, China
    Shanghai Research Center of Industrial Biotechnology, Shanghai, China
    Junjie Yang
    Key Laboratory of Synthetic Biology, Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai, China
    Shanghai Research Center of Industrial Biotechnology, Shanghai, China
    Sheng Yang
    Key Laboratory of Synthetic Biology, Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai, China
    Shanghai Research Center of Industrial Biotechnology, Shanghai, China
    Shanghai Collaborative Innovation Center for Biomanufacturing Technology, Shanghai, China

    Editor

    R. M. Kelly
    Editor

    Notes

    Address correspondence to Sheng Yang, [email protected].

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  • Applied and Environmental MicrobiologyArticle
    UniFrac: a New Phylogenetic Method for Comparing Microbial Communities

    UniFrac: a New Phylogenetic Method for Comparing Microbial Communities

    ABSTRACT

    We introduce here a new method for computing differences between microbial communities based on phylogenetic information. This method, UniFrac, measures the phylogenetic distance between sets of taxa in a phylogenetic tree as the fraction of the branch length of the tree that leads to descendants from either one environment or the other, but not both. UniFrac can be used to determine whether communities are significantly different, to compare many communities simultaneously using clustering and ordination techniques, and to measure the relative contributions of different factors, such as chemistry and geography, to similarities between samples. We demonstrate the utility of UniFrac by applying it to published 16S rRNA gene libraries from cultured isolates and environmental clones of bacteria in marine sediment, water, and ice. Our results reveal that (i) cultured isolates from ice, water, and sediment resemble each other and environmental clone sequences from sea ice, but not environmental clone sequences from sediment and water; (ii) the geographical location does not correlate strongly with bacterial community differences in ice and sediment from the Arctic and Antarctic; and (iii) bacterial communities differ between terrestrially impacted seawater (whether polar or temperate) and warm oligotrophic seawater, whereas those in individual seawater samples are not more similar to each other than to those in sediment or ice samples. These results illustrate that UniFrac provides a new way of characterizing microbial communities, using the wealth of environmental rRNA sequences, and allows quantitative insight into the factors that underlie the distribution of lineages among environments.

    REFERENCES

    1.
    Acinas, S. G., V. Klepac-Ceraj, D. E. Hunt, C. Pharino, I. Ceraj, D. L. Distel, and M. F. Polz.2004. Fine-scale phylogenetic architecture of a complex bacterial community. Nature430:551-554.
    2.
    Bano, N., and J. T. Hollibaugh.2002. Phylogenetic composition of bacterioplankton assemblages from the Arctic Ocean. Appl. Environ. Microbiol.68:505-518.
    3.
    Bowman, J. P., S. A. McCammon, M. V. Brown, D. S. Nichols, and T. A. McMeekin.1997. Diversity and association of psychrophilic bacteria in Antarctic sea ice. Appl. Environ. Microbiol.63:3068-3078.
    4.
    Bowman, J. P., S. A. McCammon, J. A. Gibson, L. Robertson, and P. D. Nichols.2003. Prokaryotic metabolic activity and community structure in Antarctic continental shelf sediments. Appl. Environ. Microbiol.69:2448-2462.
    5.
    Bowman, J. P., and R. D. McCuaig.2003. Biodiversity, community structural shifts, and biogeography of prokaryotes within Antarctic continental shelf sediment. Appl. Environ. Microbiol.69:2463-2483.
    6.
    Brinkmeyer, R., K. Knittel, J. Jurgens, H. Weyland, R. Amann, and E. Helmke.2003. Diversity and structure of bacterial communities in Arctic versus Antarctic pack ice. Appl. Environ. Microbiol.69:6610-6619.
    7.
    Brown, M. V., and J. P. Bowman.2001. A molecular phylogenetic survey of sea-ice microbial communities (SIMCO). FEMS Microbiol. Ecol.35:267-275.
    8.
    Eilers, H., J. Pernthaler, F. O. Glöckner, and R. Amann.2000. Culturability and in situ abundance of pelagic bacteria from the North Sea. Appl. Environ. Microbiol.66:3044-3051.
    9.
    Felsenstein, J.2004. Inferring phylogenies. Sinauer Associates, Inc., Sunderland, Mass.
    10.
    Ferguson, R. L., E. N. Buckley, and A. V. Palumbo.1984. Response of marine bacterioplankton to differential filtration and confinement. Appl. Environ. Microbiol.47:49-55.
    11.
    Fuhrman, J. A., K. McCallum, and A. A. Davis.1993. Phylogenetic diversity of subsurface marine microbial communities from the Atlantic and Pacific oceans. Appl. Environ. Microbiol.59:1294-1302.
    12.
    Giovannoni, S. J., and M. Rappé.2000. Evolution, diversity, and molecular ecology of marine prokaryotes, p. 47-84. In D. L. Kirchman (ed.), Microbial ecology of the oceans. John Wiley & Sons, Inc., New York, N.Y.
    13.
    Glöckner, F. O., E. Zaichikov, N. Belkova, L. Denissova, J. Pernthaler, A. Pernthaler, and R. Amann.2000. Comparative 16S rRNA analysis of lake bacterioplankton reveals globally distributed phylogenetic clusters including an abundant group of actinobacteria. Appl. Environ. Microbiol.66:5053-5065.
    14.
    Helmke, E., and H. Weyland.1995. Bacteria in sea ice and underlying water of the eastern Weddell Sea in midwinter. Mar. Ecol. Prog. Ser.117:269-287.
    15.
    Hugenholtz, P.2002. Exploring prokaryotic diversity in the genomic era. Genome Biol.3:reviews0003.
    16.
    Hughes, J. B., J. J. Hellmann, T. H. Ricketts, and B. J. Bohannan.2001. Counting the uncountable: statistical approaches to estimating microbial diversity. Appl. Environ. Microbiol.67:4399-4406.
    17.
    Hur, I., and J. Chun.2004. A method for comparing multiple bacterial community structures from 16S rDNA clone library sequences. J. Microbiol.42:9-13.
    18.
    Jannasch, H. W., and G. E. Jones.1959. Bacterial populations in sea water as determined by different methods of enumeration. Limnol. Oceanogr.4:128-139.
    19.
    Junge, K., F. Imhoff, T. Staley, and J. W. Deming.2002. Phylogenetic diversity of numerically important Arctic sea-ice bacteria cultured at subzero temperature. Microb. Ecol.43:315-328.
    20.
    Juretschko, S., A. Loy, A. Lehner, and M. Wagner.2002. The microbial community composition of a nitrifying-denitrifying activated sludge from an industrial sewage treatment plant analyzed by the full-cycle rRNA approach. Syst. Appl. Microbiol.25:84-99.
    21.
    Kanawaga, T.2003. Bias and artifacts in multitemplate polymerase chain reaction. J. Biosci. Bioeng.96:317-323.
    22.
    Kelly, K. M., and A. Y. Chistoserdov.2001. Phylogenetic analysis of the succession of bacterial communities in the Great South Bay (Long Island). FEMS Microbiol. Ecol.35:85-95.
    23.
    Krzanowski, W. J.2000. Principles of multivariate analysis. A user's perspective. Oxford University Press, Oxford, United Kingdom.
    24.
    Ley, R. E., F. Backhed, P. Turnbaugh, C. A. Lozupone, R. D. Knight, and J. I. Gordon.2005. Obesity alters gut microbial ecology. Proc. Natl. Acad. Sci. USA102:11070-11075.
    25.
    Li, L., C. Kato, and K. Horikoshi.1999. Microbial diversity in sediments collected from the deepest cold-seep area, the Japan Trench. Mar. Biotechnol. (New York)1:391-400.
    26.
    Ludwig, W., O. Strunk, R. Westram, L. Richter, H. Meier, Yadhukumar, A. Buchner, T. Lai, S. Steppi, G. Jobb, W. Förster, I. Brettske, S. Gerber, A. W. Ginhart, O. Gross, S. Grumann, S. Hermann, R. Jost, A. König, T. Liss, R. Lüssmann, M. May, B. Nonhoff, B. Reichel, R. Strehlow, A. Stamatakis, N. Stuckmann, A. Vilbig, M. Lenke, T. Ludwig, A. Bode, and K. H. Schleifer.2004. ARB: a software environment for sequence data. Nucleic Acids Res.32:1363-1371.
    27.
    Magurran, A. E.1988. Ecological diversity and its measurement. Princeton University Press, Princeton, N.J.
    28.
    Magurran, A. E.2004. Measuring biological diversity. Blackwell, Oxford, United Kingdom.
    29.
    Maidak, B. L., J. R. Cole, T. G. Lilburn, C. T. Parker, Jr., P. R. Saxman, R. J. Farris, G. M. Garrity, G. J. Olsen, T. M. Schmidt, and J. M. Tiedje.2001. The RDP-II (Ribosomal Database Project). Nucleic Acids Res.29:173-174.
    30.
    Martin, A. P.2002. Phylogenetic approaches for describing and comparing the diversity of microbial communities. Appl. Environ. Microbiol.68:3673-3682.
    31.
    Massana, R., A. E. Murray, C. M. Preston, and E. F. DeLong.1997. Vertical distribution and phylogenetic characterization of marine planktonic archaea in the Santa Barbara Channel. Appl. Environ. Microbiol.63:50-56.
    32.
    Mullins, T. D., T. B. Britschgi, R. L. Krest, and S. J. Giovannoni.1995. Genetic comparisons reveal the same unknown bacterial lineages in Atlantic and Pacific bacterioplankton communities. Limnol. Oceanogr.40:148-158.
    33.
    Nübel, U., F. Garcia-Pichel, M. Kuhl, and G. Muyzer.1999. Quantifying microbial diversity: morphotypes, 16S rRNA genes, and carotenoids of oxygenic phototrophs in microbial mats. Appl. Environ. Microbiol.65:422-430.
    34.
    Pace, N. R.1997. A molecular view of microbial diversity and the biosphere. Science276:734-740.
    35.
    Pace, N. R., D. A. Stahl, D. J. Lane, and G. J. Olsen.1986. The analysis of natural microbial populations by ribosomal RNA sequences. Adv. Microb. Ecol.9:1-55.
    36.
    Pace, N. R., D. A. Stahl, D. J. Lane, and G. J. Olsen.1985. Analyzing natural microbial populations by rRNA sequences. ASM News51:4-12.
    37.
    Rappé, M. S., and S. J. Giovannoni.2003. The uncultured microbial majority. Annu. Rev. Microbiol.57:369-394.
    38.
    Ravenschlag, K., K. Sahm, J. Pernthaler, and R. Amann.1999. High bacterial diversity in permanently cold marine sediments. Appl. Environ. Microbiol.65:3982-3989.
    39.
    Schloss, P. D., B. R. Larget, and J. Handelsman.2004. Integration of microbial ecology and statistics: a test to compare gene libraries. Appl. Environ. Microbiol.70:5485-5492.
    40.
    Singleton, D. R., M. A. Furlong, S. L. Rathbun, and W. B. Whitman.2001. Quantitative comparisons of 16S rRNA gene sequence libraries from environmental samples. Appl. Environ. Microbiol.67:4374-4376.
    41.
    Spear, J. R., J. J. Walker, T. M. McCollom, and N. R. Pace.2005. Hydrogen and bioenergetics in the Yellowstone geothermal ecosystem. Proc. Natl. Acad. Sci. USA102:2555-2560.
    42.
    Staley, J. T., and J. J. Gosink.1999. Poles apart: biodiversity and biogeography of sea ice bacteria. Annu. Rev. Microbiol.53:189-215.
    43.
    von Wintzingerode, F., U. B. Göbel, and E. Stackebrandt.1997. Determination of microbial diversity in environmental samples: pitfalls of PCR-based rRNA analysis. FEMS Microbiol. Rev.21:213-229.
    44.
    Wheeler, P. A., M. Gosselin, E. Sherr, D. Thibault, D. L. Kirchman, R. Benner, and T. E. Whitledge.1996. Active cycling of organic carbon in the central Arctic Ocean. Nature380:697-699.
    45.
    Zwart, G., W. D. Hiorns, B. A. Methe, M. P. Van Agterveld, R. Huismans, S. C. Nold, J. P. Zehr, and H. J. Laanbroek.1998. Nearly identical 16S rRNA sequences recovered from lakes in North America and Europe indicate the existence of clades of globally distributed freshwater bacteria. Syst. Appl. Microbiol.21:546-556.

