ABSTRACT
Technological advancements in fields such as molecular genetics and the human microbiome have resulted in an unprecedented recognition of new bacterial genus/species designations by the International Journal of Systematic and Evolutionary Microbiology. Knowledge of designations involving clinically significant bacterial species would benefit clinical microbiologists in the context of emerging pathogens, performance of accurate organism identification, and antimicrobial susceptibility testing. In anticipation of subsequent taxonomic changes being compiled by the Journal of Clinical Microbiology on a biannual basis, this compendium summarizes novel species and taxonomic revisions specific to bacteria derived from human clinical specimens from the calendar years 2012 through 2015.
KEYWORDS: anaerobes, bacteria, Gram-negative bacteria, Gram-positive bacteria, taxonomy
INTRODUCTION
Human microbiome studies, particularly those involving genome sequencing, have resulted in a seeming explosion of novel bacterial taxonomy. While many of these organisms appear to play a commensal role in site-specific ecology, some of the organisms may be of clinical significance in various patient populations. Moreover, enhanced studies of known bacterial genomes in a variety of applications, including those of an epidemiologic nature, have given rise to revisions and amendments to accepted bacterial taxonomy. Summaries of microbial taxonomy updates, such as those introduced in this edition of the Journal of Clinical Microbiology, are essential to routine practice in the clinical microbiology laboratory.
Since 2014, laboratories subscribing to the College of American Pathologists accreditation program have encountered checklist standard MIC.11375 in the context of biennial inspection exercises. The standard (1) requires laboratories to assimilate “taxonomic changes that potentially affect the choice of appropriate antimicrobials to report and/or the interpretative breakpoints to use.” Cited as an example for the context of this standard is the Gram-negative bacillus with the former taxonomic designation Actinobacillus actinomycetemcomitans. The taxonomic revision in 1985 (2) resulting in organism classification within the genus Haemophilus subsequently enabled antimicrobial susceptibility testing of clinically significant isolates using standards outlined in Table 2E of CLSI supplement M100S (example provided in [3]). Haemophilus test medium, with a 16- to 18-hour incubation in 5% CO2 enrichment, could be utilized for disk diffusion. Haemophilus test medium broth could also be inoculated for broth microdilution testing with 20- to 24-hour incubation in ambient air.
TABLE 2.
Revised bacterial taxa between January 2012 and December 2015
| Old name | Revised name | Other information | References |
|---|---|---|---|
| Aerobic Gram-positive rod | |||
| Bacillus massiliensis | Lysinibacillus massiliensis comb. nov. | Isolated from human cerebrospinal fluid | 153, 154 |
| Anaerobic Gram-positive cocci | |||
| Ruminococcus obeum | Blautium obeum comb. nov. | Isolated from human feces | 155 |
| Anaerobic Gram-negative rods | |||
| Prevotella tannerae | Alloprevotella tannerae gen. nov. | Endodontic infections | 138 |
| Bifidobacterium stercoris | Bifidobacterium adolescentis | Isolated from human feces | 156 |
| Anaerobic Gram-positive rods | |||
| Eubacterium saburreum | Lachnoanaerobaculum saburreum comb. nov. | Isolated from dental plaque | 125 |
| Clostridium hathewayi | Hungatella hathewayi gen. nov., comb. nov. | Isolated from human feces | 157 |
| Actinobaculum urinale | Actinotignum urinale comb. nov. | Urinary tract infections | 132 |
| Actinobactulum schaalii | Actinotignum schaalii gen. nov., comb. nov. | Urinary tract infections | 132 |
| Gram-negative cocci | |||
| Neisseria mucosa var. heidelbergensis | Neisseria oralis | Neisseria oralis sp. nov. referenced in Table 1 of this minireview | 33, 158 |
| Aerobic and facultative Gram-negative rods | |||
| “Candidatus Helicobacter heilmannii” | Helicobacter heilmannii sp. nov. | Newly recognized due to in vitro cultivation of the organism, significance in humans described in reference 47 | 46, 47 |
| Cronobacter genomospecies 1 | Cronobacter universalis sp. nov. | Pathogenicity of strain 731 previously demonstrated in leg infection | 159 |
| Pasteurella species B | Pasteurella oralis sp. nov. | Type strain isolated in 1981 from cat bite wound of human | 160 |
| Selected CDC group II-i isolates | Sphingobacterium mizutaii | Two isolates recovered from blood culture (one from patient with septicemia) | 161 |
| Yersinia frederiksenii genospecies 2 | Yersinia massiliensis | Phylogenetic analysis grouped 15 strains of Y. frederiksenii genospecies 2/Y. massiliensis apart from Y. frederiksenii genospecies 1 and 3 | 162 |
| 142 group | Chryseobacterium bernardetii sp. nov. | Isolated from tongue swab, sputum, blood, finger abscess | 163 |
| 78 group | Chryseobacterium nakagawai sp. nov. | Isolated from kidney abscess, urine | 163 |
| 212 group (contribution of CDC groups IIc and IIe) | Chryseobacterium taklimakanense comb. nov. | Isolated from blood, wound, cerebrospinal fluid | 163 |
| Aeromonas hydrophila subsp. dhakensis | Aeromonas dhakensis sp. nov. comb nov. | Pathogenicity in humans described in references 50, 53 | 48a, 50, 53 |
| Aeromonas aquariorum | Aeromonas dhakensis sp. nov. comb nov. | Pathogenicity in humans described in references 51, 52 | 48a, 51, 52 |
| Aeromonas hydrophila subsp. anaerogenes | Aeromonas caviae | Original taxonomy discussed in reference 164 | 79b, 164 |
| Enterobacter gergoviae | Pluralibacter gergoviae comb. nov. | E. gergoviae sp. nov. pathogenicity first characterized in reference 165 | 63c, 165 |
| Enterobacter amnigenus | Lelliottia amnigena comb. nov. | One recent example of E. amnigenus pathogenicity was bloodstream isolate harboring both blaKPC and rmtB on single plasmid, as published in reference 166 | 63c, 166 |
| Achromobacter genogroup 2 | Achromobacter insuavis | Isolated from cystic fibrosis, non-cystic fibrosis patient sputum | 167d |
| Achromobacter genogroup 5 | Achromobacter aegrifaciens | Isolated from cystic fibrosis, non-cystic fibrosis patient sputum | 167d |
| Achromobacter genogroup 7 | Achromobacter anxifer | Isolated from cystic fibrosis patient sputum | 167d |
| Achromobacter genogroup 14 | Achromobacter dolens | Isolated from cystic fibrosis, non-cystic fibrosis patient sputum | 167d |
| Wautersiella falsenii | Empedobacter falsenii comb. nov. | Pathogenicity in humans described in references 56, 57 | 54–57 |
| Rahnella genomospecies 2 | Rahnella variigena sp. nov. | Type strain isolated from human burn specimen | 80e |
Taxonomic designation subsequently accepted in validation list no. 161 (49).
