Minireview
30 January 2019

An Update on the Novel Genera and Species and Revised Taxonomic Status of Bacterial Organisms Described in 2016 and 2017

ABSTRACT

Recognition and acknowledgment of novel bacterial taxonomy and nomenclature revisions can impact clinical practice, disease epidemiology, and routine clinical microbiology laboratory operations. The Journal of Clinical Microbiology (JCM) herein presents its biannual report summarizing such changes published in the years 2016 and 2017, as published and added by the International Journal of Systematic and Evolutionary Microbiology. Noteworthy discussion centers around descriptions of novel Corynebacteriaceae and an anaerobic mycolic acid-producing bacterium in the suborder Corynebacterineae; revisions within the Propionibacterium, Clostridium, Borrelia, and Enterobacter genera; and a major reorganization of the family Enterobacteriaceae. JCM intends to sustain this series of reports as advancements in molecular genetics, whole-genome sequencing, and studies of the human microbiome continue to produce novel taxa and clearer understandings of bacterial relatedness.

INTRODUCTION

In 2017, the Journal of Clinical Microbiology (JCM) published its first series of minireviews summarizing newly published novel microbial taxa and revisions to taxonomic nomenclature within the disciplines of bacteriology (1), parasitology (2), virology (3), mycology (4), and mycobacteriology (5). With respect to bacteriology, this itemization and discussion of novel taxa and changes to taxonomy are particularly relevant because these are often the by-products of human microbiome investigations and/or advancements in molecular genetics and genomic sequencing strategies. Applications of taxonomic changes can be broad ranging. The impact on clinical care includes appropriate utilization of antimicrobial susceptibility testing standards in terms of test procurement and data interpretation (6) and a broader understanding of the pathogenesis and epidemiology of emerging pathogens (7, 8). In addition, nomenclature changes can directly impact a given clinical microbiology laboratory from an administrative standpoint (conformity to accreditation checklist standards [9]). In a recent survey on the impact of taxonomic changes on clinical care sent to the American Society for Microbiology ClinMicroNet listserv, several respondents mentioned the challenge of trying to know when changes are made and how to efficiently implement and communicate their relevance to both the laboratory and clinicians (K. Carroll, unpublished data).
As such, we add to the comprehensive capstone previously established (1, 10) by providing a (second) biannual update of novel prokaryotic taxa and bacterial nomenclature revisions published in the years 2016 and 2017. Unless otherwise indicated, the presented organisms were derived from human clinical material and nomenclature designations have been published or added by the International Journal of Systematic and Evolutionary Microbiology (IJSEM).

METHODS

Validly published novel and revised taxa pertinent to prokaryotic species must meet one of two requirements: (i) they must be described in an original investigation published in IJSEM, or (ii) they must be described in a study published in an alternative journal with later inclusion on an approved list in IJSEM. Journals that have published studies providing an effective description of validly named new taxa which may be relevant to the practice of clinical microbiology include Anaerobe; Antonie Van Leeuwenhoek; APMIS; Clinical Microbiology and Infection; Current Microbiology; Diagnostic Microbiology and Infectious Disease; Emerging Microbes and Infections; Frontiers in Genetics; Frontiers in Microbiology; Infection, Genetics and Evolution; Journal of Antimicrobial Chemotherapy; JCM; Journal of General and Applied Microbiology; Microbiology and Immunology; Microbiologyopen; New Microbes and New Infections; Research in Microbiology; Standards in Genomic Sciences; and Systematic and Applied Microbiology. Six times per year, IJSEM publishes papers entitled “List of new names and new combinations previously effectively, but not validly, published” (an example is provided in reference 11). To be considered for inclusion on this approved list, authors must submit a copy of the published article to the editorial office of IJSEM for confirmation that all elements necessary for valid publication have been met. In addition, type strains are to be deposited into recognized culture collections in two separate countries. Taxa on these approved lists may be subject to reclassification on the basis of a synonym designation or transfer to another genus. Within this article, taxa that were previously and effectively described in journals outside of IJSEM are footnoted in such fashion.
All issues of IJSEM published from January 2016 through December 2017 were searched for original articles describing new species taxonomy or accepted changes in taxonomic nomenclature. This audit was further filtered by organisms recovered from human sources. When an initial organism reservoir could not be ascertained, PubMed primary literature searches (U.S. National Library of Medicine and the National Institutes of Health) of the novel or revised taxon attempted to index subsequent case reports for further investigation; several of these case reports are referenced throughout this article. A number of IJSEM publications simply identified isolates as being derived from a specific specimen source (including sterile body sites) but did not provide contextual clinical data. Therefore, in these scenarios (including for a number of novel taxa derived from blood culture), the clinical significance of these taxa was interpreted as “not established” (examples are provided in references 12 to 21). (By way of PubMed primary literature searches, attempts were also made to investigate the uncertain clinical significance of previously reported novel and revised taxa [1]). Additional studies may be necessary to characterize the ultimate clinical significance of novel taxa (22).
Twice per year, IJSEM publishes papers entitled “Notification of changes in taxonomic opinion previously published outside the IJSEM.” The journal publicizes these changes in taxonomic opinion simply as a service to bacteriology, rather than statements of validly published or approved taxonomy. No such reports pertaining to isolates derived from human sources were found in searches of IJSEM literature from 2016 and 2017; two such publications from 2014 and 2015 (23, 24) were noted in the previous minireview (1). Future JCM taxonomy compendia will report pertinent findings from such publications in an effort to subsequently ascertain either the true clinical significance of isolates or determine if official taxonomic status has been granted.