    Information & Contributors

    Information

    Published In

    Applied and Environmental Microbiology
    Volume 71Number 12December 2005
    Pages: 8228 - 8235
    PubMed: 16332807

    History

    Received: 3 May 2005
    Accepted: 26 August 2005
    Published online: 1 December 2005

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    Contributors

    Authors

    Catherine Lozupone
    Department of Molecular, Cellular, and Developmental Biology, University of Colorado, Boulder, Colorado 80309
    Department of Chemistry and Biochemistry, University of Colorado, Boulder, Colorado 80309

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  • Applied and Environmental MicrobiologyArticle
    UV Inactivation of SARS-CoV-2 across the UVC Spectrum: KrCl* Excimer, Mercury-Vapor, and Light-Emitting-Diode (LED) Sources

    UV Inactivation of SARS-CoV-2 across the UVC Spectrum: KrCl* Excimer, Mercury-Vapor, and Light-Emitting-Diode (LED) Sources

    ABSTRACT

    Effective disinfection technology to combat severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) can help reduce viral transmission during the ongoing COVID-19 global pandemic and in the future. UV devices emitting UVC irradiation (200 to 280 nm) have proven to be effective for virus disinfection, but limited information is available for SARS-CoV-2 due to the safety requirements of testing, which is limited to biosafety level 3 (BSL3) laboratories. In this study, inactivation of SARS-CoV-2 in thin-film buffered aqueous solution (pH 7.4) was determined across UVC irradiation wavelengths of 222 to 282 nm from krypton chloride (KrCl*) excimers, a low-pressure mercury-vapor lamp, and two UVC light-emitting diodes. Our results show that all tested UVC devices can effectively inactivate SARS-CoV-2, among which the KrCl* excimer had the best disinfection performance (i.e., highest inactivation rate). The inactivation rate constants of SARS-CoV-2 across wavelengths are similar to those for murine hepatitis virus (MHV) from our previous investigation, suggesting that MHV can serve as a reliable surrogate of SARS-CoV-2 with a lower BSL requirement (BSL2) during UV disinfection tests. This study provides fundamental information on UVC’s action on SARS-CoV-2 and guidance for achieving reliable disinfection performance with UVC devices.
    IMPORTANCE UV light is an effective tool to help stem the spread of respiratory viruses and protect public health in commercial, public, transportation, and health care settings. For effective use of UV, there is a need to determine the efficiency of different UV wavelengths in killing pathogens, specifically SARS-CoV-2, to support efforts to control the ongoing COVID-19 global pandemic and future coronavirus-caused respiratory virus pandemics. We found that SARS-CoV-2 can be inactivated effectively using a broad range of UVC wavelengths, and 222 nm provided the best disinfection performance. Interestingly, 222-nm irradiation has been found to be safe for human exposure up to thresholds that are beyond those effective for inactivating viruses. Therefore, applying UV light from KrCl* excimers in public spaces can effectively help reduce viral aerosol or surface-based transmissions.

    REFERENCES

    1.
    World Health Organization. 2020. Transmission of SARS-CoV-2: implications for infection prevention precautions. World Health Organization, Geneva, Switzerland.
    2.
    Pitol AK, Julian TR. 2021. Community transmission of SARS-CoV-2 by fomites: risks and risk reduction strategies. Environ Sci Technol Lett 8:263–269.
    3.
    van Doremalen N, Bushmaker T, Morris DH, Holbrook MG, Gamble A, Williamson BN, Tamin A, Harcourt JL, Thornburg NJ, Gerber SI, Lloyd-Smith JO, de Wit E, Munster VJ. 2020. Aerosol and surface stability of SARS-CoV-2 as compared with SARS-CoV-1. N Engl J Med 382:1564–1567.
    4.
    Beck SE, Rodriguez RA, Linden KG, Hargy TM, Larason TC, Wright HB. 2014. Wavelength dependent UV inactivation and DNA damage of adenovirus as measured by cell culture infectivity and long range quantitative PCR. Environ Sci Technol 48:591–598.
    5.
    Hull NM, Linden KG. 2018. Synergy of MS2 disinfection by sequential exposure to tailored UV wavelengths. Water Res 143:292–300.
    6.
    Linden KG, Hull N, Speight V. 2019. Thinking outside the treatment plant: UV for water distribution system disinfection. Acc Chem Res 52:1226–1233.
    7.
    Beck SE, Ryu H, Boczek LA, Cashdollar JL, Jeanis KM, Rosenblum JS, Lawal OR, Linden KG. 2017. Evaluating UV-C LED disinfection performance and investigating potential dual-wavelength synergy. Water Res 109:207–216.
    8.
    Kowalski W, Bahnfleth W, Hernandez M. 2009. A genomic model for predicting the ultraviolet susceptibility of viruses. IUVA News 11:15–28.
    9.
    Tenkate TD. 1998. Ultraviolet radiation: human exposure and health risks. J Environ Health 61:9–15.
    10.
    Zaffina S, Camisa V, Lembo M, Vinci MR, Tucci MG, Borra M, Napolitano A, Cannatã V. 2012. Accidental exposure to UV radiation produced by germicidal lamp: case report and risk assessment. Photochem Photobiol 88:1001–1004.
    11.
    Buonanno M, Ponnaiya B, Welch D, Stanislauskas M, Randers-Pehrson G, Smilenov L, Lowy FD, Owens DM, Brenner DJ. 2017. Germicidal efficacy and mammalian skin safety of 222-nm UV light. Radiat Res 187:483–491.
    12.
    Buonanno M, Welch D, Shuryak I, Brenner DJ. 2020. Far-UVC light (222 nm) efficiently and safely inactivates airborne human coronaviruses. Sci Rep 10:10285–10288.
    13.
    Narita K, Asano K, Morimoto Y, Igarashi T, Nakane A. 2018. Chronic irradiation with 222-nm UVC light induces neither DNA damage nor epidermal lesions in mouse skin, even at high doses. PLoS One 13:e0201259.
    14.
    Kaidzu S, Sugihara K, Sasaki M, Nishiaki A, Ohashi H, Igarashi T, Tanito M. 2021. Re-evaluation of rat corneal damage by short-wavelength UV revealed extremely less hazardous property of far-UV-C. Photochem Photobiol 97:505–516.
    15.
    Biasin M, Bianco A, Pareschi G, Cavalleri A, Cavatorta C, Fenizia C, Galli P, Lessio L, Lualdi M, Tombetti E, Ambrosi A, Redaelli EMA, Saulle I, Trabattoni D, Zanutta A, Clerici M. 2021. UV-C irradiation is highly effective in inactivating SARS-CoV-2 replication. Sci Rep 11:6260–6267.
    16.
    Patterson EI, Prince T, Anderson ER, Casas-Sanchez A, Smith SL, Cansado-Utrilla C, Solomon T, Griffiths MJ, Acosta-Serrano Á, Turtle L, Hughes GL. 2020. Methods of inactivation of SARS-CoV-2 for downstream biological assays. J Infect Dis 222:1462–1467.
    17.
    Storm N, McKay LGA, Downs SN, Johnson RI, Birru D, de Samber M, Willaert W, Cennini G, Griffiths A. 2020. Rapid and complete inactivation of SARS-CoV-2 by ultraviolet-C irradiation. Sci Rep 10:22421–22425.
    18.
    Heilingloh CS, Aufderhorst UW, Schipper L, Dittmer U, Witzke O, Yang D, Zheng X, Sutter K, Trilling M, Alt M, Steinmann E, Krawczyk A. 2020. Susceptibility of SARS-CoV-2 to UV irradiation. Am J Infect Control 48:1273–1275.
    19.
    Robinson RT, Mahfooz N, Rosas-Mejia O, Liu Y, Hull NM. 2021. SARS-CoV-2 disinfection in aqueous solution by UV 222 from a krypton chlorine excilamp. medRxiv
    20.
    Kitagawa H, Nomura T, Nazmul T, Omori K, Shigemoto N, Sakaguchi T, Ohge H. 2021. Effectiveness of 222-nm ultraviolet light on disinfecting SARS-CoV-2 surface contamination. Am J Infect Control 49:299–301.
    21.
    Kitagawa H, Nomura T, Nazmul T, Kawano R, Omori K, Shigemoto N, Sakaguchi T, Ohge H. 2021. Effect of intermittent irradiation and fluence-response of 222 nm ultraviolet light on SARS-CoV-2 contamination. Photodiagnosis Photodyn Ther 33:102184.
    22.
    Ma B, Linden YS, Gundy PM, Gerba CP, Sobsey MD, Linden KG. 2021. Inactivation of coronaviruses and phage Phi6 from irradiation across UVC wavelengths. Environ Sci Technol Lett 8:425–430.
    23.
    Beck SE, Rodriguez RA, Hawkins MA, Hargy TM, Larason TC, Linden KG. 2015. Comparison of UV-induced inactivation and RNA damage in MS2 phage across the germicidal UV spectrum. Appl Environ Microbiol 82:1468–1474.
    24.
    American Conference of Governmental Industrial Hygienists. 2021. 2021 threshold limit values (TLVs) and biological exposure indices (BEIs). American Conference of Governmental Industrial Hygienists, Washington, DC.
    25.
    Chun-Chieh T, Li C-S. 2007. Inactivation of viruses on surfaces by ultraviolet germicidal irradiation. J Occup Environ Hyg 4:400–405.
    26.
    Walker CM, Ko G. 2007. Effect of ultraviolet germicidal irradiation on viral aerosols. Environ Sci Technol 41:5460–5465.
    27.
    Beck SE, Wright HB, Hargy TM, Larason TC, Linden KG. 2015. Action spectra for validation of pathogen disinfection in medium-pressure ultraviolet (UV) systems. Water Res 70:27–37.
    28.
    Beck SE, Hull NM, Poepping C, Linden KG. 2018. Wavelength-dependent damage to adenoviral proteins across the germicidal UV spectrum. Environ Sci Technol 52:223–229.
    29.
    Gerchman Y, Mamane H, Friedman N, Mandelboim M. 2020. UV-LED disinfection of coronavirus: wavelength effect. J Photochem Photobiol B Biol 212:112044.
    30.
    Kim K, Jothikumar N, Sen A, Murphy JL, Chellam S. 2021. Removal and inactivation of an enveloped virus surrogate by iron conventional coagulation and electrocoagulation. Environ Sci Technol 55:2674–2683.
    31.
    Silverman AI, Boehm AB. 2020. Systematic review and meta-analysis of the persistence and disinfection of human coronaviruses and their viral surrogates in water and wastewater. Environ Sci Technol Lett 7:544–553.
    32.
    Aquino De Carvalho N, Stachler EN, Cimabue N, Bibby K. 2017. Evaluation of Phi6 persistence and suitability as an enveloped virus surrogate. Environ Sci Technol 51:8692–8700.
    33.
    Payment P, Trudel M (ed). 1994. Methods and techniques in virology. Marcel Dekker, Inc, New York, NY.
    34.
    Ramakrishnan MA. 2016. Determination of 50% endpoint titer using a simple formula. World J Virol 5:85–86.
    35.
    Bolton JR, Linden KG. 2003. Standardization of methods for fluence (UV dose) determination in bench-scale UV experiments. J Environ Eng 129:209–215.
    36.
    Linden KG, Darby JL. 1997. Estimating effective germicidal dose from medium pressure UV lamps. J Environ Eng 123:1142–1149.