Taxonomic designation not recognized on validation list in International Journal of Systematic and Evolutionary Microbiology; offered as component of changes in taxonomic opinion no. 19 (77).
Taxonomic designation subsequently accepted in validation list no. 154 (64).
Taxonomic designation subsequently accepted in validation list no. 155 (149).
Taxonomic designation not recognized on validation list in International Journal of Systematic and Evolutionary Microbiology; offered as component of changes in taxonomic opinion no. 22 (78).
Subsequent reclassification of this organism into the genus Aggregatibacter (4) has resulted in the transition of susceptibility testing guidelines to those specific to (former) HACEK group organisms (Aggregatibacter spp., Cardiobacterium spp., Eikenella corrodens, and Kingella spp.) in Table 9 of the CLSI guideline M45 (5).
The shift of the former A. actinomycetemcomitans from Table 2E of the CLSI M100S supplement (3) to the M45 guideline (5) also impacted tested and reported anti-infective agents. While MIC interpretive criteria remained largely unchanged for trimethoprim-sulfamethoxazole, rifampin, tetracycline, ampicillin, macrolide agents, and β-lactam/β-lactamase inhibitor combinations between the two documents, the number of reportable fluoroquinolone agents via broth microdilution and disk diffusion testing in a past M100S supplement (3) was reduced from nine to two in the current M45 guideline (5). These two agents, levofloxacin and ciprofloxacin, are only assessed by broth microdilution and now possess intermediate and resistant interpretive criteria. Similarly, the number of reportable cephem agents (fifteen) in a previous M100S supplement was reduced to two for Aggregatibacter spp. in the context of the M45 guideline; intermediate and resistant interpretive criteria now exist. Penicillin susceptibility testing is newly available per the CLSI M45 guideline, along with Aggregatibacter genus-specific MIC interpretive criteria for carbapenem susceptibility testing. In an analogous fashion, clinically significant organisms in generic CLSI classifications, such as “other non-Enterobacteriaceae” or “Streptococcus spp. viridans group,” could hypothetically be moved into categories that have alternative susceptibility testing guidelines or that do not allow for any testing.
The accurate identification of organisms is important for understanding the epidemiology of emerging pathogens. One contemporary example of this paradigm resides within the newly described taxon Elizabethkingia anophelis. This oxidase-positive Gram-negative bacillus was first isolated from the midgut of an Anopheles gambiae mosquito originating from McCarthy Island, The Gambia (6). Full-gene 16S rRNA sequence similarities of 98.6% and 98.2% were reported to strains Elizabethkingia meningoseptica ATCC 13253T and Elizabethkingia miricola GTC 862T, respectively. An initial attribution of clinical significance (7) involved a case of neonatal meningitis in Bangui, Central African Republic. Although it was identified as E. meningoseptica by biochemical analysis, full 16S rRNA gene sequencing of this isolate resulted in a definitive identification as E. anophelis. On the basis of geographic location and discovery origin, it was originally hypothesized that mosquito vectors were central to E. anophelis disease epidemiology.
However, Balm et al. (8) chronicled an E. meningoseptica outbreak in cardiothoracic and surgical intensive care units of a tertiary Singapore hospital. The organism was isolated from blood and respiratory specimens and identified by matrix-assisted laser desorption ionization–time of flight mass spectrometry (MALDI-TOF MS). Initial epidemiologic relatedness between the clinical isolates and E. meningoseptica isolates derived from sampling of water taps/aerators was established by repetitive element palindromic PCR. Subsequent 16S rRNA sequencing and whole-genome alignment identified the outbreak strains as being E. anophelis. Additional genetic determinants were consistent with the clinical course (antimicrobial treatment failure and mortality) in a number of patients.
Moreover, Lau et al. (9) reported three cases of E. anophelis sepsis from one Hong Kong inpatient facility. Neonatal meningitis was additionally diagnosed in two cases, and the third involved a maternal chorioamnionitis related to one neonatal case. The isolates were originally identified as E. meningoseptica by both a commercial biochemical system and MALDI-TOF MS (scores ≥1.8). Full-gene 16S rRNA sequencing revealed 99.1% to 99.9% identity to E. anophelis R26T and 97.4% to 99.9% identity to GenBank E. meningoseptica deposits. Draft genome sequencing not only identified the isolates as E. anophelis, but also implicated perinatal vertical transmission in two cases.
Lau and colleagues (10) expanded clinical and epidemiologic analyses of Elizabethkingia spp. bacteremia to five regional Hong Kong hospitals in the context of additional non-glucose-fermenting Gram-negative bacilli (including Chryseobacterium and Flavobacterium spp.). Bacteremia caused by Elizabethkingia spp. was associated with clinically significant infection (P = 0.00009), positive cultures from additional sources (P = 0.005), higher complication rates (P = 0.01), and increased attributable mortality rates (P = 0.025) compared to those of bacteremia caused by non-Elizabethkingia spp. Moreover, 81% of Elizabethkingia spp. bacteremic episodes were related to E. anophelis, as confirmed by full-gene 16S rRNA sequencing. The mortality rate in these patients was 23.5% (4/17), while none of the three E. meningoseptica bacteremia cases was fatal. Patients with E. anophelis bacteremia carried additional clinical diagnoses of community-acquired or nosocomial pneumonia (29.4% of cases), catheter-related bacteremia (23.5%), and neonatal meningitis (17.6%).