RESULTS AND DISCUSSION

Table 1 is a compilation of novel taxa recovered from human sources stratified by Gram reaction, cellular morphology, and oxygen requirement for growth. Table 2 lists taxonomic revisions for organisms recovered from human sources. Finally, Table 3, on the basis of recent peer-reviewed publications, attempts to retrospectively ascribe clinical significance to a number of organisms whose clinical significance was not established in the previous taxonomy compendium or to add new knowledge for organisms recovered from clinical infections (1). Those findings warranting emphasis are discussed below.
TABLE 1
TABLE 1 New bacterial species recovered from human clinical material reported from January 2016 through December 2017
Scientific nameFamilySourceClinical relevanceGrowth characteristicsReference(s)
Gram-positive cocci     
    Streptococcus halichoeri subsp. hominis subsp. nov.StreptococcaceaeBlood, empyema, sinusAt least one patient had sepsisGram-positive cocci occurring in pairs or chains; non-spore forming; hydrolyzes bile esculin; colony description is similar to the species description provided in reference 25; colonies are white, nonhemolytic, and umbonate; Lancefield group B2527
    Auricoccus indicus gen. nov., sp. nov.StaphylococcaceaeSkinIsolated from the external ear of a healthy humanGram-positive aerobic cocci, nonmotile, non-spore forming; positive for catalase and oxidase; grows between 20 and 40°C, with optimum growth at 35°C28
Gram-positive bacilli     
    Tsukamurella hongkongensis sp. nov.TsukamurellaceaeCorneal scraping; blood cultureIsolated from a patient who had keratitis and a second patient with catheter-related bacteremia; both patients were from Hong KongAerobic, Gram-positive, nonmotile, non-spore-forming bacillus; catalase positive; grows best on Columbia agar with 5% defibrinated sheep blood agar; colonies are orange to red, dry, and rough after 48 h of incubation at 37°C29
    Tsukamurella sinensis sp. nov.TsukamurellaceaeConjunctival swabIsolated from a patient in Hong Kong with conjunctivitisAerobic, Gram-positive, nonmotile, non-spore-forming rod; catalase positive; grows best on Columbia agar with 5% defibrinated sheep blood agar; colonies are white, dry, and rough after 48 h of incubation at 37°C29
    Dermabacter vaginalis sp. nov.DermabacteraceaeVaginal fluidNot established; isolated from vaginal fluid of a Korean femaleFacultative anaerobic, Gram-positive, short bacillus; non-spore forming, nonmotile, catalase positive, oxidase negative; creamy white colonies that grow optimally at 37°C30
    Dermabacter jinjuensis sp. nov.DermabacteraceaePus from a finger woundPatient in a hospital in Jinju, South Korea, with finger necrosisCells are Gram-positive coryneform-like coccobacilli; on sheep blood agar, colonies are gray-white, round, and 0.5–1 mm; growth is optimum at 30–40°C; cells grow under anaerobic conditions and can tolerate NaCl up to 6%; pyrrolidonyl arylamidase positive; acid is produced from a variety of carbohydrates31
    Corynebacterium lowii sp. nov.CorynebacteriaceaeEyeAssociated with ocular infectionsShort to medium-length Gram-positive bacilli that occur singly or in palisades, pairs, or V shapes; colonies are slow growing (72 h), convex smooth gray-white or light beige, nonhemolytic; grows in air, in 5% CO2, and under anaerobic conditions at 37°C or 42°C but not at 25°C; catalase positive, oxidase negative, nonmotile, lipophilic, urease positive, nitrate negative32
    Corynebacterium oculi sp. nov.CorynebacteriaceaeEyeAssociated with ocular infectionsShort to medium-length Gram-positive bacilli that occur singly or in palisades, pairs, or V shapes; colonies are slow growing (72 h), convex smooth gray-white or light beige, nonhemolytic; grows in air, in 5% CO2, and under anaerobic conditions at 37°C and 42°C but not at 25°C; catalase positive, oxidase negative, nonmotile, lipophilic, urease positive, nitrate negative32
    Lawsonella clevelandensis gen. nov., sp. nov.Suborder Corynebacterineae; no family assignmentAbscessesAssociated with a variety of human abscesses in the breast, liver, spine, peritoneumPleomorphic Gram-positive cocci and bacilli; partially acid fast; forms pinpoint, waxy colonies on CDC anaerobic blood agar after 5–7 days of incubation; optimal growth at 35°C in an environment of ≤1.0% oxygen3335
    Nocardia shinanonensis sp. nov.NocardiaceaeEyeIsolated from the aqueous humor from a patient with endophthalmitisAerobic Gram-positive partially acid fast, nonmotile; forms white aerial mycelium; grows at 25, 35, and 45°C36
    Gordonia hongkongensis sp. nov.NocardiaceaeBloodRecovered from two patients: in one from a blood culture and in the other from peritoneal dialysis effluentGram-positive modified acid-fast, nonsporulating bacilli; grows on Columbia agar with 5% defibrinated sheep blood aerobically as pink to orange nonhemolytic colonies; catalase positive; oxidase negative12
    Corynebacterium gottingense sp. nov.CorynebacteriaceaeBloodIsolated from the blood of a patient with bacteremia of unknown origin in Göttingen, GermanyGram-positive, bacillus-shaped bacteria that show typical palisade arrangements of the cells; non-spore forming, catalase positive, oxidase negative; forms white-cream circular colonies on Columbia blood agar13
    Paenibacillus ihumii sp. nov.PaenibacillaceaeaFecesNot established; the isolate was from a female in France prior to bariatric surgeryMotile, spore-forming, Gram-positive bacillus (frequently overdecolorizes in Gram stain); optimal growth at 37°C; capable of growth under microaerophilic and anaerobic conditions; 1- to 2-mm-diameter gray colonies on blood-enriched Columbia agar; catalase and urease negative; utilization of several carbohydrates37b
Gram-negative cocci     
    Neisseria dumasiana sp. nov.NeisseriaceaeSputum (n = 2)Not established; clinical isolates submitted to a U.S. reference laboratory in 2009 and 2012Facultative anaerobic, nonmotile, oxidase-positive Gram-negative coccus or coccobacillus; optimal growth at 37°C; gray-pigmented 1.9- to 2.8-mm-diameter colonies cultivated on chocolate agar plates supplemented with 10% horse blood in 5% CO2; catalase and proline isomerase positive; reduces nitrate to nitrite; acid production from D-glucose but not from maltose or sucrose38
Gram-negative bacilli     
    Enterobacter bugandensis sp. nov.EnterobacteriaceaeBlood (17)Isolates from a neonatal septicemia outbreak in Tanzania; possessed the CTX-M-15 resistance gene; resistant to fluoroquinolone, aminoglycoside, and tetracycline antimicrobialsColonial growth consistent with that of other Enterobacter spp.; lactose fermentation observed only after 24 h of incubation; citrate, arginine dihydrolase, and ornithine decarboxylase positive; lysine decarboxylase, urease, and Voges-Proskauer negative39
    Alkanindiges hongkongensis sp. nov.MoraxellaceaeParotid abscess incision and drainageInfected Warthin’s tumor resulting in parotid gland abscess and peripheral leukocytosis; the patient responded to drainage and amoxicillin-clavulanateAerobic, nonmotile, oxidase-negative Gram-negative coccobacillus; 0.5-mm-diameter (nonhemolytic) colonies on blood and MacConkey agars at 37°C; general failure to ferment or oxidize carbohydrates40c
    Microvirga massiliensis sp. nov.MethylobacteriaceaeFecesNot established; possesses the largest genome (9.2 megabases) of any human isolateAerobic, nonmotile, non-spore-forming, oxidase-negative Gram-negative bacillus; colonies propagated on modified 7H10 medium supplemented with sheep blood; optimal growth at 37°C; leucine arylamidase, nitrate reductase, and cysteine arylamidase positive; alkaline phosphatase negative41d
    Oblitimonas alkaliphila gen. nov., sp. novPseudomonadaceaeUrine (n = 3), leg tissue (n = 2), liver, lung tissue, and foot wound specimensNot established; clinical isolates submitted to a U.S. reference laboratory from 1969 to 1979Microaerophilic, nonmotile, oxidase-positive Gram-negative bacillus; growth on routine bacteriologic media (including blood agar and MacConkey agar); optimal growth at 20–35°C; urea, gelatin, and esculin hydrolysis negative; leucine arylamidase and glucose oxidation positive; lactose and sucrose utilization negative42
    Burkholderia concitansBurkholderiaceaeLung tissue, bloodNot establishedNonmotile, oxidase-positive Gram-negative bacillus; less than 1-mm-diameter colonies cultivated on tryptic soy and MacConkey agars at 15–28°C; positive for Tween 60 hydrolysis, negative for Tween 80 hydrolysis; urease, esculin hydrolysis, β-galactosidase, and caprate assimilation negative; subsequent taxonomic revision described in Table 214e
    Burkholderia turbansBurkholderiaceaePleural fluidNot establishedNonmotile, oxidase-positive Gram-negative bacillus; less than 1-mm-diameter colonies cultivated on tryptic soy and MacConkey agars at 15–37°C; positive for Tween 60 hydrolysis, negative for Tween 80 hydrolysis; glucose and caprate assimilation positive; urease, esculin hydrolysis, and β-galactosidase negative; subsequent taxonomic revision is described in Table 214e
