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Environmental Microbiology
Research Article
6 July 2023

Phytoplankton Producer Species and Transformation of Released Compounds over Time Define Bacterial Communities following Phytoplankton Dissolved Organic Matter Pulses


Phytoplankton-bacterium interactions are mediated, in part, by phytoplankton-released dissolved organic matter (DOMp). Two factors that shape the bacterial community accompanying phytoplankton are (i) the phytoplankton producer species, defining the initial composition of released DOMp, and (ii) the DOMp transformation over time. We added phytoplankton DOMp from the diatom Skeletonema marinoi and the cyanobacterium Prochlorococcus marinus MIT9312 to natural bacterial communities from the eastern Mediterranean and determined the bacterial responses over a time course of 72 h in terms of cell numbers, bacterial production, alkaline phosphatase activity, and changes in active bacterial community composition based on rRNA amplicon sequencing. Both DOMp types were demonstrated to serve the bacterial community as carbon and, potentially, phosphorus sources. Bacterial communities in diatom-derived DOM treatments maintained higher Shannon diversities throughout the experiment and yielded higher bacterial production and lower alkaline phosphatase activity compared to cyanobacterium-derived DOM after 24 h of incubation (but not after 48 and 72 h), indicating greater bacterial usability of diatom-derived DOM. Bacterial communities significantly differed between DOMp types as well as between different incubation times, pointing to a certain bacterial specificity for the DOMp producer as well as a successive utilization of phytoplankton DOM by different bacterial taxa over time. The highest differences in bacterial community composition with DOMp types occurred shortly after DOMp additions, suggesting a high specificity toward highly bioavailable DOMp compounds. We conclude that phytoplankton-associated bacterial communities are strongly shaped by the phytoplankton producer as well as the transformation of its released DOMp over time.
IMPORTANCE Phytoplankton-bacterium interactions influence biogeochemical cycles of global importance. Phytoplankton photosynthetically fix carbon dioxide and subsequently release the synthesized compounds as dissolved organic matter (DOMp), which becomes processed and recycled by heterotrophic bacteria. Yet the importance of phytoplankton producers in combination with the time-dependent transformation of DOMp compounds on the accompanying bacterial community has not been explored in detail. The diatom Skeletonema marinoi and the cyanobacterium Prochlorococcus marinus MIT9312 belong to globally important phytoplankton genera, and our study revealed that DOMp of both species was selectively incorporated by the bacterial community. The producer species had the highest impact shortly after DOMp appropriation, and its effect diminished over time. Our results improve the understanding of the dynamics of organic matter produced by phytoplankton in the oceans as it is utilized and modified by cooccurring bacteria.