Analogous to the original Hong Kong report (9), all E. anophelis isolates were originally identified as E. meningoseptica by a commercial biochemical system; nearly 60% were identified as E. meningoseptica by MALDI-TOF MS. Database revision by the addition of seven E. anophelis spectra facilitated the identification of all E. anophelis isolates. An increased resistance to piperacillin and co-trimoxazole was observed within the E. anophelis collection compared to that of the limited subset of E. meningoseptica isolates (10). In summary, the recognition of current bacterial taxonomy can assist in future epidemiologic and prognostic delineations of Elizabethkingia spp. infections and additional emerging infectious agents.
Attempts to summarize and centralize taxonomic changes into a single resource were previously undertaken (11, 12), and there have been recent attempts to renew this practice (13, 14). The following compendium of clinically significant bacterial taxonomy changes from the calendar years 2012 to 2015 attempts to provide a comprehensive capstone for the biannual updating of bacterial taxonomy by editors of the Journal of Clinical Microbiology.
METHODS AND DATA
Validly published novel (Table 1) and revised (Table 2) taxa pertinent to prokaryotic species must meet one of two requirements: (i) an original investigation published in the International Journal of Systematic and Evolutionary Microbiology (IJSEM) or (ii) a study published in an alternative journal, with later inclusion on an approved list in IJSEM. Journals that publish studies reporting new taxa that may be relevant to the practice of clinical microbiology include Antonie Van Leeuwenhoek, Current Microbiology, International Journal of Medical 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” (example provided in [69]). To be considered for inclusion on this approved list, authors must submit a copy of the published manuscript to the editorial office of IJSEM for confirmation that all the elements necessary for valid publication have been met. In addition, type strains are to be deposited into two recognized culture collections in separate nations. Taxa on these approved lists may be subject to reclassification on the basis of a synonym designation or transfer to another genus. Accepted taxa within Tables 1 and 2 that were previously published outside IJSEM are represented by appropriate footnoting.
TABLE 1.
New bacterial species recovered from human clinical material reported between January 2012 and December 2015
| Scientific name | Family | Source (no. of cases) | Clinical relevance | Growth characteristics | Reference(s) |
|---|---|---|---|---|---|
| Gram-positive cocci | |||||
| Streptococcus tigurinus sp. nov. | Streptococcaceae | Isolated from human blood | Associated with serious clinical infections, such as endocarditis, meningitis, spondylodiscitis, and possibly also periodontitis | Gram-positive non-motile cocci arranged in chains, colonies are white to gray, alpha-hemolytic on sheep blood agar after 24 h at 37°C | 15–22, 81 |
| Streptococcus anginosus subsp. whileyi subsp. nov | Streptococcaceae | Human throat | Not established | Grow well aerobically and anaerobically, growth enhanced by CO2, all strains are beta-hemolytic and contain Lancefield group C antigen | 82 |
| Streptococcus anginosus subsp. anginosus subsp. nov | Streptococcaceae | Human throat | Pharyngitis, pleuropulmonary, intraabdominal, and urogenital infections, bacteremia | Grow well aerobically and anaerobically, growth enhanced by CO2, all strains are beta-hemolytic and contain Lancefield group G antigen | 82 |
| Streptococcus constellatus subsp. viborgensis subsp. nov. | Streptococcaceae | Human throat | Not established | Grow well aerobically and anaerobically, growth enhanced by CO2, all strains are beta-hemolytic and contain Lancefield group C antigen | 82 |
| Streptococcus hongkongensis sp. nov. | Streptococcaceae | Infected tissue, marine fish | Wound infection | Facultatively anaerobic Gram-positive cocci, grow well on blood agar at 37°C, non-hemolytic | 83 |
| Streptococcus rubneri sp. nov. | Streptococcaceae | Human throat | Not established | Gram-positive ovoid cocci, grow well on CNA and 5% sheep blood agar at 37°C, 2 mm zone of beta-hemolysis | 84 |
| Streptococcus dentisani sp. nov | Streptococcaceae | Caries-free human tooth surfaces | Not established | Gram-positive cocci that grow in short chains, facultatively anaerobic, alpha-hemolytic on Columbia agar plates | 85 |
| Staphylococcus jettensis sp. nov. Reclassified as S. petrassii subsp. jettensis subsp. nov. | Staphylococcaceae | Multiple human specimen types: blood, CSF, deep wounds | Bacteremia, wounds | Facultatively anaerobic Gram-positive cocci, narrow zone of beta-hemolysis, late yellow pigment | 23, 24 |
| Staphylococcus petrasii subspecies pragensis subsp. nov. | Staphylococcaceae | Isolated from an ejaculate specimen of a man with prostatitis | Prostatitis | Spherical cocci appearing in pairs and clusters, weakly hemolytic on sheep blood agar, grow at 45°C, coagulase negative, novobiocin susceptible | 25 |
| Staphylococcus argenteus sp. nov. | Staphylococcaceae | Multiple specimen types, including blood | Bacteremia, skin, soft tissue, bone and joint infections | Creamy white colonies that exhibit beta-hemolysis on blood agar, coagulase positive, facultatively anaerobic | 26, 27 |
| Gemella parahemolysans sp. nov. | Not assigned | Isolated from blood cultures | Opportunistic infections in immunocompromised patients | Gram-positive cocci, non-hemolytic colonies on 5% SBA, grow as pinpoint colonies in 24 h at 37°C, facultatively anaerobic | 28 |
| Bacillales family XI incertae sedis | |||||
| Gemella taiwanensis sp. nov | Not assigned | Isolated from blood cultures | Opportunistic infections in immunocompromised patients | Gram-positive cocci, non-hemolytic colonies on 5% SBA, grow as pinpoint colonies in 24 h at 37°C, facultatively anaerobic | 28 |
| Bacillales family XI incertae sedis | |||||
| Gram-positive rods | |||||
| Dietzia aurantiaca sp. nov. | Dietziaceae | Isolated from human cerebrospinal fluid | Not established | Gram positive coccoid cells, oxidase and catalase positive, grow well at 10–37°C, optimal at 30°C, colonies are convex and have orange pigmentation | 86 |