    Achromobacter deleyi sp. nov.AlcaligeneaceaeProstatic secretion, pharyngeal swabNot established; pharyngeal isolate from a U.S. cystic fibrosis patientMotile, oxidase-positive Gram-negative bacillus; nonpigmented 1.0- to 1.5-mm-diameter colonies cultivated on tryptic soy agar at 28°C; growth of selected strains on cetrimide agar in the presence of 3.0% and 4.5% NaCl; nitrite reduction and denitrification negative; caprate assimilation and alkaline phosphatase positive43
    Acinetobacter dijkshoorniae sp. nov.MoraxellaceaeClinical strains, including those from wound (n = 3), sputum (n = 2), blood, urine, catheter, and nephrology drain specimensNot establishedAerobic, nonmotile, oxidase-negative Gram-negative coccobacillus; 1- to 2-mm-diameter nonhemolytic colonies cultivated on tryptic soy agar at 30°C; gelatin hydrolysis and citraconate negative; produces acid from D-glucose; 53% of strains utilize tryptamine15
    Vibrio cidicii sp. nov.VibrionaceaeBlood (n = 3)Not establishedCurved, motile, oxidase-positive Gram-negative bacillus; sucrose-fermentative colonies cultivated on thiosulfate-citrate-bile salts-sucrose agar; growth observed in tryptic soy broth at 30°C with NaCl concentrations up to 8% for most isolates; utilizes L-rhamnose as the sole carbon source; most isolates do not utilize sodium citrate16
    Enterobacter hormaechei subsp. hormaechei subsp. nov.EnterobacteriaceaeSputum (n = 2), throat, blood, groin, and fecal samples, as described in reference 17Not establishedGram-negative bacillus exhibiting general characteristics of Enterobacter cloacae complex; dulcitol positive; adonitol, D-arabitol, D-sorbitol, and D-melibiose negative17f
    Enterobacter hormaechei subsp. oharae subsp. nov.EnterobacteriaceaeBlood (n = 2), trachea (n = 2), bronchoalveolar lavage fluid (n = 2), throat (n = 2), feces, ear, sputum, mouth, urine, and abscess specimens, as described previously (17)Not establishedGram-negative bacillus exhibiting general characteristics of the Enterobacter cloacae complex; AmpC hyperproduction in 25% of strains characterized in reference 17; D-sorbitol and D-melibiose positive; adonitol, D-arabitol, and dulcitol negative17f
    Enterobacter hormaechei subsp. steigerwaltii subsp. nov.EnterobacteriaceaeWound (n = 6), urine (n = 5), blood (n = 3), trachea (n = 2), bronchoalveolar lavage fluid, sputum, lung biopsy, throat, vaginal, and central line specimens, as described previously (17)Not establishedGram-negative bacillus exhibiting general characteristics of Enterobacter cloacae complex; AmpC hyperproduction in 42% of strains characterized in reference 17; positive adonitol, D-arabitol, D-sorbitol, and D-melibiose test results; negative dulcitol test result17f
    Citrobacter europaeus sp. nov.EnterobacteriaceaeFecesNot established; isolate from a U.S. patient with diarrheaGram-negative bacillus exhibiting general characteristics of Citrobacter spp.; growth observed from 20 to 50°C; H2S, inositol, and salicin positive; arginine dihydrolase, citrate, sucrose, and starch negative44
    Sphingobacterium cellulitidis sp. nov.SphingobacteriaceaeToePurulent discharge from a Kuwaiti cellulitis patient; nucleic acid homology demonstrated with previously unnamed Singapore environmental isolateAerobic, nonmotile, non-spore-forming, oxidase-positive Gram-negative bacillus; 0.5-mm-diameter pale yellow colonies cultivated on nutrient, tryptic soy, and MacConkey agars after 48 h of incubation at 28–37°C; catalase, Voges-Proskauer, tryptophan deaminase, and β-galactosidase positive; urease, decarboxylases, citrate, and nitrate negative45
    Haemophilus massiliensis sp. nov.PasteurellaceaePeritoneal fluidIsolate from a Senegalese female with pelvic peritonitis complicating a ruptured ovarian abscessFacultative, nonmotile, non-spore-forming, oxidase-positive Gram-negative bacillus; 0.5- to 1-mm-diameter nonhemolytic colonies on blood-enriched Columbia agar; optimal growth at 37°C; alkaline phosphatase, leucine arylamidase, and D-glucose utilization positive; indole and D-mannose utilization negative46b
    Weeksella massiliensis sp. nov.FlavobacteriaceaeUrineIsolate from a Senegalese male with acute cystitisAerobic, nonmotile, non-spore-forming, oxidase-positive Gram-negative bacillus; light yellow, 2-mm-diameter, smooth, nonhemolytic colonies on blood-enriched Columbia agar; alkaline phosphatase, leucine arylamidase, and D-xylose utilization positive; trypsin, indole, urease, β-galactosidase, and D-glucose utilization negative47b
    Ehrlichia muris subsp. eauclairensis subsp. nov.AnaplasmataceaeWhole bloodIsolate from a febrile Wisconsin (USA) patient with a history of tick exposure in 2009Morphologic and cultural similarities to E. muris subsp. muris subsp. nov. (Table 2); however, E. muris subsp. euclairensis subsp. nov. is localized to the United States; the sole vector is Ixodes scapularis, and it causes human disease48
    Kingella negevensis sp. nov.NeisseriaceaeOropharynx (n = 21)Not established; isolates from healthy Israeli and Swiss childrenNonmotile, non-spore-forming, oxidase-positive Gram-negative coccobacillus that exhibits capnophilic growth; pale yellow, beta-hemolytic 0.5- to 1-mm-diameter colonies on blood-enriched Columbia agar; optimal growth at 37°C; leucine arylamidase positive; urease, catalase, indole, ornithine decarboxylase, and proline arylamidase negative49
    Psychrobacter pasteurii sp. nov.MoraxellaceaeHuman origin (n = 2); not otherwise specifiedNot established; isolates submitted to a French collection bank in 1972Aerobic, nonmotile, non-spore-forming, oxidase-positive Gram-negative coccobacillus; optimal growth at 30°C; translucent, bright, 1- to 2-mm-diameter colonies observed on blood agar; catalase, urease, and lipase positive; reduces nitrate to nitrite; originally identified as a member of the Moraxella genus50
    Psychrobacter piechaudii sp. nov.MoraxellaceaeHuman origin (n = 4); not otherwise specifiedNot established; isolates submitted to a French collection bank in 1972Aerobic, nonmotile, non-spore-forming, oxidase-positive Gram-negative coccobacillus; optimal growth at 30°C; translucent, bright, 1- to 2-mm-diameter colonies observed on blood agar; catalase positive; urease and lipase activity is variable; unable to reduce nitrate to nitrite; originally identified as a member of the Moraxella genus50
    Burkholderia singularis sp. nov.BurkholderiaceaeRespiratory (n = 4)Not established; isolates from cystic fibrosis patients in Canada and GermanyAerobic, non-spore-forming Gram-negative bacillus; motility variable; growth on Columbia sheep blood agar (mucoid, nonhemolytic colonies), Burkholderia cepacia agar, yeast extract mannitol agar, and MacConkey agar at 42°C; slow oxidase activity; acidification of glucose, maltose, lactose, and xylose but not sucrose; nitrate reduction, lysine decarboxylase, and ornithine decarboxylase negative51g
    Shewanella carassii sp. nov.ShewanellaceaeFecesNot established; isolate from a Chinese infant with diarrheaFacultative, motile, oxidase-positive Gram-negative bacillus; growth on LB agar and blood agar (hemolytic), with optimal growth at 35°C; poor growth on MacConkey agar; colonies on LB agar are pink-orange with a 2- to 3-mm diameter; catalase, H2S, nitrate reduction, and L-proline arylamidase positive; urease and ornithine decarboxylase negative; does not grow in 10% NaCl52
Gram-positive anaerobes     
    Sellimonas intestinalis gen. nov., sp. nov.LachnospiraceaeFecesNot established; isolated from a fecal sample from a healthy Korean womanGram-positive diplococcus-shaped, obligate anaerobe, non-spore-forming; forms ivory yellow colonies; growth occurs at 25–45°C; the optimal growth temperature is 37°C; motile; H2S, indole, urease, and esculin hydrolysis negative; acid production from a variety of carbohydrates53
    Peptoniphilus catoniae sp. nov.PeptoniphilaceaeFecesNot established; isolated from a human fecal sample in southern PeruGram-positive, non-spore-forming coccus; obligate anaerobe; colonies on blood agar are needle point in size, beige, and circular with a smooth surface; optimal growth at 37°C; catalase, urease, indole, and nitrate negative54
    Propionibacterium namnetense sp. nov.PropionibacteriaceaeBoneInfected tibial fractureGram-positive, non-spore-forming, nonmotile, pleomorphic bacilli; anaerobic; after 6 days of incubation colonies are circular, dome shaped, and from pale cream to orange-salmon; optimal growth at 35°C55
    Agathobaculum butyriciproducens gen. nov., sp. nov.RuminococcaceaeFecesNot established; recovered from the feces of a healthy 23-year-old Korean womanGram-positive, non-spore-forming strict anaerobe; grows optimally at 37°C in the presence of 0.5% NaCl, pH 7; nonmotile; catalase and oxidase negative; butyrate producing56
    Butyricicoccus faecihominis sp. nov.ClostridiaceaeFecesNot established; recovered from the feces of a healthy human adultGram-positive coccoid-shaped organisms; nonmotile without spores; obligately anaerobic; colonies may appear waxy and yellowish after growth at 37°C for 72 h; indole positive57