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Field CB, Behrenfeld MJ, Randerson JT, Falkowski P. 1998. Primary production of the biosphere: Integrating terrestrial and oceanic components. Science 281:237–240.
Azam F, Malfatti F. 2007. Microbial structuring of marine ecosystems. Nat Rev Microbiol 5:782–791.
Azam F, Fenchel T, Field J, Gray JS, Meyer-Reil LA, Thingstad F. 1983. The ecological role of water-column microbes in the sea. Mar Ecol Prog Ser 10:257–263.
Roth-Rosenberg D, Aharonovich D, Omta AW, Follows MJ, Sher D. 2021. Dynamic macromolecular composition and high exudation rates in Prochlorococcus. Limnol Oceanogr 66:1759–1773.
Beliaev AS, Romine MF, Serres M, Bernstein HC, Linggi BE, Markillie LM, Isern NG, Chrisler WB, Kucek LA, Hill EA, Pinchuk GE, Bryant DA, Wiley HS, Fredrickson JK, Konopka A. 2014. Inference of interactions in cyanobacterial-heterotrophic co-cultures via transcriptome sequencing. ISME J 8:2243–2255.
Riemann L, Holmfeldt K, Titelman J. 2009. Importance of viral lysis and dissolved DNA for bacterioplankton activity in a P-limited estuary, Northern Baltic Sea. Microb Ecol 57:286–294.
Eigemann F, Rahav E, Grossart H-P, Aharonovich D, Sher D, Vogts A, Voss M. 2022. Phytoplankton exudates provide full nutrition to a subset of accompanying heterotrophic bacteria via carbon, nitrogen and phosphorus allocation. Environ Microbiol 24:2467–2483.
Mühlenbruch M, Grossart HP, Eigemann F, Voss M. 2018. Mini-review: phytoplankton-derived polysaccharides in the marine environment and their interactions with heterotrophic bacteria. Environ Microbiol 20:2671–2685.
Seymour JR, Amin SA, Raina JB, Stocker R. 2017. Zooming in on the phycosphere: the ecological interface for phytoplankton-bacteria relationships. Nat Microbiol 2:17065.
Cole JJ. 1982. Interactions between bacteria and algae in aquatic ecosystems. Annu Rev Ecol Syst 13:291–314.
Amin SA, Hmelo LR, van Tol HM, Durham BP, Carlson LT, Heal KR, Morales RL, Berthiaume CT, Parker MS, Djunaedi B, Ingalls AE, Parsek MR, Moran MA, Armbrust EV. 2015. Interaction and signalling between a cosmopolitan phytoplankton and associated bacteria. Nature 522:98–101.
Christie-Oleza JA, Sousoni D, Lloyd M, Armengaud J, Scanlan DJ. 2017. Nutrient recycling facilitates long-term stability of marine microbial phototroph-heterotroph interactions. Nat Microbiol 2:17100.
Grossart HP, Czub G, Simon M. 2006. Algae-bacteria interactions and their effects on aggregation and organic matter flux in the sea. Environ Microbiol 8:1074–1084.
York A. 2018. Marine biogeochemical cycles in a changing world. Nat Rev Microbiol 16:259–259.
Sison-Mangus MP, Jiang S, Kudela RM, Mehic S. 2016. Phytoplankton-associated bacterial community composition and succession during toxic diatom bloom and non-bloom events. Front Microbiol 7:1433.
Biddanda B, Benner R. 1997. Carbon, nitrogen, and carbohydrate fluxes during the production of particulate and dissolved organic matter by marine phytoplankton. Limnol Oceanogr 42:506–518.
Ríos A, Fraga F, Pérez FF, Figueiras FG. 1998. Chemical composition of phytoplankton and particulate organic matter in the Ría de Vigo (NW Spain). Scientia Marina 62:257–271.
Aluwihare LI, Repeta DJ. 1999. A comparison of the chemical characteristics of oceanic DOM and extracellular DOM produced by marine algae. Mar Ecol Prog Ser 186:105–117.
Castillo CR, Sarmento H, Álvarez-Salgado XA, Gasol JM, Marraséa C. 2010. Production of chromophoric dissolved organic matter by marine phytoplankton. Limnol Oceanogr 55:446–454.
Romera-Castillo C, Sarmento H, Alvarez-Salgado XA, Gasol JM, Marrasé C. 2011. Net production and consumption of fluorescent colored dissolved organic matter by natural bacterial assemblages growing on marine phytoplankton exudates. Appl Environ Microbiol 77:7490–7498.
Meon B, Kirchman DL. 2001. Dynamics and molecular composition of dissolved organic material during experimental phytoplankton blooms. Marine Chemistry 75:185–199.
Becker J, Berube P, Follett C, Waterbury J, Chisholm S, DeLong E, Repeta D. 2014. Closely related phytoplankton species produce similar suites of dissolved organic matter. Front Microbiol 5:111.
Myklestad SM. 2000. Dissolved organic carbon from phytoplankton, p 111–148. In Wangersky PJ (ed), Marine chemistry. Springer, Berlin, Germany.