    Information & Contributors

    Information

    Published In

    Applied and Environmental Microbiology
    Volume 87Number 2228 October 2021
    eLocator: e01532-21
    Editor: Edward G. Dudley, The Pennsylvania State University
    PubMed: 34495736

    History

    Received: 2 August 2021
    Accepted: 31 August 2021
    Accepted manuscript posted online: 8 September 2021
    Published online: 28 October 2021

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    KEYWORDS

    1. UV disinfection
    2. far UVC
    3. COVID-19
    4. surrogate
    5. human coronavirus 229E
    6. murine hepatitis virus
    7. MHV
    8. bacteriophage Phi6

    Contributors

    Authors

    Department of Civil, Environmental, and Architectural Engineering, University of Colorado Boulder, Boulder, Colorado, USA
    Patricia M. Gundy
    Department of Environmental Science, University of Arizona, Tucson, Arizona, USA
    Charles P. Gerba
    Department of Environmental Science, University of Arizona, Tucson, Arizona, USA
    Mark D. Sobsey
    Department of Environmental Science and Engineering, Gillings School of Public Health, University of North Carolina, Chapel Hill, North Carolina, USA
    Department of Civil, Environmental, and Architectural Engineering, University of Colorado Boulder, Boulder, Colorado, USA

    Editor

    Edward G. Dudley
    Editor
    The Pennsylvania State University

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  • Applied and Environmental MicrobiologyArticle
    Longer Contact Times Increase Cross-Contamination of Enterobacter aerogenes from Surfaces to Food

    Longer Contact Times Increase Cross-Contamination of Enterobacter aerogenes from Surfaces to Food

    ABSTRACT

    Bacterial cross-contamination from surfaces to food can contribute to foodborne disease. The cross-contamination rate of Enterobacter aerogenes on household surfaces was evaluated by using scenarios that differed by surface type, food type, contact time (<1, 5, 30, and 300 s), and inoculum matrix (tryptic soy broth or peptone buffer). The surfaces used were stainless steel, tile, wood, and carpet. The food types were watermelon, bread, bread with butter, and gummy candy. Surfaces (25 cm2) were spot inoculated with 1 ml of inoculum and allowed to dry for 5 h, yielding an approximate concentration of 107 CFU/surface. Foods (with a 16-cm2 contact area) were dropped onto the surfaces from a height of 12.5 cm and left to rest as appropriate. Posttransfer, surfaces and foods were placed in sterile filter bags and homogenized or massaged, diluted, and plated on tryptic soy agar. The transfer rate was quantified as the log percent transfer from the surface to the food. Contact time, food, and surface type all had highly significant effects (P < 0.000001) on the log percent transfer of bacteria. The inoculum matrix (tryptic soy broth or peptone buffer) also had a significant effect on transfer (P = 0.013), and most interaction terms were significant. More bacteria transferred to watermelon (∼0.2 to 97%) than to any other food, while the least bacteria transferred to gummy candy (∼0.1 to 62%). Transfer of bacteria to bread (∼0.02 to 94%) was similar to transfer of bacteria to bread with butter (∼0.02 to 82%), and these transfer rates under a given set of conditions were more variable than with watermelon and gummy candy.
    IMPORTANCE The popular notion of the “five-second rule” is that food dropped on the floor and left there for <5 s is “safe” because bacteria need time to transfer. The rule has been explored by a single study in the published literature and on at least two television shows. Results from two academic laboratories have been shared through press releases but remain unpublished. We explored this topic by using four different surfaces (stainless steel, ceramic tile, wood, and carpet), four different foods (watermelon, bread, bread with butter, and gummy candy), four different contact times (<1, 5, 30, and 300 s), and two bacterial preparation methods. Although we found that longer contact times result in more transfer, we also found that other factors, including the nature of the food and the surface, are of equal or greater importance. Some transfer takes place “instantaneously,” at times of <1 s, disproving the five-second rule.

    REFERENCES

    1.
    Scallan E, Hoekstra RM, Angulo FJ, Tauxe RV, Widdowson MA, Roy SL, Jones JL, Griffin PM. 2011. Foodborne illness acquired in the United States–major pathogens. Emerg Infect Dis 17:7–15.
    2.
    Gould LH, Walsh KA, Vieira AR, Herman K, Williams IT, Hall AJ, Cole D. 2013. Surveillance for foodborne disease outbreaks—United States, 1998–2008. MMWR Surveill Summ 62:1–34. http://www.cdc.gov/mmwr/preview/mmwrhtml/ss6202a1.htm.
    3.
    Centers for Disease Control and Prevention (CDC). 2013. Surveillance for foodborne disease outbreaks—United States, 2009–2010. Morb Mortal Wkly Rep 62:41–47. http://www.cdc.gov/mmwr/preview/mmwrhtml/mm6203a1.htm.
    4.
    Centers for Disease Control and Prevention (CDC). 2013. Surveillance for foodborne disease outbreaks—United States, 2011: annual report. Centers for Disease Control and Prevention, Atlanta, GA. http://www.cdc.gov/foodsafety/pdfs/foodborne-disease-outbreaks-annual-report-2011-508c.pdf.
    5.
    Centers for Disease Control and Prevention (CDC). 2014. Surveillance for foodborne disease outbreaks—United States, 2012: annual report. Centers for Disease Control and Prevention, Atlanta, GA. http://www.cdc.gov/foodsafety/pdfs/foodborne-disease-outbreaks-annual-report-2012-508c.pdf.
    6.
    Centers for Disease Control and Prevention (CDC). 2015. Surveillance for foodborne disease outbreaks—United States, 2013: annual report. Centers for Disease Control and Prevention, Atlanta, GA. http://www.cdc.gov/foodsafety/pdfs/foodborne-disease-outbreaks-annual-report-2013-508c.pdf.
    7.
    Jensen DA, Friedrich LM, Harris LJ, Danyluk MD, Schaffner DW. 2013. Quantifying transfer rates of Salmonella and Escherichia coli O157:H7 between fresh-cut produce and common kitchen surfaces. J Food Prot 76:1530–1538.
    8.
    Dawson P, Han I, Cox M, Black C, Simmons L. 2007. Residence time and food contact time effects on transfer of Salmonella Typhimurium from tile, wood, and carpet: testing the five-second rule. J Appl Microbiol 102:945–953.
    9.
    Wendt C, Dietze B, Dietz E, Rüden H. 1997. Survival of Acinetobacter baumannii on dry surfaces. J Clin Microbiol 35:1394–1397.
    10.
    Kusumaningrum HD, vanAsselt ED, Beumer RR, Zwietering MH. 2004. A quantitative analysis of cross-contamination of Salmonella and Campylobacter spp. via domestic kitchen surfaces. J Food Prot 67:1892–1903.
    11.
    Moore CM, Sheldon BW, Jaykus LA. 2003. Transfer of Salmonella and Campylobacter from stainless steel to romaine lettuce. J Food Prot 66:2231–2236.
    12.
    Midelet G, Carpentier B. 2002. Transfer of microorganisms, including Listeria monocytogenes, from various materials to beef. Appl Environ Microbiol 68:4015–4024.
    13.
    Chen Y, Jackson KM, Chea FP, Schaffner DW. 2001. Quantification and variability analysis of bacterial cross-contamination rates in common food service tasks. J Food Prot 64:72–80.
    14.
    Zhao P, Zhao T, Doyle MP, Rubino JR, Meng J. 1998. Development of a model for evaluation of microbial cross-contamination in the kitchen. J Food Prot 61:960–963.
    15.
    Lankford MG, Collins S, Youngberg L, Rooney DM, Warren JR, Noskin GA. 2006. Assessment of materials commonly utilized in health care: implications for bacterial survival and transmission. Am J Infect Control 34:258–263.
    16.
    Rice DH, Hancock DD, Szymanski MH, Scheenstra BC, Cady KM, Besser TE, Chudek PA. 2003. Household contamination with Salmonella enterica. Emerg Infect Dis 9:120–122.
    17.
    Holah JT, Thorpe RH. 1990. Cleanability in relation to bacterial retention on unused and abraded domestic sink materials. J Appl Bacteriol 69:599–608.
    18.
    Wilks SA, Michels HT, Keevil CW. 2006. Survival of Listeria monocytogenes Scott A on metal surfaces: implications for cross-contamination. Int J Food Microbiol 111:93–98.
    19.
    Kuhn PJ. 1983. Doorknobs: a source of nosocomial infection. Diagn Med November-December:62–63. http://www.antimicrobialcopper.org/sites/default/files/upload/Media-library/Files/PDFs/UK/Scientific_literature/kuhn-doorknob.pdf.
    20.
    Robine E, Boulangé-Petermann L, Derangère D. 2002. Assessing bactericidal properties of materials: the case of metallic surfaces in contact with air. J Microbiol Methods 49:225–234.
    21.
    Wilks SA, Michels H, Keevil CW. 2005. The survival of Escherichia coli O157 on a range of metal surfaces. Int J Food Microbiol 105:445–454.
    22.
    Berto AM. 2007. Ceramic tiles: above and beyond traditional applications. J Eur Ceram Soc 27:1607–1613.
    23.
    Ak NO, Cliver DO, Kaspar CW. 1994. Cutting boards of plastic and wood contaminated experimentally with bacteria. J Food Prot 57:16–22.
    24.
    Welker C, Faiola N, Davis S, Maffatore I, Batt CA. 1997. Bacterial retention and cleanability of plastic and wood cutting boards with commercial food service maintenance practices. J Food Prot 60:407–413.
    25.
    United States Department of Agriculture (USDA). 2013. Cutting boards and food safety. United States Department of Agriculture, Washington, DC. http://www.fsis.usda.gov/wps/portal/fsis/topics/food-safety-education/get-answers/food-safety-fact-sheets/safe-food-handling/cutting-boards-and-food-safety.
    26.
    Yu H. 2007. The effect of chemical finishing on the microbial transfer from carpets to human skin and selected fabrics. Ph.D. dissertation. University of Georgia, Athens, GA.
    27.
    . 2003. If you drop it, should you eat it? Scientists weigh in on the 5-second rule. University of Illinois at Urbana-Champaign, Urbana, IL. http://news.aces.illinois.edu/news/if-you-drop-it-should-you-eat-it-scientists-weigh-5-second-rule.
    28.
    MythBusters. 2005. 5 second rule with food on floor. Discovery Communications, Silver Spring, MD.http://www.discovery.com/tv-shows/mythbusters/mythbusters-database/5-second-rule-with-food/.
    29.
    Garbett J. 10 March 2014. Researchers prove the five-second rule is real. Aston University, Birmingham, United Kingdom. http://www.aston.ac.uk/about/news/releases/2014/march/five-second-food-rule-does-exist/.
    30.
    Moran L. 2016. Science explains why the 5-second rule is actually true. The Huffington Post, New York, NY. http://www.huffingtonpost.com/entry/5-second-rule-scienceexplainer_us_56b07205e4b057d7d7c809a8.
    31.
    Schaffner DW. 2003. Challenges in cross contamination modelling in home and food service settings. Food Aust 55:583–586.
    32.
    Sharma M, Taormina PJ, Beuchat LR. 2003. Habituation of foodborne pathogens exposed to extreme pH conditions: genetic basis and implications in foods and food processing environments. Food Sci Technol Res 9:115–127.
    33.
    Kusumaningrum HD, Riboldi G, Hazeleger WC, Beumer RR. 2003. Survival of foodborne pathogens on stainless steel surfaces and cross-contamination to foods. Int J Food Microbiol 85:227–236.
    34.
    Donlan RM. 2002. Biofilms: microbial life on surfaces. Emerg Infect Dis 8:881–890.
    35.
    Ryu JH, Beuchat LR. 2005. Biofilm formation by Escherichia coli O157:H7 on stainless steel: effect of exopolysaccharide and curli production on its resistance to chlorine. Appl Environ Microbiol 71:247–254.
    36.
    Wachtel MR, Charkowski AO. 2002. Cross-contamination of lettuce with Escherichia coli O157:H7. J Food Prot 65:465–470.
    37.
    Mbithi JN, Springthorpe VS, Boulet JR, Sattar SA. 1992. Survival of hepatitis A virus on human hands and its transfer on contact with animate and inanimate surfaces. J Clin Microbiol 30:757–763.
    38.
    D'Souza DH, Sair A, Williams K, Papafragkou E, Jean J, Moore C, Jaykus L. 2006. Persistence of caliciviruses on environmental surfaces and their transfer to food. Int J Food Microbiol 108:84–91.
    39.
    Escudero BI, Rawsthorne H, Gensel C, Jaykus LA. 2012. Persistence and transferability of noroviruses on and between common surfaces and foods. J Food Prot 75:927–935.
    40.
    Pérez-Rodríguez F, Valero A, Carrasco E, García RM, Zurera G. 2008. Understanding and modelling bacterial transfer to foods: a review. Trends Food Sci Technol 19:131–144.
    41.
    Montville R, Schaffner DW. 2003. Inoculum size influences bacterial cross contamination between surfaces. Appl Environ Microbiol 69:7188–7193.