    Faecalimonas umbilicata gen. nov., sp. nov.LachnospiraceaeFecesNot established; recovered from the feces of a healthy human adultGram-positive bacilli in pairs or chains; obligate anaerobe; nonmotile; nonpigmented; may form spores; colonies have a depressed center (umbilicate); H2S produced; indole, catalase, and urease negative58
    Merdimonas faecis gen. nov., sp. nov.LachnospiraceaeFecesNot established; recovered from the feces of a healthy human adultGram-positive strictly anaerobic; non-spore forming; catalase, indole, and oxidase negative; colonies are ivory colored and grow optimally at 37°C59
    Monoglobus pectinilyticus gen. nov., sp. nov.RuminococcaceaeFecesNot established; recovered from the feces of a 27-year-old healthy woman living in New ZealandGram-positive cocci that are strictly anaerobic; catalase positive; oxidase negative; indole negative; ferments pectin; optimum growth between 30 and 40°C60
Gram-negative anaerobes     
    Anaerospora hongkongensis gen. nov., sp. nov.VeillonellaceaeBloodNot established; isolates from an asymptomatic intravenous drug abuserObligate anaerobic, slightly curved, multiple-spore-forming, Gram-negative bacillus (up to 14 μm in length); yields pinpoint, catalase-negative, nonhemolytic colonies on blood agar following 48 h of incubation at 37°C; relatively inert biochemically18c
    Megasphaera massiliensis sp. nov.VeillonellaceaeFecesNot established; isolate from an HIV-positive patientObligate anaerobic, non-spore-forming, nonmotile Gram-negative coccobacillus; yields catalase-negative, 0.5- to 1.0-mm-diameter colonies on blood-enriched Columbia agar; optimal growth at 37°C; acid production from sorbitol and arabitol61c
    Sedimentibacter hongkongensis sp. nov.PeptostreptococcaceaehBloodIsolated from a patient with septic shock and multiorgan failure secondary to colon carcinomaObligate anaerobic, slightly curved, motile, terminal-spore-forming Gram-negative bacillus; yields pinpoint colonies on buffered charcoal yeast extract agar following 72 h of incubation at 37°C; growth on agar utilizing Bactec anaerobic blood culture broth under anaerobic conditions; no growth on brucella agar, brain heart infusion medium, or cooked meat medium; catalase and indole positive; nitrate reduction negative62c
    Dielma fastidiosa gen. nov., sp. nov.ErysipelotrichaceaeFecesNot establishedObligate anaerobic, motile, non-spore-forming Gram-negative bacillus; 0.5- to 1.0-mm-diameter colonies on blood-enriched Columbia agar; optimal growth at 30°C; esculin hydrolysis and acid arylamidase positive; mannose, sucrose, and D-glucose utilization negative63d
    Prevotella colorans sp. nov.PrevotellaceaeWoundIsolated in the context of a polymicrobial infectionObligate anaerobic, nonmotile, non-spore-forming, short and pleomorphic Gram-negative bacillus; after 2–5 days of incubation at 35–37°C, 1-mm-diameter colonies have weak greyish brown pigment; colonies develop toffee brown pigment after extended incubation; glucose, sucrose, and lactose fermentation positive; catalase (15% H2O2) and indole negative64
    Ruthenibacterium lactatiformans gen. nov., sp. nov.RuminococcaceaeFecesNot established; isolate from a healthy Russian maleObligate anaerobic, nonmotile, non-spore-forming Gram-negative bacillus; nonhemolytic, 0.15- to 0.40-mm-diameter colonies after 96 h of incubation on EG agar at 37°C; bile tolerant; growth can be stimulated by 5 mg hemin, 0.5% maltose, and 2–3% Oxgall; esculin and starch hydrolysis positive65
    Gabonibacter massiliensis gen. nov., sp. nov.PorphyromonadaceaeFecesNot established; isolate from a healthy Gabonese maleObligate anaerobic, motile Gram-negative coccobacillus; 2-mm-diameter white colonies after incubation on sheep blood-enriched Columbia agar at 37°C; indole, esterase, esterase lipase, and acid phosphatase positive; catalase, oxidase, alkaline phosphatase, and lipase negative66i
    Fournierella massiliensis gen. nov., sp. nov.RuminococcaceaeFecesNot established; isolate from a healthy French maleObligate anaerobic, nonmotile, non-spore-forming Gram-negative bacillus; optimal growth at 37°C; 1-mm-diameter colonies exhibit white pigment; catalase, oxidase, and indole negative; nitrate reductase, D-mannose, and maltose positive; the major short-chain fatty acid is acetic acid67
    Alistipes ihumii sp. nov.RikenellaceaeFecesIsolate from a French female with anorexia nervosa; clinical significance not establishedObligate anaerobic, non-spore-forming, nonmotile Gram-negative bacillus; optimal growth at 37°C; translucent 0.2-mm-diameter colonies on blood-enriched Columbia agar; leucyl glycine arylamidase, raffinose, and mannose positive; urease, indole, catalase, and nitrate reductase negative68b
    Bacteroides koreensis sp. nov.BacteroidaceaeFecesNot established; isolate from a healthy adultObligate anaerobic, nonmotile, non-spore-forming Gram-negative bacillus; optimal growth at 37°C; smooth, creamy, 1-mm-diameter colonies on reinforced clostridial medium; grows in the presence of bile; similar biochemical and fatty acid profile as Bacteroides kribbi sp. nov., with the exception of negative reactions for β-glucosidase and glutamic acid decarboxylase69
    Bacteroides kribbi sp. nov.BacteroidaceaeFecesNot established; isolate from a healthy adultObligate anaerobic, nonmotile, non-spore-forming Gram-negative bacillus; optimal growth at 37°C; smooth, creamy, 1-mm-diameter colonies on reinforced clostridial medium; grows in the presence of bile; similar biochemical and fatty acid profile as Bacteroides koreensis sp. nov., with the exception of positive reactions for β-glucosidase and glutamic acid decarboxylase69
Spirochetes     
    Haematospirillum jordaniae gen. nov., sp. nov.RhodospirillaceaeBlood (n = 14)Clinical diagnoses of septicemia (n = 3) and bacteremia (n = 1) provided in select instancesMotile, helical Gram-negative bacterium with dimensions of 1.6 μm by 0.1–0.25 μm; 1-mm-diameter colonies with slight alpha-hemolysis cultivated on heart infusion agar supplemented with 5% rabbit blood after 48 h of incubation at 35°C; catalase, oxidase, and hydrogen sulfide positive; urease, nitrate reduction, and indole negative70, 71e
    Borrelia mayonii sp. nov.SpirochaetaceaeBlood (n = 5), synovial fluidClinical significance is described in reference 72Motile spirochetes cultivated from blood specimens utilizing Barbour-Stoenner-Kelly medium in a 34°C microaerophilic environment; B. mayonii-specific nucleic acid detected by PCR from Ixodes scapularis ticks collected in Wisconsin and Minnesota (USA)73
a
Other members of the Paenibacillaceae have been reported to be Gram positive, Gram negative, or Gram variable.
b
Taxonomic designation subsequently added in validation list no. 176 (74).
c
Taxonomic designation subsequently added in validation list no. 168 (11).
d
Taxonomic designation subsequently added in validation list no. 170 (75).
e
Taxonomic designation subsequently added in validation list no. 171 (76).
f
Taxonomic designation subsequently added in validation list no. 172 (77).
g
Taxonomic designation subsequently added in validation list no. 178 (78).
h
Genera of Peptostreptococcaceae are typically Gram-positive organisms.
i
Taxonomic designation subsequently added in validation list no. 173 (79).
TABLE 2
TABLE 2 Revised bacterial taxa from January 2016 through December 2017
Former nameRevised nameOther informationReference(s)
Gram-positive cocci   
    Streptococcus oralis emended description The main characteristics are those provided in references 80 and 81, with the addition that some strains hydrolyze arginine82
    Streptococcus oralis subsp. oralis subsp. nov.Closely related species to S. oralis in the mitis group have been reclassified as subspecies of S. oralisS. oralis subsp. oralis was created; all strains produce IgA1 protease and extracellular polysaccharide; they do not hydrolyze arginine82
    Streptococcus dentisaniStreptococcus oralis subsp. dentisani comb. nov.The description is the same as that provided in reference 83, with the addition that it does not produce IgA1 protease or extracellular polysaccharide; most strains possess α-galactosidase; strains have been isolated from the dorsum of the tongue and human caries-free tooth surfaces82
    Streptococcus tigurinusStreptococcus oralis subsp. tigurinus comb. nov.The description is the same as that provided in reference 84, with the addition that most strains possess the enzyme α-galactosidase and all possess the gene for N-acetyl-β-glucosaminidase; strains have been isolated from human blood82
Gram-positive bacilli   
    Brevibacterium massilienseBrevibacterium ravenspurgense emendedThe previous taxonomic status of B. massiliense is described in reference 85; organism originally isolated from ankle discharge86
    Arthrobacter sanguinusHaematomicrobium sanguinus gen. nov., comb. nov.Original isolation from blood culture is described in reference 87; it has also caused peritonitis in a dialysis patient (88)89
Gram-negative bacilli   
    Achromobacter spiritinusAchromobacter marplatensisTaxonomy revision related to previous erroneous report of sequence data; the previous taxonomy of A. spiritinus is described in references 1, 90, and 91; clinical relevance in humans is not established92