Landa M, Cottrell MT, Kirchman DL, Kaiser K, Medeiros PM, Tremblay L, Batailler N, Caparros J, Catala P, Escoubeyrou K, Oriol L, Blain S, Obernosterer I. 2014. Phylogenetic and structural response of heterotrophic bacteria to dissolved organic matter of different chemical composition in a continuous culture study. Environ Microbiol 16:1668–1681.
Sarmento H, Romera-Castillo C, Lindh M, Pinhassi J, Sala MM, Gasol JM, Marrase C, Taylor GT. 2013. Phytoplankton species-specific release of dissolved free amino acids and their selective consumption by bacteria. Limnol Oceanogr 58:1123–1135.
Tada Y, Suzuki K. 2016. Changes in the community structure of free-living heterotrophic bacteria in the open tropical Pacific Ocean in response to microalgal lysate-derived dissolved organic matter. FEMS Microbiol Ecol 92:fiw099.
Livanou E, Lagaria A, Psarra S, Lika K. 2017. Dissolved organic matter release by phytoplankton in the context of the dynamic energy budget theory. Biogeosciences 42:1–33.
Xiao X, Guo W, Li X, Wang C, Chen X, Lin X, Weinbauer MG, Zeng Q, Jiao N, Zhang R. 2021. Viral lysis alters the optical properties and biological availability of dissolved organic matter derived from prochlorococcus picocyanobacteria. Appl Environ Microbiol 87:e02271-20.
Gómez-Consarnau L, Lindh MV, Gasol JM, Pinhassi J. 2012. Structuring of bacterioplankton communities by specific dissolved organic carbon compounds. Environ Microbiol 14:2361–2378.
Rooney-Varga JN, Giewat MW, Savin MC, Sood S, LeGresley M, Martin JL. 2005. Links between phytoplankton and bacterial community dynamics in a coastal marine environment. Microb Ecol 49:163–175.
Grossart HP, Levold F, Allgaier M, Simon M, Brinkhoff T. 2005. Marine diatom species harbour distinct bacterial communities. Environ Microbiol 7:860–873.
Buchan A, LeCleir GR, Gulvik CA, Gonzalez JM. 2014. Master recyclers: features and functions of bacteria associated with phytoplankton blooms. Nat Rev Microbiol 12:686–698.
Stock W, Blommaert L, De Troch M, Mangelinckx S, Willems A, Vyverman W, Sabbe K. 2019. Host specificity in diatom–bacteria interactions alleviates antagonistic effects. FEMS Microbiol Ecol 95:fiz171.
Jackrel SL, Yang JW, Schmidt KC, Denef VJ. 2021. Host specificity of microbiome assembly and its fitness effects in phytoplankton. ISME J 15:774–788.
Beier S, Rivers AR, Moran MA, Obernosterer I. 2015. The transcriptional response of prokaryotes to phytoplankton-derived dissolved organic matter in seawater. Environ Microbiol 17:3466–3480.
Kieft B, Li Z, Bryson S, Hettich RL, Pan C, Mayali X, Mueller RS. 2021. Phytoplankton exudates and lysates support distinct microbial consortia with specialized metabolic and ecophysiological traits. Proc Natl Acad Sci USA 118:e2101178118.
Teeling H, Fuchs BM, Becher D, Klockow C, Gardebrecht A, Bennke CM, Kassabgy M, Huang S, Mann AJ, Waldmann J, Weber M, Klindworth A, Otto A, Lange J, Bernhardt J, Reinsch C, Hecker M, Peplies J, Bockelmann FD, Callies U, Gerdts G, Wichels A, Wiltshire KH, Glockner FO, Schweder T, Amann R. 2012. Substrate-controlled succession of marine bacterioplankton populations induced by a phytoplankton bloom. Science 336:608–611.
Teeling H, Fuchs BM, Bennke CM, Kruger K, Chafee M, Kappelmann L, Reintjes G, Waldmann J, Quast C, Glockner FO, Lucas J, Wichels A, Gerdts G, Wiltshire KH, Amann RI. 2016. Recurring patterns in bacterioplankton dynamics during coastal spring algae blooms. Elife 5:e11888.
Hach PF, Marchant HK, Krupke A, Riedel T, Meier DV, Lavik G, Holtappels M, Dittmar T, Kuypers MMM. 2020. Rapid microbial diversification of dissolved organic matter in oceanic surface waters leads to carbon sequestration. Sci Rep 10:13025.
Grossart H-P, Ploug H. 2001. Microbial degradation of organic carbon and nitrogen on diatom aggregates. Limnol Oceanogr 46:267–277.
Jiao N, Herndl GJ, Hansell DA, Benner R, Kattner G, Wilhelm SW, Kirchman DL, Weinbauer MG, Luo T, Chen F, Azam F. 2011. The microbial carbon pump and the oceanic recalcitrant dissolved organic matter pool. Nat Rev Microbiol 9:555–555.
Francis TB, Bartosik D, Sura T, Sichert A, Hehemann J-H, Markert S, Schweder T, Fuchs BM, Teeling H, Amann RI, Becher D. 2021. Changing expression patterns of TonB-dependent transporters suggest shifts in polysaccharide consumption over the course of a spring phytoplankton bloom. ISME J 15:2336–2350.
Arnosti C, Wietz M, Brinkhoff T, Hehemann JH, Probandt D, Zeugner L, Amann R. 2021. The biogeochemistry of marine polysaccharides: sources, inventories, and bacterial drivers of the carbohydrate cycle. Annu Rev Mar Sci 13:81–108.