    Information & Contributors

    Information

    Published In

    Applied and Environmental Microbiology
    Volume 82Number 211 November 2016
    Pages: 6490 - 6496
    Editor: C. A. Elkins, FDA Center for Food Safety and Applied Nutrition
    PubMed: 27590818

    History

    Received: 16 June 2016
    Accepted: 16 August 2016
    Published online: 14 October 2016

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    Contributors

    Authors

    Robyn C. Miranda
    Rutgers, The State University of New Jersey, New Brunswick, New Jersey, USA
    Rutgers, The State University of New Jersey, New Brunswick, New Jersey, USA

    Editor

    C. A. Elkins
    Editor
    FDA Center for Food Safety and Applied Nutrition

    Notes

    Address correspondence to Donald W. Schaffner, [email protected].

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  • Applied and Environmental MicrobiologyArticle
    Assessment of Antiviral Coatings for High-Touch Surfaces by Using Human Coronaviruses HCoV-229E and SARS-CoV-2

    Assessment of Antiviral Coatings for High-Touch Surfaces by Using Human Coronaviruses HCoV-229E and SARS-CoV-2

    ABSTRACT

    A novel and robust approach to evaluate the antiviral activity of coatings was developed, assessing three commercially available leave-on surface coating products for efficacy against human coronaviruses (HCoVs) HCoV-229E and severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2). The assessment is based on three criteria that reflect real-life settings, namely, (i) immediate antiviral effect, (ii) effect after repeated cleaning of the coated surface, and (iii) antiviral activity in the presence of organic material. The results showed that only a copper compound-based coating successfully met all three criteria. A quaternary ammonium compound-based coating did not meet the second criterion, and a coating based on reactive oxygen species showed no antiviral effect. Moreover, the study demonstrated that HCoV-229E is a relevant SARS-CoV-2 surrogate for such experiments. This new approach allows benchmarking of currently available antiviral coatings and future coating developments to avoid unjustified claims. The deployment of efficient antiviral coatings can offer an additional measure to mitigate the risk of transmission of respiratory viruses like SARS-CoV-2 or influenza viruses from high-touch surfaces.
    IMPORTANCE SARS-CoV-2, the virus responsible for the coronavirus disease 2019 (COVID-19) pandemic, is transmitted mainly person-to-person through respiratory droplets, while the contribution of fomite transmission is less important than suspected at the beginning of the pandemic. Nevertheless, antiviral-coating solutions can offer an additional measure to mitigate the risk of SARS-CoV-2 transmission from high-touch surfaces. The deployment of antiviral coatings is not new, but what is currently lacking is solid scientific evidence of the efficacy of commercially available self-disinfecting surfaces under real-life conditions. Therefore, we developed a novel, robust approach to evaluate the antiviral activity of such coatings, applying strict quality criteria to three commercially available products to test their efficacies against SARS-CoV-2. We also showed that HCoV-229E is a relevant surrogate for such experiments. Our approach will also bring significant benefit to the evaluation of the effects of coatings on the survival of nonenveloped viruses, which are known to be more tolerant to desiccation and disinfectants and for which high-touch surfaces play an important role.