    Acinetobacter genomic species 14BJAcinetobacter courvalinii sp. nov.Human strains include those isolated from skin and soft tissue (n = 3), blood (n = 1), urine (n = 1), conjunctiva (n = 1), and tracheal aspirate (n = 1) specimens; the previous designation is described in references 93 and 94; the clinical relevance of all isolates could not be ascertained19
    Acinetobacter genomic species 17Acinetobacter dispersus sp. nov.Human strains include those isolated from skin and soft tissue specimens (n = 3) and an unknown source (n = 1); the previous designation is described in reference 93; the clinical relevance of all isolates could not be ascertained19
    Acinetobacter taxon 18Acinetobacter modestus sp. nov.Human strains include those isolated from blood (n = 2), throat (n = 1), urine (n = 1), and skin and soft tissue (n = 1) specimens; the previous designation is described in references 94 to 96; the clinical relevance of all isolates could not be ascertained19
    Acinetobacter taxon 19Acinetobacter proteolyticus sp. nov.Human isolates from skin and soft tissue (n = 4), blood (n = 1), and ear (n = 1) specimens; the previous designation is described in reference 93; the clinical relevance of all isolates could not be ascertained19
    Acinetobacter taxon 20Acinetobacter vivianii sp. nov.Human strains include those isolated from blood (n = 2) and skin and soft tissue (n = 1) specimens and an unknown source (n = 1); the previous designation is described in references 93 and 94; the clinical relevance of all isolates could not be ascertained19
    Klebsiella albaKlebsiella quasipneumoniae subsp. similipneumoniaeK. alba was originally isolated from a polluted soil sample in China, with the taxonomy previously published (97) and added (98); the taxonomic status and clinical significance of K. quasipneumoniae subsp. similipneumoniae human isolates are discussed elsewhere (1, 99)100
    Capnocytophaga canimorsus (selected strains)Capnocytophaga canis sp. nov.Subset of less virulent C. canimorsus strains not isolated from human infections has been given a novel species designation; the C. canimorsus designation is reserved for species including human pathogens101a
    Paraburkholderia zhejiangensisCaballeronia zhejiangensis comb. nov.The initial designation of Burkholderia zhejiangensis was published in reference to a wastewater isolate (102) and augmented by three clinical isolates (blood, respiratory secretions) (103); the intermediate taxonomic status of P. zhejiangensis was previously published (104) and added (105)20
    Helicobacter cinaedi (selected strains)Helicobacter canicola sp. nov.Subset of H. cinaedi strains not isolated from human infections has been given a novel species designation106b
    Rhizobium pusenseAgrobacterium pusense comb. nov.The initial designation of R. pusense was published in reference to a rhizosphere isolate (107); the pathogenicity of R. pusense (and the previous reclassification of other Agrobacterium spp. as R. pusense) in human infections is described in reference 10821b
    Agrobacterium sp. genomovar G2Agrobacterium pusense comb. nov.Isolated from human blood21b,c
    Elizabethkingia endophyticaElizabethkingia anophelisClinical relevance not established in humans; the previous designation of E. endophytica is described in reference 109; E. endophytica is no longer considered a separate species of the genus Elizabethkingia110
    Rahnella genomospecies 2Rahnella variigena sp. nov.Taxonomic status previously discussed in reference 1111d
    Enterobacter aerogenesKlebsiella aerogenes comb. nov.Taxonomic status previously discussed in reference 112113
    Herbaspirillum massilienseNoviherbaspirillum massiliense comb. nov.Isolation from feces of a healthy Senegal patient, with the initial taxonomic status previously described in references 1, 114, and 115116, 117
[Pasteurella] pneumotropicaRodentibacter pneumotropicus comb. nov.Official 16S rRNA-based taxonomic designation granted for (misclassified) [P.] pneumotropica; human respiratory tract isolates are described in reference 118119
    Ehrlichia murisEhrlichia muris subsp. muris subsp. nov.Clinical significance in humans not definitively established; serologic evidence of human infection in Japan (120)48
    Acinetobacter genospecies 13Acinetobacter colistiniresistens sp. nov.Isolation previously described in reference 93121
    Acinetobacter DNA group 14Acinetobacter colistiniresistens sp. nov.Isolation previously described in reference 122121
    Burkholderia concitansCaballeronia concitans comb. nov.Isolation and proposed taxonomic status previously published (14) and added (76)123
    Burkholderia turbansCaballeronia turbans comb. nov.Isolation and proposed taxonomic status previously described (14) and added (76)123
    Enterobacter massiliensisMetakosakonia massiliensis comb. nov.Previous taxonomic status of E. massiliensis described in references 1 and 124125e
    Escherichia vulnerisPseudescherichia vulneris comb. nov.Previous taxonomic status of E. vulneris described in reference 126125e
Gram-positive anaerobes   
    Propionibacterium acnesCutibacterium acnes comb. nov.The description is the same as that provided in reference 127128, 129
    Propionibacterium avidumCutibacterium avidum comb. nov.The description is the same as that provided in reference 127 
    Propionibacterium granulosumCutibacterium granulosum comb. nov.The description is the same as that provided in reference 127 
    Propionibacterium propionicumPseudopropionibacterium propionicum comb. nov.The description is the same as that provided in reference 127; the species has been associated with abscesses at a variety of different sites (psoas, brain)128
    Clostridium difficileClostridioides difficile gen. nov., comb. nov.The description is identical to that for Clostridium difficile (130)131
    Clostridium mangenotiiClostridioides mangenotii comb. nov.The description of Clostridioides mangenotii is identical to that provided in reference 132 
    Eubacterium contortumFaecalicatena contorta gen. nov., comb. nov.A previous description of Eubacterium contorta can be found in reference 133; Faecalicatena spp. are obligately anaerobic Gram-positive bacilli found in chains or pairs; nonmotile; may or may not form spores; F. contorta grows optimally at 37°C58
a
Taxonomic designation subsequently added in validation list no. 170 (75).
b
Taxonomic designation subsequently added in validation list no. 172 (77).
c
X. Nesme, personal communication.
d
Taxonomic designation subsequently added in validation list no. 174 (134).
e
Taxonomic designation subsequently added in validation list no. 178 (78).
TABLE 3
TABLE 3 Update on clinical relevance for selected new taxonomy described previously in JCM in 2017
OrganismSource previously reported in JCM (1)Updated clinical relevanceReference
Streptococcus dentisaniCaries-free human tooth surfacesInfective endocarditis; refer to Table 2 for current taxonomic status135
Staphylococcus argenteusLymph node drainagePurulent lymphadenitis in a Japanese boy136
Gemella taiwanensisBloodInfective endocarditis in a woman with dental caries137
Nocardia kroppenstedtiiBrain abscess, bloodImmunocompromised patient who presented with central nervous system symptoms; the patient was found to have brain abscesses and endocarditis138
Achromobacter animicusSputumMultidrug-resistant organism implicated in wound infection in Tanzania139
Burkholderia pseudomultivoransSputumBacteremia (not otherwise specified)140
Klebsiella quasipneumoniae subsp. quasipneumoniaeType strain derived from bloodBiliary tract infection141
  Liver abscess142
  Urinary tract infection (n = 2)143
Klebsiella quasipneumoniae subsp. similipneumoniaeType strain derived from bloodExtended-spectrum β-lactamase-producing urine culture isolate144
  Sepsis (necrotizing fasciitis source)145
  Clinical isolates from Malaysia (not otherwise specified) harboring CTX-M, TEM, and NDM resistance determinants146
  Odontogenic infection147
  Nosocomial infection isolates from Brazil (not otherwise specified) harboring KPC-2 and OKP-B-6 resistance determinants148
Acinetobacter variabilisUrine, feces, ocular, blood, leg, peritoneal dialysis fluid, toeNeonatal sepsis in India149
  Sputum from cystic fibrosis patients in Brazil150
Acinetobacter seifertiiBlood, ulcer, respiratoryCatheter-related bloodstream infection151
  Sputum from cystic fibrosis patients in Brazil150
  Ten isolates characterized, including urine culture isolate from elderly female with dizziness152
  Catheter-related sepsis in pediatric patient; pressure ulcer; intra-abdominal abscess153
  Archived tracheal aspirate and nasal secretion isolates from 1993 and 1997 harboring OXA-58 resistance determinant154
Christensenella minutaFecesCoisolated with Desulfovibrio desulfuricans from blood of patient with acute appendicitis155
Eisenbergiella tayiBloodCanadian study of eight blood culture isolates and one appendix tissue culture isolate (also with positive blood culture)156
Klebsiella michiganensisToothbrush holderIsolate harboring KPC-2, NDM-1, and NDM-5 resistance determinants recovered from immunocompromised Chinese patient with acute diarrhea157
Actinotignum spp.BloodBacteremia among elderly patients158