| Bacillus cytotoxicus sp. nov. | B. cereus group Bacillaceae | Vegetable, potato purees, semolina | Food poisoning | Thermotolerant (grow at 20–50°C), facultative anaerobe | 87 |
| Lactobacillus saniviri sp. nov. | Lactobacillaceae | Isolated from feces of a healthy Japanese male | Not established | Gram-positive facultatively anaerobic rods, not spore forming, alpha hemolysis apparent after aerobic incubation for 3 d at 37°C | 29 |
| Lactobacillus senioris sp. nov. | Lactobacillaceae | Isolated from the feces of a 100-year-old female in Japan | Not established | Rod-shaped Gram-positive organisms that occur singly, in pairs, or in short chains, not spore forming, facultatively anaerobic, grows at 15–37°C | 29 |
| Lactobacillus hominis sp. nov. | Lactobacillaceae | Human intestine | Not established | Facultative anaerobe | 30 |
| Paenibacillus vulneris sp. nov | Paenibacillaceae | Necrotic wound | Wound infection | Aerobic spore forming | 88 |
| Nocardia amikacinitolerans | Nocardiaceae | Eye of a 12-year-old girl | Not established | Aerobic, orange pigmented, grows best at 25°C | 89 |
| Nocardia kroppenstedtii | Nocardiaceae | Isolated from a lung transplant patient with pulmonary infection | Pneumonia | Aerobic, Gram-positive partially acid fast rod forms irregular, wrinkled, matt, pale orange-yellow pigmented colonies after 5 days growth at 30°C, grows at 25–37°C, optimal at 28°C | 90 |
| Alicyclobacillus consociatus sp. nov. Reclassified as Effusibacillus consociatus comb. nov. | Alicyclobacillaceae | Blood from an adult woman | Bacteremia | Aerobic, spore-forming rods grow at 15–45°C, optimal at 30°C | 91, 92 |
| Hazenella coriacea gen. nov., sp. nov. | Thermoactinomycetaceae | Human blood | Bacteremia | Thin, branching Gram-positive spore-forming rods grow on sheep blood agar at 22–45°C, optimal at 42–45°C, beta-hemolysis observed at 48 h | 31 |
| Canibacter oris gen. nov., sp. nov. | Microbacteriaceae | Infected dog bite wound | Dog bite infections | Rod-shaped Gram-positive cells that form Y or V shapes, facultative anaerobe, non-hemolytic on sheep blood agar | 32 |
| Gordonia iterans sp. nov. | Nocardiaceae | Isolated from sputum of a patient with bacterial pneumonia | Pneumonia | Aerobic, Gram-positive, partially acid-fast coccobacilli, yellow-pigmented colonies, grows at 15–40°C | 93 |
| Gram-negative cocci | |||||
| Neisseria oralis sp. nov | Neisseriaceae | Human oral cavity and clinical samples | Bacteremia, also isolated from urine, peritoneal cavity | Gram-negative diplococci, yellow, grow best at 37°C in 5% CO2 | 33 |
| Faucicola mancuniensis gen nov. sp. nov | Moraxellaceae | Tonsils of a healthy adult female | Not established | Aerobic Gram-negative, non-motile coccus, growth occurs at 20–37°C on Columbia blood agar | 34 |
| Gram-negative rods | |||||
| Bartonella rochalimae sp. nov. | Bartonellaceae | Blood | Bacteremia in context of fever and splenomegaly | Aerobic, fastidious bacillus with unipolar flagella, growth on fresh defibrinated rabbit blood agar at 35°C with enhanced CO2 | 94a |
| Haemophilus sputorum sp. nov. | Pasteurellaceae | Blood, throat swab (5), sputum (2), female urethra, tooth alveolitis | Occasional involvement in human infections, has been isolated from cystic fibrosis patients | Beta-hemolysis on horse blood agar and sheep blood agar, rare strains do not grow on sheep blood agar, oxidase positive, catalase variable | 95b |
| Psychrobacter sanguinis sp. nov. | Moraxellaceae | Blood (4), cerebrospinal fluid | Not established in bacteremic patients, post-neurosurgical meningitis | Growth on blood agar, no growth on MacConkey agar, growth promoted by Tween 80, oxidase positive, non-glucose fermentative | 35, 36 |
| Legionella nagasakiensis sp. nov. | Legionellaceae | Bronchoalveolar lavage | Pneumonia | Growth on BCYE agar, requires l-cysteine, negative for β-galactosidase activity | 96 |
| Massilia oculi sp. nov. | Oxalobacteraceae | Ocular | Endophthalmitis | Beige colonies on blood agar and nutrient agar, growth on MacConkey agar, oxidase negative, assimilates D-glucose | 97 |
| Myroides phaeus sp. nov. | Flavobacteriaceae | Saliva | Not established | Growth of pale-yellow/brown colonies on routine laboratory medium at 6–37°C, optimal growth at 28°C, negative for β-galactosidase activity | 98 |
| Legionella steelei sp. nov. | Legionellaceae | Respiratory tract (2) | Not established | Growth on BCYE agar, requires l-cysteine, oxidase positive | 99 |
| Kerstersia similis sp. nov. | Alcaligenaceae | Leg wound (3), neck abscess | Skin and soft tissue infection | Growth on nutrient agar and blood agar, colonies are white-to-light brown and have swarming appearance, oxidase negative | 100 |
| Legionella cardiaca sp. nov. | Legionellaceae | Aortic valve tissue | Native valve endocarditis | Growth on BCYE agar, requires l-cysteine, non-glucose fermentative | 101 |
| Cruoricaptor ignavus gen. nov. sp. nov. | Flavobacteriaceae | Blood | Septicemia | Yellowish-orange, non-hemolytic colonies on Columbia agar with 5% sheep blood, chocolate agar, no growth on MacConkey agar, optimal growth in microaerobic or capnophilic environments, cells are non-motile, oxidase positive, acid not generated from D-glucose | 102c |
| Herbaspirillum massiliense sp. nov. | Oxalobacteraceae | Feces | Not established | 2-mm diam convex, cream-colored, opaque colonies on BHI agar, optimal growth at 30–37°C in aerobic conditions, oxidase negative | 103d |
| Enterobacter massiliensis sp. nov. | Enterobacteriaceae | Feces | Not established | 0.5-mm diam light-brown, opaque colonies on blood agar, optimal growth at 37°C in aerobic conditions, oxidase-positive, curved Gram-negative bacillus | 104d |
| Acidovorax wautersii sp. nov. | Comamonadaceae | Blood (1), non-specified human isolate (1) | Not established | Growth on routine media in 37°C aerobic environment but not at 42°C, oxidase positive, urease positive, indole negative | 70 |
| Achromobacter animicus sp. nov. | Alcaligenaceae | Sputum (3) | Not established, has been isolated from cystic fibrosis patients | Growth of some strains at 42°C, tolerates 3% NaCl, no acid generated from D-glucose, no glucose assimilation | 105e |