    REFERENCES

    1.
    Li Q, Guan X, Wu P, Wang X, Zhou L, Tong Y, Ren R, Leung KSM, Lau EHY, Wong JY, Xing X, Xiang N, Wu Y, Li C, Chen Q, Li D, Liu T, Zhao J, Liu M, Tu W, Chen C, Jin L, Yang R, Wang Q, Zhou S, Wang R, Liu H, Luo Y, Liu Y, Shao G, Li H, Tao Z, Yang Y, Deng Z, Liu B, Ma Z, Zhang Y, Shi G, Lam TTY, Wu JT, Gao GF, Cowling BJ, Yang B, Leung GM, Feng Z. 2020. Early transmission dynamics in Wuhan, China, of novel coronavirus-infected pneumonia. N Engl J Med 382:1199–1207.
    2.
    Zhou P, Yang X-L, Wang X-G, Hu B, Zhang L, Zhang W, Si H-R, Zhu Y, Li B, Huang C-L, Chen H-D, Chen J, Luo Y, Guo H, Jiang R-D, Liu M-Q, Chen Y, Shen X-R, Wang X, Zheng X-S, Zhao K, Chen Q-J, Deng F, Liu L-L, Yan B, Zhan F-X, Wang Y-Y, Xiao G-F, Shi Z-L. 2020. A pneumonia outbreak associated with a new coronavirus of probable bat origin. Nature 579:270–273.
    3.
    WHO. 2021. Coronavirus disease (COVID-19) Weekly Epidemiological Update and Weekly Operational Update. World Health Organization, Geneva, Switzerland. https://www.who.int/emergencies/diseases/novel-coronavirus-2019/situation-reports. Accessed 16 February 2021.
    4.
    Chu DK, Akl EA, Duda S, Solo K, Yaacoub S, Schünemann HJ. 2020. Physical distancing, face masks, and eye protection to prevent person-to-person transmission of SARS-CoV-2 and COVID-19: a systematic review and meta-analysis. Lancet 395:1973–1987.
    5.
    van Doremalen N, Bushmaker T, Morris DH, Holbrook MG, Gamble A, Williamson BN, Tamin A, Harcourt JL, Thornburg NJ, Gerber SI, Lloyd-Smith JO, de Wit E, Munster VJ. 2020. Aerosol and surface stability of SARS-CoV-2 as compared with SARS-CoV-1. N Engl J Med 382:1564–1567.
    6.
    Pastorino B, Touret F, Gilles M, de Lamballerie X, Charrel R. 2020. Prolonged infectivity of SARS-CoV-2 in fomites. Emerg Infect Dis J 26:2256–2257.
    7.
    Guo ZD, Wang ZY, Zhang SF, Li X, Li L, Li C, Cui Y, Fu RB, Dong YZ, Chi XY, Zhang MY, Liu K, Cao C, Liu B, Zhang K, Gao YW, Lu B, Chen W. 2020. Aerosol and surface distribution of severe acute respiratory syndrome coronavirus 2 in hospital wards, Wuhan, China, 2020. Emerg Infect Dis 26:1583–1591.
    8.
    Ma J, Qi X, Chen H, Li X, Zhan Z, Wang H, Sun L, Zhang L, Guo J, Morawska L, Grinshpun SA, Biswas P, Flagan RC, Yao M. 2020. Exhaled breath is a significant source of SARS-CoV-2 emission. medRxiv
    9.
    Harvey AP, Fuhrmeister ER, Cantrell M, Pitol AK, Swarthout JM, Powers JE, Nadimpalli ML, Julian TR, Pickering AJ. 2020. Longitudinal monitoring of SARS-CoV-2 RNA on high-touch surfaces in a community setting. medRxiv
    10.
    Kratzel A, Todt D, V’Kovski P, Steiner S, Gultom M, Thao TTN, Ebert N, Holwerda M, Steinmann J, Niemeyer D, Dijkman R, Kampf G, Drosten C, Steinmann E, Thiel V, Pfaender S. 2020. Inactivation of severe acute respiratory syndrome coronavirus 2 by WHO-recommended hand rub formulations and alcohols. Emerg Infect Dis 26:1592–1595.
    11.
    Ong SWX, Tan YK, Chia PY, Lee TH, Ng OT, Wong MSY, Marimuthu K. 2020. Air, surface environmental, and personal protective equipment contamination by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) from a symptomatic patient. JAMA 323:1610–1612.
    12.
    Kampf G, Todt D, Pfaender S, Steinmann E. 2020. Persistence of coronaviruses on inanimate surfaces and their inactivation with biocidal agents. J Hosp Infect 104:246–251.
    13.
    De Benedictis P, Beato MS, Capua I. 2007. Inactivation of avian influenza viruses by chemical agents and physical conditions: a review. Zoonoses Public Health 54:51–68.
    14.
    Weber DJ, Rutala WA. 2013. Self-disinfecting surfaces: review of current methodologies and future prospects. Am J Infect Control 41:S31–S35.
    15.
    Tripathy A, Sen P, Su B, Briscoe WH. 2017. Natural and bioinspired nanostructured bactericidal surfaces. Adv Colloid Interface Sci 248:85–104.
    16.
    Querido MM, Aguiar L, Neves P, Pereira CC, Teixeira JP. 2019. Self-disinfecting surfaces and infection control. Colloids Surf B Biointerfaces 178:8–21.
    17.
    Imani SM, Ladouceur L, Marshall T, Maclachlan R, Soleymani L, Didar TF. 2020. Antimicrobial nanomaterials and coatings: current mechanisms and future perspectives to control the spread of viruses including SARS-CoV-2. ACS Nano 14:12341–12369.
    18.
    ASTM. 2011. ASTM E1053-11. Standard test method to assess virucidal activity of chemicals intended for disinfection of inanimate, nonporous environmental surfaces. ASTM International, West Conshohocken, PA.
    19.
    ISO. 2017 ISO 21702. Measurement of antiviral activity on plastics and other non-porous surfaces. ISO, Geneva, Switzerland.
    20.
    Nakano R, Hara M, Ishiguro H, Yao Y, Ochiai T, Nakata K, Murakami T, Kajioka J, Sunada K, Hashimoto K, Fujishima A, Kubota Y. 2013. Broad spectrum microbicidal activity of photocatalysis by TiO 2. Catalysts 3:310–323.
    21.
    Warnes SL, Little ZR, Keevil CW. 2015. Human coronavirus 229E remains infectious on common touch surface materials. mBio 6:e01697-15.
    22.
    Behzadinasab S, Chin A, Hosseini M, Poon LLM, Ducker WA. 2020. A surface coating that rapidly inactivates SARS-CoV-2. ACS Appl Mater Interfaces 12:34723–34727.
    23.
    Sunada K, Minoshima M, Hashimoto K. 2012. Highly efficient antiviral and antibacterial activities of solid-state cuprous compounds. J Hazard Mater 235–236:265–270.
    24.
    Joonaki E, Hassanpouryouzband A, Heldt CL, Areo O. 2020. Surface chemistry can unlock drivers of surface stability of SARS-CoV-2 in a variety of environmental conditions. Chem 6:2135–2146.
    25.
    Botequim D, Maia J, Lino MM, Lopes LM, Simões PN, Ilharco LM, Ferreira L. 2012. Nanoparticles and surfaces presenting antifungal, antibacterial and antiviral properties. Langmuir 28:7646–7656.
    26.
    Boyce JM, Havill NL, Guercia KA, Schweon SJ, Moore BA. 2014. Evaluation of two organosilane products for sustained antimicrobial activity on high-touch surfaces in patient rooms. Am J Infect Control 42:326–328.
    27.
    Su S, Wong G, Shi W, Liu J, Lai ACK, Zhou J, Liu W, Bi Y, Gao GF. 2016. Epidemiology, genetic recombination, and pathogenesis of coronaviruses. Trends Microbiol 24:490–502.
    28.
    Bar-On YM, Flamholz A, Phillips R, Milo R. 2020. SARS-CoV-2 (COVID-19) by the numbers. Elife 9:e57309.
    29.
    Shewale JG, Ratcliff JL. 2021. Overinterpretation of the antiviral results for human coronavirus strain 229E (HCoV‐229E) relative to severe acute respiratory syndrome coronavirus‐2 (SARS‐CoV‐2). J Med Virol 93:1900–1902.
    30.
    Gerba CP. 2015. Quaternary ammonium biocides: efficacy in application. Appl Environ Microbiol 81:464–469.
    31.
    Zhou Z, Zuber S, Cantergiani F, Butot S, Li D, Stroheker T, Devlieghere F, Lima A, Piantini U, Uyttendaele M. 2017. Inactivation of viruses and bacteria on strawberries using a levulinic acid plus sodium dodecyl sulfate based sanitizer, taking sensorial and chemical food safety aspects into account. Int J Food Microbiol 257:176–182.
    32.
    ISO. 2017 ISO 15216-1:2017. Microbiology of the food chain—Horizontal method for determination of hepatitis A virus and norovirus in food using real-time RT-PCR—Part 1: method for quantification. ISO, Geneva, Switzerland.
    33.
    Wölfel R, Corman VM, Guggemos W, Seilmaier M, Zange S, Müller MA, Niemeyer D, Jones TC, Vollmar P, Rothe C, Hoelscher M, Bleicker T, Brünink S, Schneider J, Ehmann R, Zwirglmaier K, Drosten C, Wendtner C. 2020. Virological assessment of hospitalized patients with COVID-2019. Nature 581:465–469.
    34.
    Zhu J, Guo J, Xu Y, Chen X. 2020. Viral dynamics of SARS-CoV-2 in saliva from infected patients. J Infect 81:e48–e50.

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    Applied and Environmental Microbiology
    Volume 87Number 1910 September 2021
    eLocator: e01098-21
    Editor: Christopher A. Elkins, Centers for Disease Control and Prevention
    PubMed: 34288707

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    Received: 3 June 2021
    Accepted: 12 July 2021
    Accepted manuscript posted online: 21 July 2021
    Published online: 10 September 2021

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    KEYWORDS

    1. SARS-CoV-2
    2. antiviral activity
    3. antiviral coating
    4. human coronavirus 229E
    5. viral log reduction

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    S. Butot
    Société des Produits Nestlé, Nestlé Research, Institute of Food Safety and Analytical Science, Lausanne, Switzerland
    Société des Produits Nestlé, Nestlé Research, Institute of Food Safety and Analytical Science, Lausanne, Switzerland
    S. Zuber
    Société des Produits Nestlé, Nestlé Research, Institute of Food Safety and Analytical Science, Lausanne, Switzerland

    Editor

    Christopher A. Elkins
    Editor
    Centers for Disease Control and Prevention

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  • Applied and Environmental MicrobiologyArticle
    Biofilms and Coronavirus Reservoirs: a Perspective Review

    ABSTRACT

    Bats are a key reservoir of coronaviruses (CoVs), including the agent of the severe acute respiratory syndrome, SARS-CoV-2, responsible for the recent deadly viral pneumonia pandemic. However, understanding how bats can harbor several microorganisms without developing illnesses is still a matter under discussion. Viruses and other pathogens are often studied as stand-alone entities, despite that, in nature, they mostly live in multispecies associations called biofilms—both externally and within the host. Microorganisms in biofilms are enclosed by an extracellular matrix that confers protection and improves survival. Previous studies have shown that viruses can secondarily colonize preexisting biofilms, and viral biofilms have also been described. In this review, we raise the perspective that CoVs can persistently infect bats due to their association with biofilm structures. This phenomenon potentially provides an optimal environment for nonpathogenic and well-adapted viruses to interact with the host, as well as for viral recombination. Biofilms can also enhance virion viability in extracellular environments, such as on fomites and in aquatic sediments, allowing viral persistence and dissemination. Moreover, understanding the biofilm lifestyle of CoVs in reservoirs might contribute to explaining several burning questions as to persistence and transmissibility of highly pathogenic emerging CoVs.