Novel taxa.

Of the two novel genera that fall into the “Gram-positive cocci” group in Table 1, the most interesting is Streptococcus halichoeri subsp. hominis. Streptococcus halichoeri was originally isolated from gray seals (Halichoerus grypus) in 2004 in the United Kingdom (25). Subsequent to the description of this organism, isolates that were associated with infections in humans (four from blood and one from a sinus) and that were sent to the Centers for Disease Control and Prevention (CDC) were found to be phenotypically similar to S. halichoeri (26). In 2014, an additional isolate was recovered from a man with empyema in Singapore (27). None of these patients were believed to have an association with seals or ocean water; the average age of the patients was 63 years, and they were from different geographic locations (26). In a comprehensive investigation of the human isolates of S. halichoeri, the six isolates were characterized by Shewmaker et al. (26) using whole-genome and targeted gene sequencing and a variety of phenotypic methods. The six human isolates were genetically and phenotypically identical and most closely related to S. halichoeri. They can be distinguished from the type strain recovered from a seal as follows: positive for bile esculin and esculin hydrolysis, positive for acid production from sucrose, and positive for β-glucosidase, β-glucuronidase, and acid production from methyl-β-d-glucopyranoside (Rapid ID32 test system [bioMérieux, Inc., Durham, NC]) (26). On the basis of both phenotypic and genotypic differences from the seal type strain, the human isolates are believed to be a subspecies of S. halichoeri and are referred to as S. halichoeri subsp. hominis. Strains from marine animals are referred to as S. halichoeri subsp. halichoeri.
Two new Gram-positive aerobic bacilli associated with ocular infections have been added to the genus Corynebacterium. Corynebacterium lowii and Corynebacterium oculi were recovered primarily from patients in Japan at the time of ocular surgery and/or from patients with conjunctivitis (32). At the time of recovery from clinical material, they were described as high-level fluoroquinolone-resistant isolates distinguishable from Corynebacterium macginleyi (32). Additional characterization found them to be novel species.
Another noteworthy novel genus and species listed with the aerobic Gram-positive bacilli is Lawsonella clevelandensis gen nov., sp. nov. This is a very unusual organism, in that it grows best anaerobically, requiring prolonged incubation, yet it is modified acid-fast positive and beaded and branching on Gram stain and by sequencing is most closely related to members of the genus Dietzia (33, 34). In the original paper describing these infections, patients from Cleveland, Ohio, Winnipeg, Manitoba, Canada, and New York City had significant abscess collections of the spine (hardware associated), breast, and liver, respectively (34). Three of the patients were immunocompromised, and diabetes was a significant comorbid factor. Because of the fastidious nature of the organism growth, susceptibility testing could not be performed. Two of the patients responded to a combination of abscess drainage and amoxicillin-clavulanate; the other patients received regimens that included trimethoprim-sulfamethoxazole (34). Two additional cases of infection caused by L. clevelandensis have been reported. The first occurred in a patient with ulcerative colitis and a right lower quadrant intra-abdominal abscess (35). Because of the acid-fast nature of the organism, the patient was initially thought to have intra-abdominal tuberculosis. However, subsequent 16S rRNA gene sequencing performed on the abscess fluid identified the organism as L. clevelandensis, and the patient responded well to amoxicillin-clavulanate and drainage of the abscess (35). A very recent case report involved a 29-year-old woman who had a breast nodule that yielded a Gram-positive filamentous organism identified by molecular methods as L. clevelandensis (159).
With respect to Gram-negative organisms, three valid subspecies of Enterobacter hormaechei (namely, Enterobacter hormaechei subsp. hormaechei subsp. nov., Enterobacter hormaechei subsp. oharae subsp. nov., and Enterobacter hormaechei subsp. steigerwaltii subsp. nov.) have been officially added by IJSEM (17, 77), though clinical data were not provided to ascribe true clinical relevance. A novel Enterobacter spp., Enterobacter bugandensis sp. nov. (39), was isolated from 17 neonates in a Tanzanian sepsis outbreak. These isolates tested resistant to fluoroquinolones, aminoglycosides, and tetracycline and harbored the CTX-M-15 resistance determinant. A pair of facultative Gram-negative bacilli, Citrobacter europaeus sp. nov. (44) and Shewanella carassii sp. nov. (52), have been isolated from individuals with diarrhea.
The nonmotile coccobacillus Alkanindiges hongkongensis sp. nov. was isolated from a Chinese patient with an infected Warthin’s tumor that resulted in a parotid gland abscess and peripheral leukocytosis (11, 40). The patient responded well to surgical drainage of the abscess and a course of amoxicillin-clavulanate. Organism growth was significantly enhanced by Tween 80 supplementation. The oxidase-positive, Gram-negative bacillus Sphingobacterium cellulitidis sp. nov. (45) was isolated from a patient with cellulitis in Kuwait. The erythematous and purulent infection resolved following a 1-week amoxicillin-clavulanate regimen. During genetic characterization of the clinical isolate, homology with a previously unnamed activated sludge isolate derived from Singapore was demonstrated.
A novel member of the Anaplasmataceae, Ehrlichia muris subsp. eauclairensis subsp. nov. (48), was isolated from an upper midwestern United States febrile patient with previous Ixodes scapularis tick exposure. This subspecies is now delineated from Ehrlichia muris subsp. muris subsp. nov. (Table 2), in that the latter has been recovered from multiple genera of ticks, involves multiple natural reservoir hosts, and has distribution in Eastern Europe and Japan. Furthermore, human clinical disease with an E. muris subsp. muris subsp. nov. etiology has not been definitively established, though serologic evidence of a human immune response has been reported from Japan (120).
Only one of the new species listed under the Gram-positive anaerobes category in Table 1 was recovered from a clinical infection. Propionibacterium namnetense sp. nov. was isolated from a patient who had an infected tibial fracture (55). The remaining novel genera and species were recovered from the feces of otherwise healthy humans in many cases during the study of intestinal microbiomes. Similarly, many of the novel anaerobic Gram-negative agents have not had clinical significance established, though Megasphaera massiliensis sp. nov. (11, 61) was isolated from an HIV-positive patient and Sedimentibacter hongkongensis sp. nov. (11, 62) was recovered from a patient with septic shock and multiorgan failure.
With respect to spirochetes, the valid name of Haematospirillum jordaniae gen. nov., sp. nov. (70, 71), was added by IJSEM in 2016 (76). The type strain was derived from human blood and referred to CDC in 2010. During a brief interval in 2012, 3 isolates with identical 16S rRNA sequences matching those of both the type strain and 10 previously characterized (but unnamed) isolates were forwarded to CDC. All isolates were derived from men (mean age, 60 years), and the clinical diagnoses ranged from septicemia to tularemia. Limited clinical data were available (70), though two patients reported headache, fever, chills, diarrhea, and swelling in the lower extremities.
Routine Borrelia burgdorferi sensu lato oppA1 PCR testing performed at an upper midwestern United States reference laboratory revealed six clinical specimens (five blood specimens and one synovial fluid specimen from six patients) with atypical melting curve profiles (72). Subsequent sequencing of amplified 16S rRNA, in part, resulted in the characterization of the novel taxon Borrelia mayonii sp. nov. (73). Field surveys in Wisconsin and Minnesota recovered I. scapularis ticks from which B. mayonii sp. nov. DNA was detected by PCR. This form of spirochetal disease differed from typical Lyme borreliosis paradigms in several facets (72). In the limited data set, the novel agent was detected more frequently from blood specimens than from synovial fluid specimens. To an extent, these data were corroborated by higher median oppA1 copy numbers and profound spirochetemia (as observed by microscopy) compared to those in infections caused by B. burgdorferi sensu stricto. Finally, clinical presentations included findings of diffuse macular rash not consistent with erythema migrans, nausea and vomiting, and high-grade fever. Several symptoms more closely resembled those associated with relapsing fever borrelial disease (160).