| Achromobacter mucicolens sp. nov. | Alcaligenaceae | Sputum (4), epiglottis swab (1) | Not established, has been isolated from cystic fibrosis patients | Growth of most strains at 42°C, tolerates 3% NaCl, no acid generated from D-glucose, no glucose assimilation | 105e |
| Achromobacter pulmonis sp. nov. | Alcaligenaceae | Sputum (3) | Not established, has been isolated from cystic fibrosis patients | Growth of most strains at 42°C, tolerates 3% NaCl, no acid generated from D-glucose, glucose assimilation is strain-dependent | 105e |
| Achromobacter spiritinus sp. nov. | Alcaligenaceae | Sputum (3) | Not established | Growth of some strains at 42°C, tolerates 3% NaCl, no acid generated from D-glucose, no glucose assimilation | 105e |
| Burkholderia pseudomultivorans sp. nov. | Burkholderiaceae | Sputum (10) | Not established, has been isolated from cystic fibrosis patients | Growth capable at 42°C, growth on blood agar and MacConkey agar, oxidase positive, lysine decarboxylase positive, ornithine decarboxylase negative | 106d |
| Frederiksenia canicola gen. nov., sp. nov. | Pasteurellaceae | Skin and soft tissue (3) | Canine bite wound | Non-hemolytic colonies on blood agar, oxidase positive, indole positive, glucose fermentation without gas production, CAMP test positive | 107f |
| Yersinia wautersii sp. nov. | Enterobacteriaceae | Feces, one other human isolate not well defined | Putative pathogenicity elucidated only by characterization of genetic determinants, taxonomic status questioned by reference 108 | Overnight growth on routine media at 28°C and 37°C, urease positive, indole negative | 108, 109f |
| Pelistega indica sp. nov. | Alcaligenaceae | Feces | Not established | Growth on TSA and MacConkey agars at 20–40°C, optimal growth at 30–35°C, motile organisms that are catalase negative and oxidase positive | 110 |
| Campylobacter fetus subsp. testudinum subsp. nov. | Campylobacteraceae | Feces, blood, pleural fluid, hematoma, bile | Diarrhea, pulmonary edema, cellulitis documented in references 38, 40 | Growth on blood agar in microaerobic conditions at 25–42°C, majority of strains grow microaerobically on MacConkey agar, oxidase positive, catalase positive, urease negative, non-hydrolysis of hippurate and indoxyl acetate | 37–40 |
| Streptobacillus hongkongensis sp. nov. | Bacteroidaceae | Aspirate, olecranon fluid | Peritonsillar abscess, septic arthritis | Optimal growth after 48 h on Columbia agar with 5% sheep blood either incubated in 37°C anaerobic environment or in 37°C aerobic environment supplemented with 5% CO2, no growth on MacConkey agar, oxidase negative | 111 |
| Klebsiella quasipneumoniae subsp. quasipneumoniae subsp. nov. | Enterobacteriaceae | Human infection (9), type strain derived from blood | Not established | Growth characteristics similar to other Klebsiella spp., utilizes tricarballylic acid, lysine decarboxylase positive, ornithine decarboxylase negative, indole negative, urease positive | 71 |
| Klebsiella quasipneumoniae subsp. similipneumoniae subsp. nov. | Enterobacteriaceae | Human infection (3), type strain derived from blood | Not established | Growth characteristics similar to other Klebsiella spp., utilizes tricarballylic acid, lysine decarboxylase positive, ornithine decarboxylase negative, indole negative, urease-positive | 71 |
| Vibrio metoecus sp. nov. | Vibrionaceae | Blood, stool | Hypothesized to be an opportunistic pathogen | Typical Vibrio cholerae-like appearance after 30°C incubation on thiosulfate citrate bile salts medium, negative Voges-Proskauer reaction, utilizes D-glucuronic acid | 72 |
| Pseudocitrobacter faecalis sp. nov. | Enterobacteriaceae | Feces | Clinical significance not established, isolate possessed NDM-1 carbapenemase and CTX-M-15 extended spectrum β-lactamase | Non-hemolytic, oxidase-negative, facultative anaerobe, lysine decarboxylase negative, ornithine decarboxylase negative | 112g |
| Pseudocitrobacter anthropi sp. nov. | Enterobacteriaceae | Feces | Clinical significance not established, isolate possessed NDM-1 carbapenemase and CTX-M-15 extended spectrum β-lactamase | Non-hemolytic, oxidase-negative, facultative anaerobe, weakly positive for lysine and ornithine decarboxylases | 112g |
| Myroides injenensis sp. nov. | Flavobacteriaceae | Urine | Febrile illness | Pale-yellow or ivory colonies on TSA, strictly aerobic, cells are non-motile, grow at 10–45°C (optimal at 37°C), oxidase positive, urease positive | 113h |
| Acinetobacter variabilis sp. nov. | Moraxellaceae | Urine (2), feces (1), ocular (2), blood (2), leg (2), peritoneal dialysis fluid (1), toe (1) | Not established | Strictly aerobic, oxidase-negative Gram-negative cocci, non-hemolytic colonies generated following overnight incubation at 25–41°C | 73 |
| Acinetobacter seifertii sp. nov. | Moraxellaceae | Blood (9), ulcer (1), respiratory (3) | Not established | Growth similar to other Acinetobacter spp. | 74 |
| Citrobacter pasteurii sp. nov. | Enterobacteriaceae | Feces | Diarrhea outbreak | Growth similar to other Citrobacter spp., catalase negative, indole negative | 114 |
| Rouxiella chamberiensis sp. nov. | Enterobacteriaceae | Parenteral nutrition bag (6) | Nutrition intended for premature newborns (NICU) | Growth on routine media (lemon yellow colonies) at 4–30°C, optimal growth at 30°C, non-hemolytic on blood agar, non-lactose fermenter on MacConkey agar, cells are non-motile, positive Voges-Proskauer reaction | 115 |
| Paracoccus sanguinis sp. nov. | Rhodobacteraceae | Blood (4) | Not established | Grow at 22–37°C, optimal at 28°C, pale-yellow, non-hemolytic colonies on blood agar, oxidase positive, urease negative, no decarboxylation of ornithine, lysine, or arginine | 75 |
| Tatumella saanichensis sp. nov. | Enterobacteriaceae | Sputum | Not established, has been isolated from cystic fibrosis patients | Growth on blood agar, incubation at 25–35°C, cells are non-motile, oxidase negative, lactose fermentative, negative Voges-Proskauer reaction | 116 |