    REFERENCES

    1.
    Schlesinger WH. 2006. Global change ecology. Trends Ecol Evol 21:348–351.
    2.
    Palmer M, Bernhardt E, Chornesky E, Collins S, Dobson A, Duke C, Gold B, Jacobson R, Kingsland S, Kranz R, Mappin M, Martinez ML, Micheli F, Morse J, Pace M, Pascual M, Palumbi S, Reichman OJ, Simons A, Townsend A, Turner M. 2004. Ecology. Ecology for a crowded planet. Science 304:1251–1252.
    3.
    Bavel JJV, Baicker K, Boggio PS, Capraro V, Cichocka A, Cikara M, Crockett MJ, Crum AJ, Douglas KM, Druckman JN, Drury J, Dube O, Ellemers N, Finkel EJ, Fowler JH, Gelfand M, Han S, Haslam SA, Jetten J, Kitayama S, Mobbs D, Napper LE, Packer DJ, Pennycook G, Peters E, Petty RE, Rand DG, Reicher SD, Schnall S, Shariff A, Skitka LJ, Smith SS, Sunstein CR, Tabri N, Tucker JA, Linden SVD, Lange PV, Weeden KA, Wohl MJA, Zaki J, Zion SR, Willer R. 2020. Using social and behavioural science to support COVID-19 pandemic response. Nat Hum Behav 4:460–471.
    4.
    Bastone P, Truyen U, Löchelt M. 2003. Potential of zoonotic transmission of non-primate foamy viruses to humans. J Vet Med B Infect Dis Vet Public Health 50:417–423.
    5.
    Nature. 1968. Virology: coronaviruses. Nature 220:650.
    6.
    Baudette FR, Hudson CB. 1933. New recognized poultry disease. North Am Vet 14:50–54.
    7.
    McClurkin AW. 1977. Probable role of viruses in calfhood diseases. J Dairy Sci 60:278–282.
    8.
    Lai MM. 1987. Molecular biology of coronavirus 1986. Adv Exp Med Biol 218:7–13.
    9.
    Mostl K. 1990. Coronaviridae, pathogenetic and clinical aspects: an update. Comp Immunol Microbiol Infect Dis 13:169–180.
    10.
    Al-Tawfiq JA. 2013. Middle East Respiratory Syndrome-coronavirus infection: an overview. J Infect Public Health 6:319–322.
    11.
    Al-Tawfiq JA, Smallwood CA, Arbuthnott KG, Malik MS, Barbeschi M, Memish ZA. 2013. Emerging respiratory and novel coronavirus 2012 infections and mass gatherings. East Mediterr Health J 19:S48–54.
    12.
    Bermingham A, Chand MA, Brown CS, Aarons E, Tong C, Langrish C, Hoschler K, Brown K, Galiano M, Myers R, Pebody RG, Green HK, Boddington NL, Gopal R, Price N, Newsholme W, Drosten C, Fouchier RA, Zambon M. 2012. Severe respiratory illness caused by a novel coronavirus, in a patient transferred to the United Kingdom from the Middle East, September 2012. Euro Surveill 17:20290.
    13.
    World Health Organization. 2020. Middle East respiratory syndrome coronavirus. World Health Organization Press, Geneva, Switzerland.
    14.
    World Health Organization. 2020. Novel coronavirus 2019. World Health Organization Press, Geneva, Switzerland.
    15.
    Zhou H, Chen X, Hu T, Li J, Song H, Liu Y, Wang P, Liu D, Yang J, Holmes EC, Hughes AC, Bi Y, Shi W. 2020. A novel bat coronavirus closely related to SARS-CoV-2 contains natural insertions at the S1/S2 cleavage site of the spike protein. Curr Biol 30:2196–2203.
    16.
    Huang C, Wang Y, Li X, Ren L, Zhao J, Hu Y, Zhang L, Fan G, Xu J, Gu X, Cheng Z, Yu T, Xia J, Wei Y, Wu W, Xie X, Yin W, Li H, Liu M, Xiao Y, Gao H, Guo L, Xie J, Wang G, Jiang R, Gao Z, Jin Q, Wang J, Cao B. 2020. Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet 395:497–506.
    17.
    Chen Y, Liu Q, Guo D. 2020. Emerging coronaviruses: genome structure, replication, and pathogenesis. J Med Virol 92:418–423.
    18.
    Perlman S, Netland J. 2009. Coronaviruses post-SARS: update on replication and pathogenesis. Nat Rev Microbiol 7:439–450.
    19.
    Neuman BW, Buchmeier MJ. 2016. Supramolecular architecture of the coronavirus particle. Adv Virus Res 96:1–27.
    20.
    Hu B, Guo H, Zhou P, Shi Z-L. 2021. Characteristics of SARS-CoV-2 and COVID-19. Nat Rev Microbiol 19:141–154.
    21.
    Sallard E, Halloy J, Casane D, Decroly E, van Helden J. 2021. Tracing the origins of SARS-COV-2 in coronavirus phylogenies: a review. Environ Chem Lett 19:769–717.
    22.
    Heinrich S, Wittman TA, Ross JV, Shepherd CR, Challender DWS, Cassey P. 2017. The global trafficking of pangolins: a comprehensive summary of seizures and trafficking routes from 2010–2015. https://www.traffic.org/publications/reports/the-global-trafficking-of-pangolins/.
    23.
    Ye ZW, Yuan S, Yuen KS, Fung SY, Chan CP, Jin DY. 2020. Zoonotic origins of human coronaviruses. Int J Biol Sci 16:1686–1697.
    24.
    Guan Y, Zheng BJ, He YQ, Liu XL, Zhuang ZX, Cheung CL, Luo SW, Li PH, Zhang LJ, Guan YJ, Butt KM, Wong KL, Chan KW, Lim W, Shortridge KF, Yuen KY, Peiris JS, Poon LL. 2003. Isolation and characterization of viruses related to the SARS coronavirus from animals in southern China. Science 302:276–278.
    25.
    Song HD, Tu CC, Zhang GW, Wang SY, Zheng K, Lei LC, Chen QX, Gao YW, Zhou HQ, Xiang H, Zheng HJ, Chern SW, Cheng F, Pan CM, Xuan H, Chen SJ, Luo HM, Zhou DH, Liu YF, He JF, Qin PZ, Li LH, Ren YQ, Liang WJ, Yu YD, Anderson L, Wang M, Xu RH, Wu XW, Zheng HY, Chen JD, Liang G, Gao Y, Liao M, Fang L, Jiang LY, Li H, Chen F, Di B, He LJ, Lin JY, Tong S, Kong X, Du L, Hao P, Tang H, Bernini A, Yu XJ, Spiga O, Guo ZM, Pan HY, He WZ, Manuguerra JC, Fontanet A, Danchin A, Niccolai N, Li YX, Wu CI, et al. 2005. Cross-host evolution of severe acute respiratory syndrome coronavirus in palm civet and human. Proc Natl Acad Sci U S A 102:2430–2435.
    26.
    Tu C, Crameri G, Kong X, Chen J, Sun Y, Yu M, Xiang H, Xia X, Liu S, Ren T, Yu Y, Eaton BT, Xuan H, Wang LF. 2004. Antibodies to SARS coronavirus in civets. Emerg Infect Dis 10:2244–2248.
    27.
    Fan Y, Zhao K, Shi ZL, Zhou P. 2019. Bat coronaviruses in China. Viruses 11:210.
    28.
    Hu B, Zeng LP, Yang XL, Ge XY, Zhang W, Li B, Xie JZ, Shen XR, Zhang YZ, Wang N, Luo DS, Zheng XS, Wang MN, Daszak P, Wang LF, Cui J, Shi ZL. 2017. Discovery of a rich gene pool of bat SARS-related coronaviruses provides new insights into the origin of SARS coronavirus. PLoS Pathog 13:e1006698.
    29.
    Ge X, Li Y, Yang X, Zhang H, Zhou P, Zhang Y, Shi Z. 2012. Metagenomic analysis of viruses from bat fecal samples reveals many novel viruses in insectivorous bats in China. J Virol 86:4620–4630.
    30.
    Cui J, Li F, Shi ZL. 2019. Origin and evolution of pathogenic coronaviruses. Nat Rev Microbiol 17:181–192.
    31.
    Chan JF, Lau SK, To KK, Cheng VC, Woo PC, Yuen KY. 2015. Middle East respiratory syndrome coronavirus: another zoonotic betacoronavirus causing SARS-like disease. Clin Microbiol Rev 28:465–522.
    32.
    Raj VS, Farag EA, Reusken CB, Lamers MM, Pas SD, Voermans J, Smits SL, Osterhaus AD, Al-Mawlawi N, Al-Romaihi HE, AlHajri MM, El-Sayed AM, Mohran KA, Ghobashy H, Alhajri F, Al-Thani M, Al-Marri SA, El-Maghraby MM, Koopmans MP, Haagmans BL. 2014. Isolation of MERS coronavirus from a dromedary camel, Qatar, 2014. Emerg Infect Dis 20:1339–1342.
    33.
    Eckerle I, Corman VM, Müller MA, Lenk M, Ulrich RG, Drosten C. 2014. Replicative capacity of MERS coronavirus in livestock cell lines. Emerg Infect Dis 20:276–279.
    34.
    Fakhoury H, Hajeer A. 2015. Re-emerging Middle East respiratory syndrome coronavirus: the hibernating bat hypothesis. Ann Thorac Med 10:218–219.
    35.
    Zhou P, Yang XL, Wang XG, Hu B, Zhang L, Zhang W, Si HR, Zhu Y, Li B, Huang CL, Chen HD, Chen J, Luo Y, Guo H, Jiang RD, Liu MQ, Chen Y, Shen XR, Wang X, Zheng XS, Zhao K, Chen QJ, Deng F, Liu LL, Yan B, Zhan FX, Wang YY, Xiao GF, Shi ZL. 2020. A pneumonia outbreak associated with a new coronavirus of probable bat origin. Nature 579:270–273.
    36.
    Xiao K, Zhai J, Feng Y, Zhou N, Zhang X, Zou J-J, Li N, Guo Y, Li X, Shen X, Zhang Z, Shu F, Huang W, Li Y, Zhang Z, Chen R-A, Wu Y-J, Peng S-M, Huang M, Xie W-J, Cai Q-H, Hou F-H, Chen W, Xiao L, Shen Y. 2020. Isolation of SARS-CoV-2-related coronavirus from Malayan pangolins. Nature 583:286–289.
    37.
    Wahba L, Jain N, Fire AZ, Shoura MJ, Artiles KL, McCoy MJ, Jeong DE. 2020. An extensive meta-metagenomic search identifies SARS-CoV-2-homologous sequences in pangolin lung viromes. mSphere 5:e00160-20.
    38.
    Liu J, Zheng X, Tong Q, Li W, Wang B, Sutter K, Trilling M, Lu M, Dittmer U, Yang D. 2020. Overlapping and discrete aspects of the pathology and pathogenesis of the emerging human pathogenic coronaviruses SARS-CoV, MERS-CoV, and 2019-nCoV. J Med Virol 92:491–494.
    39.
    Banerjee A, Kulcsar K, Misra V, Frieman M, Mossman K. 2019. Bats and coronaviruses. Viruses 11:41.
    40.
    Drexler JF, Corman VM, Wegner T, Tateno AF, Zerbinati RM, Gloza-Rausch F, Seebens A, Müller MA, Drosten C. 2011. Amplification of emerging viruses in a bat colony. Emerg Infect Dis 17:449–456.
    41.
    Quan PL, Firth C, Conte JM, Williams SH, Zambrana-Torrelio CM, Anthony SJ, Ellison JA, Gilbert AT, Kuzmin IV, Niezgoda M, Osinubi MO, Recuenco S, Markotter W, Breiman RF, Kalemba L, Malekani J, Lindblade KA, Rostal MK, Ojeda-Flores R, Suzan G, Davis LB, Blau DM, Ogunkoya AB, Alvarez Castillo DA, Moran D, Ngam S, Akaibe D, Agwanda B, Briese T, Epstein JH, Daszak P, Rupprecht CE, Holmes EC, Lipkin WI. 2013. Bats are a major natural reservoir for hepaciviruses and pegiviruses. Proc Natl Acad Sci U S A 110:8194–8199.
    42.
    Ciminski K, Pfaff F, Beer M, Schwemmle M. 2020. Bats reveal the true power of influenza A virus adaptability. PLoS Pathog 16:e1008384.
    43.
    Teeling EC, Springer MS, Madsen O, Bates P, O'Brien SJ, Murphy WJ. 2005. A molecular phylogeny for bats illuminates biogeography and the fossil record. Science 307:580–584.
    44.
    Wassenaar TM, Zou Y. 2020. 2019_nCoV/SARS-CoV-2: rapid classification of betacoronaviruses and identification of Traditional Chinese Medicine as potential origin of zoonotic coronaviruses. Lett Appl Microbiol 70:342–348.