Taxonomic revisions.

In the previous taxonomic update in this journal published in 2017, a novel Streptococcus species, Streptococcus tigurinus, was highlighted (1). Zbinden et al. (84) described this organism as causing serious and invasive infections, including bacteremia and endocarditis. In 2016, this organism was reclassified as a subspecies of Streptococcus oralis (Table 2) (82). Streptococcus oralis now has three subspecies: S. oralis subsp. oralis, S. oralis subsp. dentisani, and S. oralis subsp. tigurinus (82). S. oralis subsp. dentisani comb. nov. has been reported as a cause of infective endocarditis (Table 3) (135).
In 1971, Bascomb et al. (161) characterized a subset of Enterobacter aerogenes strains that more closely resembled Klebsiella spp. from a phenotypic perspective. At that time, taxonomic transfer to Klebsiella aerogenes was not possible and the taxon Klebsiella mobilis was utilized for naming this species. It was subsequently determined by taxonomists (113) that this nomenclature convention was illegitimate. Moreover, by way of adherence to contemporary nomenclature code (162), it was determined that the name Klebsiella aerogenes was available for use. Thus, E. aerogenes has now been transferred to Klebsiella aerogenes comb. nov. (Table 2) (113) and K. mobilis is a homotypic synonym of Klebsiella aerogenes comb. nov. The clinical utility of this taxonomic revision remains to be seen, particularly with respect to salient differences in the predicted antimicrobial susceptibility profiles of the Klebsiella and Enterobacter genera in general (particularly relevant to cephamycins, first-generation cephems, and β-lactam–β-lactamase inhibitor combinations, such as ampicillin-sulbactam [163]) and the confusion that this may present to clinicians.
In a publication not included in Table 2, Adeolu et al. (164) used comparative genomic analyses based on greater than 1,500 core proteins, 53 ribosomal proteins, and 4 multilocus sequence analysis proteins to reorganize families and genera within what is now known as Enterobacteriales ord. nov. Essentially, six new families have been created from the family Enterobacteriaceae. These new families and the inclusive genera are Erwiniaceae fam. nov. (containing the genera Erwinia, Buchnera, Pantoea, Phaseolibacter, Tatumella, and Wigglesworthia), Pectobacteriaceae fam. nov. (containing the genera Pectobacterium, Brenneria, Dickeya, Lonsdalea, and Sodalis), Yersiniaceae fam. nov. (containing the genera Yersinia, Chania, Ewingella, Rahnella, Rouxiella, Samsonia, and Serratia), Hafniaceae fam. nov. (containing the genera Hafnia, Edwardsiella, and Obesumbacterium), Morganellaceae fam. nov. (containing the genera Morganella, Arsenophonus, Cosenzaea, Moellerella, Photorhabdus, Proteus, Providencia, and Xenorhabdus), and Budviciaceae fam. nov. (containing the genera Budvicia, Leminorella, and Pragia). The remaining Enterobacteriales genera remain in an emended description of the family Enterobacteriaceae (164).
Perhaps the most clinically impactful changes have been among the genera Clostridium and Propionibacterium. The group of propionibacteria associated with the skin biome of human hosts constitutes a distinct clade in the genus Propionibacterium. Whole-genome sequencing and more sophisticated phylogenetic analyses support placing the species associated with human skin into a new genus, Cutibacterium. The novel Cutibacterium genus includes the species Cutibacterium acnes, C. avidum, and C. granulosum previously assigned to the Propionibacterium genus (Table 2) (128). The novel genus Pseudopropionibacterium now contains the species formerly called Propionibacterium propionicum (Table 2) (128). Several of the propionibacteria associated with dairy sources, such as matured cheeses, have been placed into the genus Acidipropionibacterium gen. nov. (refer to reference 128 for more details about dairy strains). As also inferred with the Klebsiella aerogenes (Enterobacter aerogenes) paradigm, the clinical microbiologist may wish to consult with clinical practitioner colleagues regarding the optimal manner to report the identification of organisms affected by taxonomic revisions. With respect to the former Propionibacterium acnes, possibilities may include “Cutibacterium acnes (formerly Propionibacterium acnes)” or “Cutibacterium acnes (formerly P. acnes).”
The genus Clostridium is also undergoing substantial changes. Application of molecular methods, including complete sequencing of the 16S rRNA gene and other methods, emphasizes the phylogenetic diversity of this group of organisms and has led to the decision to reserve the genus designation of Clostridium sensu stricto to rRNA cluster I, which includes the type species Clostridium butyricum (131, 165). Consequently, the majority of Clostridium species which are not consistent with the genus Clostridium description, as emended by Lawson and Rainey (165), will be assigned to other genera. Clostridium difficile is phylogenetically distant from cluster I and is located in cluster XI (131). Phylogenetic studies have shown that the type strain of C. difficile belongs in the family Peptostreptococcaceae. In 2013, Yutin and Galperin (166) proposed creating a new genus, Peptoclostridium, to accommodate the Clostridium species reassigned to the family Peptostreptococcaceae. This proposal, which would have placed many diverse species into a single genus (including C. difficile), was rejected as being too simplistic (167). Subsequently, with the recognition that the proposed name Peptoclostridium difficile would change the monikers of C. difficile or C diff already ingrained in commercial products, packaging, computer systems, and clinical laboratories and to avoid tremendous confusion among clinicians, Lawson and colleagues (131) proposed a compromise with the new designation of Clostridioides difficile, thereby retaining the abbreviation commonly used for C. difficile. It is hoped that this designation will mitigate the time and cost associated with the required reclassification, as oftentimes only the abbreviation is used. The only other species in this new genus is Clostridioides mangenotii. Changes to other genera not highlighted here have been made or are forthcoming. Many of these new genera contain species not associated with human infections. In the 2017 minireview, we highlighted the reassignment of Clostridium hathewayi into the new genus Hungatella as Hungatella hathewayi gen. nov., comb. nov., in 2014 (1). A resident of the human intestinal tract, this organism has been associated with surgical site infections and bacteremia (reviewed in reference 168). Like other clostridia, it may stain Gram negative.
One major paradigm of bacterial taxonomy revision was, unfortunately, overlooked in our first compendium. Adeolu and Gupta (169) proposed a reclassification of Borrelia sp. spirochetes in 2014. Agents responsible for Lyme disease (formerly residing in the Borrelia burgdorferi sensu lato complex) were transferred to Borreliella gen. nov., while spirochetal agents largely responsible for relapsing fever retained the Borrelia genus designation (type species, Borrelia anserina). Per Adeolu and Gupta (169), specific agents within Borreliella gen. nov. include Borreliella burgdorferi comb. nov. (the type species of Borreliella), B. afzelii comb. nov., B. americana comb. nov., B. bavariensis comb. nov., B. carolinensis comb. nov., B. garinii comb. nov., B. japonica comb. nov., B. kurtenbachii comb. nov., B. lusitaniae comb. nov., B. sinica comb. nov., B. spielmanii comb. nov., B. tanukii comb. nov., B. turdi comb. nov., and B. valaisiana comb. nov. Valid names of B. bavariensis, B. burgdorferi, B. carolinensis, B. garinii, B. japonica, B. kurtenbachii, B. sinica, and B. spielmanii have been added by IJSEM (170), yet this topic remains the subject of controversy and discussion (171, 172). To our knowledge, the nomenclature of the novel taxon Borrelia mayonii sp. nov. (Table 1) has not been revised.