| Burkholderia stagnalis sp. nov. | Burkholderiaceae | Tracheal aspirate, sputum | Not established, has been isolated from cystic fibrosis patients | Growth on blood, Burkholderia cepacia-selective, and MacConkey agar, rare beta-hemolysis, majority can be cultivated at 42°C, cells are motile, delayed oxidase-positive reaction | 117 |
| Bartonella ancashensis sp. nov. | Bartonellaceae | Blood (2) | Verruga peruana | Growth on TSA and Columbia agars with 5% sheep blood, growth on BHI with 10% sheep blood, no growth on chocolate agar, optimal growth after 10 d in 30°C 5% CO2, oxidase negative, catalase negative, urea negative, cells are non-motile | 118 |
| Pantoea intestinalis sp. nov. | Enterobacteriaceae | Feces | Not established | Growth on routine laboratory medium at 15–45°C, optimal growth at 35°C, urease negative, oxidase negative | 119 |
| Bordetella bronchialis sp. nov. | Alcaligenaceae | Respiratory (2) | Not established, has been isolated from cystic fibrosis patients | Non-hemolytic on blood agar, no growth on centrimide agar, growth in 3% NaCl, no growth in 4.5% NaCl | 120 |
| Bordetella flabilis sp. nov. | Alcaligenaceae | Sputum | Not established, has been isolated from cystic fibrosis patient | Non-hemolytic on blood agar, no growth on centrimide agar, no growth in 3% NaCl, no growth in 4.5% NaCl | 120 |
| Bordetella sputigena sp. nov. | Alcaligenaceae | Sputum | Not established, has been isolated from cystic fibrosis patient | Weakly-hemolytic on blood agar, weak growth on centrimide agar, growth in 3% NaCl, no growth in 4.5% NaCl | 120 |
| Gram-positive anaerobes | |||||
| Methanomassiliicoccus luminyensis gen. nov, sp. nov. | Not assigned | Isolated from human feces from a person in Marseille France | Not established | Regular, non-motile Gram-positive cocci, obligate anaerobe, produces methane | 121 |
| Ruminococcus champanellensis sp. nov. | Ruminococcaceae | Human feces | Not established | Non-motile Gram-positive cocci, strictly anaerobic- grow at 33–39°C | 122 |
| Blautia stercoris sp. nov. | Lachnospiraceae | Isolated from human feces | Not established | Strictly anaerobic Gram-positive cocci, non-motile, non-spore-forming, grow well at 37°C | 123 |
| Blautia faecis sp. nov. | Lachnospiraceae | Human intestine | Not established | Strict anaerobe Gram-positive cocci | 124 |
| Peptoniphilus duerdenii sp. nov. | Peptoniphilaceae | Isolated from human vaginal abscess | Wound infections | Anaerobic Gram-positive cocci, cells are gray, convex, circular on Brucella blood agar at 37°C after 5 d, indole-positive assacharolytic | 41 |
| Peptoniphilus koenoeneniae sp. nov. | Peptoniphilaceae | Isolated from a human buttock abscess | Wound infections | Obligately anaerobic Gram-positive cocci, cells are gray, convex, circular on Brucella blood agar at 37°C after 5 d, indole-positive assacharolytic | 41 |
| Lachnoanaerobaculum umeaense gen. nov. sp. nov. | Lachnospiraceae | Isolated from the small intestine of a child with celiac disease | Not established | Obligately anaerobic, saccharolytic spore-forming Gram-positive rod, easily decolorized, colonies are spreading and flat on blood agar 72 h at 37°C | 125 |
| Lachnoanaerobaculum orale gen. nov. sp. nov | Lachnospiraceae | Isolated from saliva of a healthy man | Not established | Obligately anaerobic, saccharolytic spore-forming Gram-positive rod, easily decolorized, colonies are spreading and circular with rhizoid edges on blood agar 72 h at 37°C | 125 |
| Stomatobaculum longum gen. nov., sp. nov | Lachnospiraceae | Human oral cavity | Human periodontal infection | Strict anaerobic rods that stain Gram variable | 126 |
| Fusicatenbacter saccharivorans gen nov., sp. nov. | Lachnospiraceae | Human feces | Not established | Gram-positive non-spore-forming rods, spindle shaped in pairs and chains, grow well on Brucella agar at 37°C, non-hemolytic | 127 |
| Anaerostipes rhamnosivorans | Lachnospiraceae | Human feces | Not established | Spore-forming rods that form curly cells in old cultures, stain Gram variable, optimal growth at 37°C | 128 |
| Gordonibacter urolithinfaciens sp. nov. | Coriobacteriaceae | Human feces | Not established | Obligately anaerobic, non-spore-forming Gram-positive coccobacilli | 129 |
| Oribacterium parvum sp. nov. | Lachnospiraceae | Human subgingival dental plaque | Periodontal disease? | Gram-positive short ovoid rods that stain Gram variable, yeast extract required for growth, grow at 30–42°C, strict anaerobe | 130 |
| Oribacterium asaccharolyticum sp. nov. | Lachnospiraceae | Human subgingival dental plaque | Periodontal disease | Gram-positive short ovoid rods that stain Gram variable, yeast extract required for growth, grow at 30–42°C, strict anaerobe | 130 |
| Bifidobacterium faecale sp. nov. | Bifidobacteriaceae | Human feces | Unknown | Gram-positive Y-shaped short rods, obligately anaerobic, grow at 30–42°C (optimal at 37°C) | 131 |
| Atopobium deltae sp. nov. | Coriobacteriaceae | Blood of a patient with Fournier's gangrene | Bacteremia | Gram-positive obligately anaerobic short rod, non-hemolytic | 43 |
| Actinotignum schaalii comb. nova | Actinomycetaceae | Urine of humans | Urinary tract infections | Gram-positive, non-motile, non-spore-forming slightly curved rods, facultatively anaerobic, do not branch | 42, 132, 133 |
| Actinotignum sanguinis sp. nov. | Actinomycetaceae | Blood cultures of a human with sepsis | Bacteremia/sepsis | Gram-positive, non-motile, non-spore-forming slightly curved rods, facultatively anaerobic, do not branch | 132 |
| Gram-negative anaerobes | |||||
| Christensenella minuta gen nov., sp. nov. | Christensenellaceae fam. nov. | Isolated from human feces | Not established | Non-spore-forming, short, anaerobic, Gram-negative rods, grow at 25–43°C, optimal growth at 37–40°C | 134 |
| Fretibacterium fastidiosum sp. nov. | Synergistaceae | Human oral cavity | Human periodontal infection | Strict anaerobe, require co-cultivation with other oral bacteria | 135 |
| Veillonella tobetsuensis sp. nov. | Veillonellaceae | Human tongue biofilm | Not established | Anaerobic cocci | 136 |
| Veillonella seminalis sp. nov. | Veillonellaceae | Human semen | Not established | Gram-negative anaerobic cocci arranged in pairs or short chains, grow well anaerobically on Columbia blood agar at 37°C | 137 |