Raveh O, David N, Rilov G, Rahav E. 2015. The temporal dynamics of coastal phytoplankton and bacterioplankton in the eastern Mediterranean Sea. PLoS One 10:e0140690.
Krom MD, Emeis KC, Van Cappellen P. 2010. Why is the eastern Mediterranean phosphorus limited? Progr Oceanogr 85:236–244.
Krom M, Kress N, Berman-Frank I, Rahav E. 2014. Past, present and future patterns in the nutrient chemistry of the Eastern Mediterranean, p 49–68. In Goffredo S, Dubinsky Z (ed), The Mediterranean Sea: its history and present challenges. Springer Netherlands, Dordrecht, The Netherlands.
White AE, Giovannoni SJ, Zhao Y, Vergin K, Carlson CA. 2019. Elemental content and stoichiometry of SAR11 chemoheterotrophic marine bacteria. Limnol Oceanogr Lett 4:44–51.
Becker S, Scheffel A, Polz MF, Hehemann JH. 2017. Accurate quantification of laminarin in marine organic matter with enzymes from marine microbes. Appl Environ Microbiol 83:e03389-16.
Bhatnagar M, Bhatnagar A. 2019. Diversity of polysaccharides in cyanobacteria, p 447–496. In Satyanarayana T, Johri BN, Das SK (ed), Microbial diversity in ecosystem sustainability and biotechnological applications: volume 1 microbial diversity in normal & extreme environments. Springer Singapore, Singapore.
Sarmento H, Morana C, Gasol JM. 2016. Bacterioplankton niche partitioning in the use of phytoplankton-derived dissolved organic carbon: quantity is more important than quality. ISME J 10:2582–2592.
Becker JW, Hogle SL, Rosendo K, Chisholm SW. 2019. Co-culture and biogeography of Prochlorococcus and SAR11. ISME J 13:1506–1519.
Riemann L, Steward GF, Azam F. 2000. Dynamics of bacterial community composition and activity during a mesocosm diatom bloom. Appl Environ Microbiol 66:578–587.
Pinhassi J, Sala MM, Havskum H, Peters F, Guadayol O, Malits A, Marrasé C. 2004. Changes in bacterioplankton composition under different phytoplankton regimens. Appl Environ Microbiol 70:6753–6766.
Sarmento H, Gasol JM. 2012. Use of phytoplankton-derived dissolved organic carbon by different types of bacterioplankton. Environ Microbiol 14:2348–2360.
Goto S, Tada Y, Suzuki K, Yamashita Y. 2017. Production and reutilization of fluorescent dissolved organic matter by a marine bacterial strain, Alteromonas macleodii. Front Microbiol 8:507.
Dadaglio L, Dinasquet J, Obernosterer I, Joux F. 2018. Differential responses of bacteria to diatom-derived dissolved organic matter in the Arctic Ocean. Aquat Microb Ecol 82:59–72.
Kearney SM, Thomas E, Coe A, Chisholm SW. 2021. Microbial diversity of co-occurring heterotrophs in cultures of marine picocyanobacteria. Environ Microbiome 16:1.
Pontiller B, Martínez-García S, Joglar V, Amnebrink D, Pérez-Martínez C, González JM, Lundin D, Fernández E, Teira E, Pinhassi J. 2022. Rapid bacterioplankton transcription cascades regulate organic matter utilization during phytoplankton bloom progression in a coastal upwelling system. ISME J 16:2360–2372.
Amin SA, Parker MS, Armbrust EV. 2012. Interactions between diatoms and bacteria. Microbiol Mol Biol Rev 76:667–684.
Eigemann F, Schulz-Vogt HN. 2019. Stable and labile associations of microorganisms with the cyanobacterium Nodularia spumigena. Aquat Microb Ecol 83:281–293.
Eigemann F, Hilt S, Salka I, Grossart HP. 2013. Bacterial community composition associated with freshwater algae: species specificity vs. dependency on environmental conditions and source community. FEMS Microbiol Ecol 83:650–663.
Mayerhofer MM, Eigemann F, Lackner C, Hoffmann J, Hellweger FL. 2021. Dynamic carbon flux network of a diverse marine microbial community. ISME Commun 1:50.
Lombard V, Golaconda Ramulu H, Drula E, Coutinho PM, Henrissat B. 2014. The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res 42:D490–D495.
Elovaara S, Eronen-Rasimus E, Asmala E, Tamelander T, Kaartokallio H. 2021. Contrasting patterns of carbon cycling and dissolved organic matter processing in two phytoplankton–bacteria communities. Biogeosciences 18:6589–6616.
Luria CM, Amaral-Zettler LA, Ducklow HW, Repeta DJ, Rhyne AL, Rich JJ. 2017. Seasonal shifts in bacterial community responses to phytoplankton-derived dissolved organic matter in the western Antarctic Peninsula. Front Microbiol 8:2117.