    45.
    Flemming HC, Wuertz S. 2019. Bacteria and archaea on Earth and their abundance in biofilms. Nat Rev Microbiol 17:247–260.
    46.
    Kernien JF, Snarr BD, Sheppard DC, Nett JE. 2017. The interface between fungal biofilms and innate immunity. Front Immunol 8:1968.
    47.
    Mateus MD. 2017. Bridging the gap between knowing and modeling viruses in marine systems—an upcoming frontier. Front Mar Sci 3.
    48.
    Flemming H-C, Wingender J. 2010. The biofilm matrix. Nat Rev Microbiol 8:623–633.
    49.
    Olsen I. 2015. Biofilm-specific antibiotic tolerance and resistance. Eur J Clin Microbiol Infect Dis 34:877–886.
    50.
    Flemming HC. 2020. Biofouling and me: my Stockholm syndrome with biofilms. Water Res 173:115576.
    51.
    Quignon F, Sardin M, Kiene L, Schwartzbrod L. 1997. Poliovirus-1 inactivation and interaction with biofilm: a pilot-scale study. Appl Environ Microbiol 63:978–982.
    52.
    Skraber S, Ogorzaly L, Helmi K, Maul A, Hoffmann L, Cauchie HM, Gantzer C. 2009. Occurrence and persistence of enteroviruses, noroviruses and F-specific RNA phages in natural wastewater biofilms. Water Res 43:4780–4789.
    53.
    Storey MV, Ashbolt NJ. 2001. Persistence of two model enteric viruses (B40-8 and MS-2 bacteriophages) in water distribution pipe biofilms. Water Sci Technol 43:133–138.
    54.
    Helmi K, Skraber S, Gantzer C, Willame R, Hoffmann L, Cauchie HM. 2008. Interactions of Cryptosporidium parvum, Giardia lamblia, vaccinal poliovirus type 1, and bacteriophages phiX174 and MS2 with a drinking water biofilm and a wastewater biofilm. Appl Environ Microbiol 74:2079–2088.
    55.
    Flemming H-C, Percival SL, Walker JT. 2002. Contamination potential of biofilms in water distribution systems. Water Supply 2:271–280.
    56.
    Storey MV, Ashbolt NJ. 2003. Enteric virions and microbial biofilms—a secondary source of public health concern? Water Sci Technol 48:97–104.
    57.
    Ahmed W, Angel N, Edson J, Bibby K, Bivins A, O'Brien JW, Choi PM, Kitajima M, Simpson SL, Li J, Tscharke B, Verhagen R, Smith WJM, Zaugg J, Dierens L, Hugenholtz P, Thomas KV, Mueller JF. 2020. First confirmed detection of SARS-CoV-2 in untreated wastewater in Australia: a proof of concept for the wastewater surveillance of COVID-19 in the community. Sci Total Environ 728:138764.
    58.
    Wang W, Xu Y, Gao R, Lu R, Han K, Wu G, Tan W. 2020. Detection of SARS-CoV-2 in different types of clinical specimens. JAMA 323:1843–1844.
    59.
    Xiang Z, Koo H, Chen Q, Zhou X, Liu Y, Simon-Soro A. 2020. Potential implications of SARS-CoV-2 oral infection in the host microbiota. J Oral Microbiol 13:1853451.
    60.
    Mazaheritehrani E, Sala A, Orsi CF, Neglia RG, Morace G, Blasi E, Cermelli C. 2014. Human pathogenic viruses are retained in and released by Candida albicans biofilm in vitro. Virus Res 179:153–160.
    61.
    Wingender J, Flemming HC. 2011. Biofilms in drinking water and their role as reservoir for pathogens. Int J Hyg Environ Health 214:417–423.
    62.
    Vasickova P, Pavlik I, Verani M, Carducci A. 2010. Issues concerning survival of viruses on surfaces. Food Environ Virol 2:24–34.
    63.
    Pais-Correia AM, Sachse M, Guadagnini S, Robbiati V, Lasserre R, Gessain A, Gout O, Alcover A, Thoulouze MI. 2010. Biofilm-like extracellular viral assemblies mediate HTLV-1 cell-to-cell transmission at virological synapses. Nat Med 16:83–89.
    64.
    Thoulouze MI, Alcover A. 2011. Can viruses form biofilms? Trends Microbiol 19:257–262.
    65.
    Sanjuán R. 2017. Collective infectious units in viruses. Trends Microbiol 25:402–412.
    66.
    Sanjuán R, Thoulouze MI. 2019. Why viruses sometimes disperse in groups? Virus Evol 5:vez014.
    67.
    Andreu-Moreno I, Sanjuán R. 2020. Collective viral spread mediated by virion aggregates promotes the evolution of defective interfering particles. mBio 11:e02156-19.
    68.
    Tozzi A, Peters J, Annesi-Maesano I, D'Amato G. 2020. Collective clustering dynamics of SARS-COV-2 particles. Preprints
    69.
    Belouzard S, Millet JK, Licitra BN, Whittaker GR. 2012. Mechanisms of coronavirus cell entry mediated by the viral spike protein. Viruses 4:1011–1033.
    70.
    Balzarini J. 2007. Carbohydrate-binding agents: a potential future cornerstone for the chemotherapy of enveloped viruses? Antivir Chem Chemother 18:1–11.
    71.
    Balzarini J. 2007. Targeting the glycans of glycoproteins: a novel paradigm for antiviral therapy. Nat Rev Microbiol 5:583–597.
    72.
    Bordería AV, Isakov O, Moratorio G, Henningsson R, Agüera-González S, Organtini L, Gnädig NF, Blanc H, Alcover A, Hafenstein S, Fontes M, Shomron N, Vignuzzi M. 2015. Group selection and contribution of minority variants during virus adaptation determines virus fitness and phenotype. PLoS Pathog 11:e1004838.
    73.
    Bakaletz LO. 2017. Viral-bacterial co-infections in the respiratory tract. Curr Opin Microbiol 35:30–35.
    74.
    Zhu X, Ge Y, Wu T, Zhao K, Chen Y, Wu B, Zhu F, Zhu B, Cui L. 2020. Co-infection with respiratory pathogens among COVID-2019 cases. Virus Res 285:198005.
    75.
    Lv Z, Cheng S, Le J, Huang J, Feng L, Zhang B, Li Y. 2020. Clinical characteristics and co-infections of 354 hospitalized patients with COVID-19 in Wuhan, China: a retrospective cohort study. Microbes Infect 22:195–199.
    76.
    Zhang G, Cowled C, Shi Z, Huang Z, Bishop-Lilly KA, Fang X, Wynne JW, Xiong Z, Baker ML, Zhao W, Tachedjian M, Zhu Y, Zhou P, Jiang X, Ng J, Yang L, Wu L, Xiao J, Feng Y, Chen Y, Sun X, Zhang Y, Marsh GA, Crameri G, Broder CC, Frey KG, Wang LF, Wang J. 2013. Comparative analysis of bat genomes provides insight into the evolution of flight and immunity. Science 339:456–460.
    77.
    Sulkin SE, Allen R. 1974. Virus infections in bats. Monogr Virol 8:1–103.
    78.
    Plowright RK, Peel AJ, Streicker DG, Gilbert AT, McCallum H, Wood J, Baker ML, Restif O. 2016. Transmission or within-host dynamics driving pulses of zoonotic viruses in reservoir-host populations. PLoS Negl Trop Dis 10:e0004796.
    79.
    Jeong J, Smith CS, Peel AJ, Plowright RK, Kerlin DH, McBroom J, McCallum H. 2017. Persistent infections support maintenance of a coronavirus in a population of Australian bats (Myotis macropus). Epidemiol Infect 145:2053–2061.
    80.
    Dominguez SR, O'Shea TJ, Oko LM, Holmes KV. 2007. Detection of group 1 coronaviruses in bats in North America. Emerg Infect Dis 13:1295–1300.
    81.
    Dawley C, Gibson KE. 2019. Virus-bacteria interactions: implications for prevention and control of human enteric viruses from environment to host. Foodborne Pathog Dis 16:81–89.
    82.
    Brook CE, Dobson AP. 2015. Bats as 'special' reservoirs for emerging zoonotic pathogens. Trends Microbiol 23:172–180.
    83.
    Subudhi S, Rapin N, Misra V. 2019. Immune system modulation and viral persistence in bats: understanding viral spillover. Viruses 11:192.
    84.
    Menachery VD, Graham RL, Baric RS. 2017. Jumping species—a mechanism for coronavirus persistence and survival. Curr Opin Virol 23:1–7.
    85.
    Davy CM, Donaldson ME, Subudhi S, Rapin N, Warnecke L, Turner JM, Bollinger TK, Kyle CJ, Dorville NAS, Kunkel EL, Norquay KJO, Dzal YA, Willis CKR, Misra V. 2018. White-nose syndrome is associated with increased replication of a naturally persisting coronaviruses in bats. Sci Rep 8:15508.
    86.
    Leroy EM, Kumulungui B, Pourrut X, Rouquet P, Hassanin A, Yaba P, Délicat A, Paweska JT, Gonzalez JP, Swanepoel R. 2005. Fruit bats as reservoirs of Ebola virus. Nature 438:575–576.
    87.
    Boone SA, Gerba CP. 2007. Significance of fomites in the spread of respiratory and enteric viral disease. Appl Environ Microbiol 73:1687–1696.
    88.
    Spicknall IH, Koopman JS, Nicas M, Pujol JM, Li S, Eisenberg JN. 2010. Informing optimal environmental influenza interventions: how the host, agent, and environment alter dominant routes of transmission. PLoS Comput Biol 6:e1000969.
    89.
    Kampf G, Todt D, Pfaender S, Steinmann E. 2020. Persistence of coronaviruses on inanimate surfaces and their inactivation with biocidal agents. J Hosp Infect 104:246–251.
    90.
    Zuber S, Brüssow H. 2020. COVID 19: challenges for virologists in the food industry. Microb Biotechnol 13:1689–1701.
    91.
    Otter JA, Donskey C, Yezli S, Douthwaite S, Goldenberg SD, Weber DJ. 2016. Transmission of SARS and MERS coronaviruses and influenza virus in healthcare settings: the possible role of dry surface contamination. J Hosp Infect 92:235–250.
    92.
    Otter JA, Yezli S, French GL. 2011. The role played by contaminated surfaces in the transmission of nosocomial pathogens. Infect Control Hosp Epidemiol 32:687–699.
    93.
    Dowell SF, Simmerman JM, Erdman DD, Wu JS, Chaovavanich A, Javadi M, Yang JY, Anderson LJ, Tong S, Ho MS. 2004. Severe acute respiratory syndrome coronavirus on hospital surfaces. Clin Infect Dis 39:652–657.
    94.
    Thomas Y, Vogel G, Wunderli W, Suter P, Witschi M, Koch D, Tapparel C, Kaiser L. 2008. Survival of influenza virus on banknotes. Appl Environ Microbiol 74:3002–3007.
    95.
    Liu Z, Xiao X, Wei X, Li J, Yang J, Tan H, Zhu J, Zhang Q, Wu J, Liu L. 2020. Composition and divergence of coronavirus spike proteins and host ACE2 receptors predict potential intermediate hosts of SARS-CoV-2. J Med Virol 92:595–601.
    96.
    Almeida JD, Berry DM, Cunningham CH, Hamre D, Hofstad MS, Mallucci L, McIntosh K, Tyrrell DAJ. 1968. Virology: coronaviruses. Nature 220:650.