Recently ascribed clinical significance.

New literature on novel Gram-positive taxa highlighted in the original series (1) is summarized here and in Table 3. A case of purulent lymphadenitis attributed to Staphylococcus argenteus was reported in a Japanese child (136). The authors highlight the observations that this organism is often misidentified as nonpigmented S. aureus. Up to this time, most human cases have been found in northeastern Thailand (136). The first case report of infective endocarditis caused by Gemella taiwanensis was published by Hikone et al. (137). In contrast to the cases mentioned in the initial description of this organism (173), this patient was not immunocompromised, and it is believed that her native valve endocarditis occurred after extensive treatment for dental caries (137). The first reported case of disseminated Nocardia kroppenstedtii was reported by Majeed et al. (138). This patient was an immunocompromised gentleman (mantle cell lymphoma) who presented with new central nervous system symptoms. He was found to have brain abscesses as well as a mitral valve mass. Blood cultures and a brain biopsy specimen were positive for N. kroppenstedtii (138). Finally, with respect to the Gram-positive anaerobes, much new literature on Actinotignum schaalii can be found via PubMed primary literature searches, and the interested reader is directed there for those papers. A comprehensive review highlighting the clinical and microbiological features of Actinotignum spp. is referenced (158), with the authors noting that Actinotignum bacteremia affects elderly persons with comorbidities and is associated with high mortality.
Particular clinical significance can be ascribed to several taxa listed in Table 3 on the basis of multidrug resistance (139, 144, 146, 148, 149, 154, 157). One of these genus/species designations, Klebsiella quasipneumoniae, is frequently misidentified by the clinical microbiology laboratory as Klebsiella pneumoniae (174), yet it has the potential to harbor similar resistance determinants and virulence factors as K. pneumoniae. Elliott et al. (175) published the whole-genome sequence of the commonly utilized quality control strain ATCC 700603, identifying it as K. quasipneumoniae subsp. similipneumoniae. K. quasipneumoniae subsp. quasipneumoniae has been recovered in clinical specimens from patients with biliary tract infection (141), liver abscess (142), and urinary tract infection (143), while K. quasipneumoniae subsp. similipneumoniae has been implicated in urinary tract infection (144), sepsis (with antecedent necrotizing fasciitis) (145), odontogenic infection (147), and nosocomial infection (148). In addition to recent reports of Acinetobacter variabilis isolation in the context of neonatal sepsis (149) and cystic fibrosis (150), organism-specific nucleic acid has been isolated from Pediculus humanus capitis organisms collected from schoolchildren and homeless individuals in northern Africa (176, 177). The authors raise the possibility of human body lice potentially serving as vectors/reservoirs of a range of pathogens broader than previously appreciated.

Other novel agents of interest.

One taxon briefly described in the first bacterial taxonomy compendium (1) was Klebsiella michiganensis, an isolate of which was originally recovered from a toothbrush holder. In 2018, Zheng et al. (157) reported a case of acute diarrhea from a patient after hematopoietic stem cell transplantation in which a K. michiganensis isolate harboring the resistance determinants KPC-2, NDM-1, and NDM-5 was recovered from a stool culture (Table 3). While not included within the formal tables of this minireview, the following paragraphs describe examples of new taxa that possess the potential to progress into the realm of human clinical disease.
Although they have yet to be associated with human clinical specimens, several new taxa have been cultivated from known disease vector agents. These include the rickettsial agents Rickettsia asembonensis sp. nov., Rickettsia amblyommatis sp. nov., Rickettsia gravesii sp. nov., and Occidentia massiliensis gen. nov., sp. nov., recovered from fleas (178) or ticks (179181); Borrelia bissettiae sp. nov., Borrelia californiensis sp. nov., and Borrelia lanei sp. nov. from Ixodes pacificus ticks (182, 183); three novel Anaplasmataceae from ticks (184, 185); and the Gram-negative bacillus Coetzeea brasiliensis gen. nov., sp. nov., from mosquito larvae (186). The valid O. massiliensis gen. nov., sp. nov., designation was subsequently added by IJSEM (74).
Other agents have been associated with ingestible or inhalable material. Serratia aquatilis sp. nov. and Ampullimonas aquatilis gen. nov., sp. nov., have recently been isolated from drinking (187) and bottled mineral (188) water, respectively. Agents recovered from raw cow’s milk include Pseudomonas helleri sp. nov., Pseudomonas weihenstephanensis sp. nov. (189), Pseudomonas lactis sp. nov., and Pseudomonas paralactis sp. nov. (190). Rooney et al. (191) reported the isolation of Acinetobacter lactucae sp. nov. from iceberg lettuce. Examples of novel agents recovered from seafood include Halomonas garicola sp. nov. (192), Proteus cibarius sp. nov. (193), and Thalassotalea crassostreae sp. nov. (194). Finally, several nonfermentative Gram-negative bacilli have been isolated from air-conditioning systems (195199).
In summary, studies of the human microbiome and advancements in molecular characterization modalities have largely been responsible for the identification of novel bacterial agents from human sources. Newer and improved tools have also contributed to the assessment of closely related pathogens and, in many instances, have resulted in revisions to previously accepted taxonomy. We have attempted to summarize these changes for 2016 and 2017 (as relevant to humans) and to provide insight into the clinical relevance of these agents. Additional changes to the Clostridiales are anticipated in the next few years. As a result, this project will be sustainable into the near future, while retrospectively attempting to ascertain the clinical significance of agents that are currently believed to have uncertain or commensal status.

ACKNOWLEDGMENT

This report was not subject to influence from any funding agency in the public, commercial, or not-for-profit sectors.

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Information & Contributors

Information

Published In

cover image Journal of Clinical Microbiology
Journal of Clinical Microbiology
Volume 57Number 2February 2019
eLocator: 10.1128/jcm.01181-18
Editor: Colleen Suzanne Kraft, Emory University

History

Published online: 30 January 2019

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Keywords

  1. bacteria
  2. nomenclature
  3. phylogenetics
  4. taxonomy

Contributors

Authors

Erik Munson
College of Health Sciences, Marquette University, Milwaukee, Wisconsin, USA
Karen C. Carroll
Division of Medical Microbiology, Department of Pathology, The Johns Hopkins University School of Medicine, Baltimore, Maryland, USA

Editor

Colleen Suzanne Kraft
Editor
Emory University

Notes

Address correspondence to Karen C. Carroll, [email protected].

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