Attermeyer K, Hornick T, Kayler ZE, Bahr A, Zwirnmann E, Grossart HP, Premke K. 2014. Enhanced bacterial decomposition with increasing addition of autochthonous to allochthonous carbon without any effect on bacterial community composition. Biogeosciences 11:1479–1489.
Baltar F, Palovaara J, Unrein F, Catala P, Horňák K, Šimek K, Vaqué D, Massana R, Gasol JM, Pinhassi J. 2016. Marine bacterial community structure resilience to changes in protist predation under phytoplankton bloom conditions. ISME J 10:568–581.
Biller SJ, Berube PM, Lindell D, Chisholm SW. 2015. Prochlorococcus: the structure and function of collective diversity. Nat Rev Microbiol 13:13–27.
Yool A, Tyrrell T. 2003. Role of diatoms in regulating the ocean's silicon cycle. Global Biogeochem Cycles 17.
Grossowicz M, Roth-Rosenberg D, Aharonovich D, Silverman J, Follows MJ, Sher D. 2017. Prochlorococcus in the lab and in silico: the importance of representing exudation. Limnol Oceanogr 62:818–835.
Guillard RRL. 1975. Culture of phytoplankton for feeding marine invertebrates, p 29–60. In Smith WL, Chanley MH (eds), Culture of marine invertebrate animals. Springer, Boston, MA.
Hansen HP, Koroleff F. 1999. Determination of nutrients, p 159–228, Methods of seawater analysis. John Wiley & Sons, New York, NY.
Simon M, Alldredge AL, Azam F. 1990. Bacterial carbon dynamics on marine snow. Mar Ecol Prog Ser 65:205–211.
Thingstad TF, Mantoura RFC. 2005. Titrating excess nitrogen content of phosphorous-deficient eastern Mediterranean surface water using alkaline phosphatase activity as a bio-indicator. Limnol Oceanogr Methods 3:94–100.
Walters W, Hyde ER, Berg-Lyons D, Ackermann G, Humphrey G, Parada A, Gilbert JA, Jansson JK, Caporaso JG, Fuhrman JA, Apprill A, Knight R. 2016. Improved bacterial 16S rRNA gene (V4 and V4-5) and fungal internal transcribed spacer marker gene primers for microbial community surveys. mSystems 1:e00009-15.
Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP. 2016. DADA2: High-resolution sample inference from Illumina amplicon data. Nat Methods 13:581–583.
R Development Team. 2020. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
R Studio Team. 2020. RStudio: integrated development for R. RStudio, PBC, Boston, MA.
Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO. 2013. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590–D596.
Fox J, Weisberg S. 2019. An {R} companion to applied regression, 3rd ed. Sage, Thousand Oaks, CA.
Pohlert T. 2014. The Pairwise Multiple Comparison of Mean Ranks Package (PMCMR). R package.
Ritchie ME, Phipson B, Wu D, Hu Y, Law CW, Shi W, Smyth GK. 2015. limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res 43:e47.
Oksanen J, Kindt R, Legendre P, O’Hara B, Simpson GL, Solymos P, Stevens MHH, Wagner H. 2008. vegan: Community Ecology Package.
Zhao S, Guo Y, Sheng Q, Shyr Y. 2014. Heatmap3: an improved heatmap package with more powerful and convenient features. BMC Bioinformatics 15:P16.
Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C. 2011. Metagenomic biomarker discovery and explanation. Genome Biol 12:R60.
Ginestet C. 2011. ggplot2: elegant graphics for data analysis. J R Stat Soc Series A Stat Soc 174:245–246.

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Published In

cover image Applied and Environmental Microbiology
Applied and Environmental Microbiology
Volume 89Number 726 July 2023
eLocator: e00539-23
Editor: Jennifer B. Glass, Georgia Institute of Technology
PubMed: 37409944


Received: 31 March 2023
Accepted: 19 June 2023
Published online: 6 July 2023


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  1. diatom
  2. Prochlorococcus
  3. phytoplankton DOM
  4. phytoplankton-bacterium interactions
  5. dissolved organic matter



Water Quality Engineering, Technical University of Berlin, Berlin, Germany
Leibniz-Institute for Baltic Sea Research, Warnemuende, Germany
Eyal Rahav
Israel Oceanographic and Limnological Research, Haifa, Israel
Hans-Peter Grossart
Leibniz-Institute of Freshwater Ecology and Inland Fisheries, Berlin, Germany
Potsdam University, Potsdam, Germany
Dikla Aharonovich
Leon H. Charney School of Marine Sciences, University Haifa, Israel
Maren Voss
Leibniz-Institute for Baltic Sea Research, Warnemuende, Germany
Leon H. Charney School of Marine Sciences, University Haifa, Israel


Jennifer B. Glass
Georgia Institute of Technology


The authors declare no conflict of interest.

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