    Author Bios

    Rafael Gomes Von Borowski https://orcid.org/0000-0003-1764-944X
    Université de Rennes, CNRS, Institut de Génétique et Développement de Rennes (IGDR) UMR6290, Rennes, France
    Rafael Gomes Von Borowski is a pharmacist and Ph.D. in Pharmaceutical Sciences (Federal University of Rio Grande do Sul, Brazil) and Microbiology (University of Rennes 1, France). His doctoral thesis received honorable mention and a Rennes 1 Foundation Theses Award. After an experience in a public hospital in the south of Brazil, he has been working in the Research and Development departments of public and private laboratories. He is particularly interested in new strategies and natural antimicrobials to control infectious disease. Currently, he is responsible for the development of a diagnostic test at a pharmaceutical biotechnology company specializing in human phage therapy.
    Departamento de Ciências Básicas da Saúde, Universidade Federal de Ciências da Saúde de Porto Alegre (UFCSPA), Porto Alegre, Brazil
    Danielle Silva Trentin is a pharmacist and holds an M.Sc. (2009) and Ph.D. (2013) in Pharmaceutical Sciences from the Federal University of Rio Grande do Sul (UFRGS), Porto Alegre, Brazil. Her thesis received honorable mention via the Brazilian national award “CAPES Theses Award,” field of Pharmacy. From 2013 to 2016, she completed postdoctoral fellowships at UFRGS. Since 2017, she has held the adjunct professor position at the Department of Basic Health Sciences at the Federal University of Health Sciences of Porto Alegre (Porto Alegre, Brazil), in Microbiology. She was awarded grant funding by the Serrapilheira Institute and is leader of the research group “Bacteriology and Alternative Experimental Models.” Her research interests are focused on microbial virulence factors, including biofilms, as an approach to control infectious disease. Currently, she is working with Galleria mellonella larvae as an experimental host to evaluate in vivo virulence-attenuating compounds and as an animal model to study plastic biodegradation.

    Information & Contributors

    Information

    Published In

    Applied and Environmental Microbiology
    Volume 87Number 1826 August 2021
    eLocator: e00859-21
    Editor: Karyn N. Johnson, University of Queensland
    PubMed: 34190608

    History

    Accepted manuscript posted online: 30 June 2021
    Published online: 26 August 2021

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    KEYWORDS

    1. coronaviruses
    2. biofilm
    3. host
    4. bat
    5. microbial interaction
    6. persistent infection

    Contributors

    Authors

    Rafael Gomes Von Borowski https://orcid.org/0000-0003-1764-944X
    Université de Rennes, CNRS, Institut de Génétique et Développement de Rennes (IGDR) UMR6290, Rennes, France
    Departamento de Ciências Básicas da Saúde, Universidade Federal de Ciências da Saúde de Porto Alegre (UFCSPA), Porto Alegre, Brazil

    Editor

    Karyn N. Johnson
    Editor
    University of Queensland

    Notes

    Rafael Gomes Von Borowski and Danielle Silva Trentin contributed equally to this work. Author order was determined by common agreement in order of increasing seniority.

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  • Applied and Environmental MicrobiologyArticle
    Soil Aggregate Microbial Communities: Towards Understanding Microbiome Interactions at Biologically Relevant Scales

    ABSTRACT

    Soils contain a tangle of minerals, water, nutrients, gases, plant roots, decaying organic matter, and microorganisms which work together to cycle nutrients and support terrestrial plant growth. Most soil microorganisms live in periodically interconnected communities closely associated with soil aggregates, i.e., small (<2 mm), strongly bound clusters of minerals and organic carbon that persist through mechanical disruptions and wetting events. Their spatial structure is important for biogeochemical cycling, and we cannot reliably predict soil biological activities and variability by studying bulk soils alone. To fully understand the biogeochemical processes at work in soils, it is necessary to understand the micrometer-scale interactions that occur between soil particles and their microbial inhabitants. Here, we review the current state of knowledge regarding soil aggregate microbial communities and identify areas of opportunity to study soil ecosystems at a scale relevant to individual cells. We present a framework for understanding aggregate communities as “microbial villages” that are periodically connected through wetting events, allowing for the transfer of genetic material, metabolites, and viruses. We describe both top-down (whole community) and bottom-up (reductionist) strategies for studying these communities. Understanding this requires combining “model system” approaches (e.g., developing mock community artificial aggregates), field observations of natural communities, and broader study of community interactions to include understudied community members, like viruses. Initial studies suggest that aggregate-based approaches are a critical next step for developing a predictive understanding of how geochemical and community interactions govern microbial community structure and nutrient cycling in soil.

    REFERENCES

    1.
    Ciric V, Manojlovic M, Nesic L, Belic M. 2012. Soil dry aggregate size distribution: effects of soil type and land use. J Soil Sci Plant Nutr 12:689–703.
    2.
    Graham EB, Knelman JE, Schindlbacher A, Siciliano S, Breulmann M, Yannarell A, Beman JM, Abell G, Philippot L, Prosser J, Foulquier A, Yuste JC, Glanville HC, Jones DL, Angel R, Salminen J, Newton RJ, Burgmann H, Ingram LJ, Hamer U, Siljanen HM, Peltoniemi K, Potthast K, Baneras L, Hartmann M, Banerjee S, Yu RQ, Nogaro G, Richter A, Koranda M, Castle SC, Goberna M, Song B, Chatterjee A, Nunes OC, Lopes AR, Cao Y, Kaisermann A, Hallin S, Strickland MS, Garcia-Pausas J, Barba J, Kang H, Isobe K, Papaspyrou S, Pastorelli R, Lagomarsino A, Lindstrom ES, Basiliko N, Nemergut DR. 2016. Microbes as engines of ecosystem function: when does community structure enhance predictions of ecosystem processes? Front Microbiol 7:214.
    3.
    Six J, Bossuyt H, Degryze S, Denef K. 2004. A history of research on the link between (micro)aggregates, soil biota, and soil organic matter dynamics. Soil Tillage Res 79:7–31.
    4.
    De Gryze S, Six J, Merckx R. 2006. Quantifying water-stable soil aggregate turnover and its implication for soil organic matter dynamics in a model study. Eur J Soil Sci 57:693–707.
    5.
    Six J, Elliott ET, Paustian K. 2000. Soil macroaggregate turnover and microaggregate formation: a mechanism for C sequestration under no-tillage agriculture. Soil Biol Biochem 32:2099–2103.
    6.
    Sexstone AJ, Revsbech NP, Parkin TB, Tiedje JM. 1985. Direct measurement of oxygen profiles and denitrification rates in soil aggregates. Soil Sci Soc Am J 49:645–651.
    7.
    Carminati A, Kaestner A, Ippisch O, Koliji A, Lehmann P, Hassanein R, Vontobel P, Lehmann E, Laloui L, Vulliet L, Flühler H. 2007. Water flow between soil aggregates. Transp Porous Media 68:219–236.
    8.
    Ebrahimi A, Or D. 2016. Microbial community dynamics in soil aggregates shape biogeochemical gas fluxes from soil profiles–upscaling an aggregate biophysical model. Glob Change Biol 22:3141–3156.
    9.
    Bailey VL, McCue LA, Fansler SJ, Boyanov MI, DeCarlo F, Kemner KM, Konopka A. 2013. Micrometer-scale physical structure and microbial composition of soil macroaggregates. Soil Biol Biochem 65:60–68.
    10.
    Sessitsch A, Weilharter A, Gerzabek MH, Kirchmann H, Kandeler E. 2001. Microbial population structures in soil particle size fractions of a long-term fertilizer field experiment. Appl Environ Microbiol 67:4215–4224.
    11.
    Weitz JS, Wilhelm SW. 2012. Ocean viruses and their effects on microbial communities and biogeochemical cycles. F1000 Biol Rep 4:17.
    12.
    Crawford JW, Deacon L, Grinev D, Harris JA, Ritz K, Singh BK, Young I. 2012. Microbial diversity affects self-organization of the soil-microbe system with consequences for function. J R Soc Interface 9:1302–1310.
    13.
    Lynch JM. 1981. Promotion and inhibition of soil aggregate stabilization by micro-organisms. Microbiology 126:371–375.
    14.
    Lynch JM, Bragg E. 1985. Microorganisms and soil aggregate stability, p 133–171. In Stewart BA (ed), Advances in soil science, vol 2. Springer, New York, NY.
    15.
    Edwards AP, Bremner JM. 1967. Microaggregates in soils. J Soil Sci 18:64–73.
    16.
    Oades JM, Waters AG. 1991. Aggregate hierarchy in soils. Soil Res 29:815–828.
    17.
    Bravo AG, Zopfi J, Buck M, Xu J, Bertilsson S, Schaefer JK, Pote J, Cosio C. 2018. Geobacteraceae are important members of mercury-methylating microbial communities of sediments impacted by waste water releases. ISME J 12:802–812.
    18.
    Jastrow JD, Miller RM, Lussenhop J. 1998. Contributions of interacting biological mechanisms to soil aggregate stabilization in restored prairie. Soil Biol Biochem 30:905–916.
    19.
    Tisdall JM, Oades JM. 1982. Organic-matter and water-stable aggregates in soils. J Soil Sci 33:141–163.
    20.
    Totsche KU, Amelung W, Gerzabek MH, Guggenberger G, Klumpp E, Knief C, Lehndorff E, Mikutta R, Peth S, Prechtel A, Ray N, Kögel-Knabner I. 2018. Microaggregates in soils. J Plant Nutr Soil Sci 181:104–136.
    21.
    Christensen BT. 2001. Physical fractionation of soil and structural and functional complexity in organic matter turnover. Eur J Soil Sci 52:345–353.
    22.
    Martin J, Martin W, Page JB, Raney WA, de Ment JD. 1955. Soil aggregation, p 1–37. In Norman AG (ed), Advances in agronomy, vol 7. Academic Press Inc, New York, NY.
    23.
    Ettema CH, Wardle DA. 2002. Spatial soil ecology. Trends Ecol Evol 17:177–183.