| Alloprevotella rava gen. nov. sp. nov. | Prevotellaceae | Human oral cavity | Not established | Strict anaerobe grows best at 35°C, range 30–42°C | 138 |
| Coprobacter fastidiosus gen nov., sp. nov. | Porphyromonadaceae | Infant feces | Not established | Strict anaerobic, Gram-negative rod grows on enriched media at 30–37°C | 139 |
| Prevotella jejuni sp. nov. | Prevotellaceae | Small intestine of a child with celiac disease | Not established | Strict anaerobe, Gram negative, grow slowly on blood agar plates at 37°C, beta-hemolytic | 140 |
| Eisenbergiella tayi gen nov., sp. nov. | Lachnospiraceae | Isolated from the blood of an elderly man | Bacteremia | Strict anaerobe | 44 |
| Megasphaera indica sp. nov. | Veillonellaceae | Isolated from stool of healthy humans | Not established | Strict anaerobic cocci, grow at 15–37°C (optimal at 37°C) | 141 |
| Butyricimonas faecihominis sp. nov. | Porphyromonadaceae | Human feces | Not established | Obligately anaerobic, non-pigmented, rods, grow optimally at 37°C | 142 |
| Butyricimonas paravirosa sp. nov. | Porphyromonadaceae | Human feces | Not established | Obligately anaerobic, non-pigmented rods, grow optimally at 37°C | 142 |
| Parabacteroides faecis sp. nov. | Porphyromonadaceae | Human feces | Not established | Obligately anaerobic, non-pigmented, non-spore forming rods, grow optimally at 37°C | 143 |
| Porphyromonas pasteri sp. nov. | Porphyromonadaceae | Human saliva | Not established | Obligately anaerobic, non-pigmented, non-spore-forming rods, grow slowly at 37°C | 144 |
| Spirochetes | |||||
| Borrelia kurtenbachii sp. nov. | Member of the Borrelia burgdorferi sensu lato species complex in North America | Ixodes scapularis | Not established | BSK and BSK-K5 mediumi | 145 |
| Leptospira mayottensis sp. nov. | Leptospiraceae | Isolated from blood of patients with leptospirosis in Mayotte | Leptospirosis | Strains grow well in EMJH medium at 30°C and 37°C | 45 |
Taxonomic designation subsequently accepted in validation list no. 144 (146).
Taxonomic designation subsequently accepted in validation list no. 146 (147).
Taxonomic designation subsequently accepted in validation list no. 149 (148).
Taxonomic designation subsequently accepted in validation list no. 155 (149).
Taxonomic designation subsequently accepted in validation list no. 152 (150).
Taxonomic designation subsequently accepted in validation list no. 158 (151).
Taxonomic designation subsequently accepted in validation list no. 157 (60).
Taxonomic designation subsequently accepted in validation list no. 163 (152).
BSK medium is the name applied to a selective medium used to grow the Lyme disease spirochete. BSK-K5 has kanamycin and 5 fluorouracil.
In such fashion, all issues of IJSEM that were published between January 2012 and December 2015 were searched for original articles describing new species taxonomy or for 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 were utilized to attempt to index subsequent case reports for further investigation; several of these case reports are referenced throughout this report. A number of IJSEM publications (examples provided in [35, 70–75]) 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 a number of novel taxa derived from blood culture), clinical significance of these taxa was interpreted as “not established.” Future studies may be necessary to characterize the true clinical significance of novel taxa (76).
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. Two such examples of taxonomic opinion (77, 78) are presented in Table 2, with antecedent primary referenced literature (79, 80). These entries have been included with the goal of revisiting them in future Journal of Clinical Microbiology compendia to either ascertain true clinical significance or to determine if official taxonomic status has been granted.
RESULTS AND DISCUSSION
Table 1 lists the new taxa recovered from humans stratified by Gram reaction and morphology. Many of the new genera and species were likely discovered from studies of the human microbiome. Much of what is listed, while recovered from human clinical material, has unknown clinical significance. There are a few exceptions that warrant emphasis.
GRAM-POSITIVE COCCI
Seven new Streptococcus species were characterized during the study period, as highlighted in Table 1. Streptococcus tigurinus, a new member of the Streptococcus mitis group, was discovered by Zbinden et al. in 2012, when it was recovered from the blood and aortic valve of a 74-year-old Swiss patient with endocarditis (15, 16). The authors performed a retrospective review of their institution's 16S rRNA gene sequence database in the 10-year period prior to 2012, and a total of 15 patients with S. tigurinus infections were discovered (16). A review of the charts revealed that all of the infections were serious and invasive and included 12 cases of bacteremia, seven of which were from patients with endocarditis (16). Other invasive infections included spondylodiscitis, prosthetic joint infections, meningitis, encephalitis, and empyema (16). Others have subsequently reported similar severe infections in patients from Korea (17), Japan (18), and the United States (19). The high virulence potential of this organism has been demonstrated in a rat model of endocarditis wherein it was demonstrated that S. tigurinus strains have increased abilities to resist macrophage-mediated phagocytosis and to invade endothelial cells (20). The oral cavity is the presumed source of the organism. An initial study found that this organism was not prevalent in the saliva of healthy volunteers (16). However, using more sensitive molecular techniques, the same group obtained saliva and pooled plaque samples from a non-periodontitis control group and a group with periodontitis (21). The overall prevalence of S. tigurinus was 53% in 51 patients and there was no difference in the frequencies of detection between the two groups (21). MALDI-TOF MS misidentifies S. tigurinus as Streptococcus oralis, Streptococcus pneumoniae, or other member of the mitis group with scores >2.0 (16, 19, 22). Identification requires the use of 16S rRNA partial or full-gene sequencing or other molecular methods (21).
Two new subspecies of the coagulase-negative Staphylococcus petrasii have been characterized. Subspecies jettensis was recovered from wounds and implicated in bacteremia, whereas subspecies pragensis is believed to have caused prostatitis (23–25). One new species of coagulase-positive Staphylococcus, Staphylococcus argenteus, was isolated from the blood of a person in Australia. This organism is phenotypically very similar to S. aureus and has likely been misidentified as such (26). The 16S rRNA gene sequence (1,474 nucleotide [nt]) of S. argenteus is identical to that of S. aureus. However, whole-genome sequencing indicates that they are separate species. In addition, the proteomics profile of S. argenteus using MALDI-TOF MS is different from that of S. aureus (26). A study in Thailand demonstrated that 4.1% of isolates believed to be S. aureus were subsequently determined to be S. argenteus (27). This organism was associated primarily with community-acquired skin and soft tissue infections, although bacteremia and bone and joint infections were seen in three and two patients, respectively (27).
Similar to other Gemella species, the two new additions to the genus, G. taiwanensis and G. parahaemolysans, were isolated from blood cultures and are believed to be a cause of opportunistic infections in immunocompromised patients (28). All of the patients from whom these isolates were recovered had significant comorbidities, including various types of solid tumors (28). These organisms grow slowly on 5% sheep blood agar and are nonhemolytic. They are easily decolorized during Gram staining (28). Biochemical tests can be used to differentiate them from other species of Gemella (28).
GRAM-POSITIVE RODS
Many aerobic or facultatively anaerobic Gram-positive rods were discovered during the 4-year period of this review. The new species of lactobacilli were recovered from the feces of patients who were otherwise healthy and likely represent a component of the normal intestinal microbiota (29, 30). Several new aerobic actinomycetes in the Nocardia and Gordonia genera were recovered from patients with pneumonia, thereby contributing to the growing list of opportunistic pathogens in immunocompromised patients. Two new genera were also described. Hazenella coriacea grows optimally between 42 and 45°C and was recovered from the blood of three separate patients, although the details of their illnesses were not provided (31). Canibacter oris was recovered from both a swab and purulent material from an infected dog-bite wound on the finger of a 58-year-old patient in Australia (32).
GRAM-NEGATIVE COCCI
Two new Gram-negative cocci have been characterized. Neisseria oralis (33) is a new species that is found in the human oral cavity and is associated with a variety of infections. The clinical significance of the new genus and species Faucicola mancuniensis, recovered from the tonsils of an otherwise healthy woman, has not been established (34).
FACULTATIVE GRAM-NEGATIVE RODS
With respect to novel Gram-negative bacillus taxa, the oxidase-positive Psychrobacter sanguinis sp. nov. was first identified from four archival blood culture isolates originating from New York (35). Clinical significance was uncertain among any of these cases, as pertinent clinical data were not provided. Full-gene 16S rRNA sequencing reported 99.7% genetic similarity to Psychrobacter sp. PRwf-1, a strain originating from a fish species caught in Puerto Rico. The aquatic strain was subsequently reclassified as P. sanguinis. A French group recently reported a case of post-neurosurgical meningitis with P. sanguinis etiology (36). An external ventricular drain was instilled into a 64-year-old female to relieve elevated intracranial pressure. Approximately 1 week after the procedure, the organism was cultivated following a lumbar puncture. It was hypothesized that the patient repeatedly touched the drain with her bare hands, facilitating the introduction of organisms from an environmental (nosocomial) source.
In 1985, Harvey and Greenwood (37) reported the isolation of Campylobacter fetus from a pet turtle in the context of three clinically ill household members and concomitant isolation of Salmonella enterica serovar Agona. Molecular analysis of a C. fetus subsp. fetus blood culture isolate derived from a precursor T lymphocyte acute lymphoblastic leukemia patient indicated a reptilian origin (38). This isolate and other archival human strains were paired with five C. fetus-like organisms from reptiles, subjected to a number of characterizations (including MALDI-TOF MS and whole-genome sequencing), and granted the novel taxon Campylobacter fetus subsp. testudinum subsp. nov. (39). Epidemiologic investigation indicated that afflicted individuals were largely Asian men who reported consumption of Asian foods or had previous exposure to reptiles (40).
ANAEROBES
Many new anaerobes have been discovered. Some have been recovered from the stool of healthy children and adults and likely represent components of the normal microbiota. Others have been isolated from dental plaque, but whether they cause periodontal disease is unclear at present. A few organisms are worth highlighting. Among the Gram-positive anaerobes, two new Peptoniphilus species, namely, duerdenii and koenoeneniae were recovered from abscesses of the vagina and buttocks, respectively (41). Actinobaculum schaalii has been moved into the genus Actinotignum. The three species in this genus, schaalii, urinale, and sanguinis, are part of the urinary microbiota, but they are also associated with urinary tract infections in men and young children (42). MALDI-TOF MS can identify these species, and the correct identification is important, as A. schaalii, the most common pathogen in the genus, is resistant to trimethoprim-sulfamethoxazole and ciprofloxacin, which are the agents commonly used for the treatment of urinary tract infections (42). Atopobium deltae, another novel Gram-positive anaerobe, was recovered from the blood of a patient with Fournier's gangrene (43). Most of the newly discovered Gram-negative anaerobes have not been clearly associated with clinical infections, except for the new genus and species Eisenbergiella tayi (44), which was associated with bacteremia in an elderly patient. Of the spirochetes recently characterized, Leptospira mayottensis has been associated with clinical disease in patients from Mayotte in the Indian Ocean (45).
TAXONOMIC REVISIONS
Table 2 lists the taxonomic revisions for organisms recovered from humans, stratified by Gram reaction and morphology. A recent report describing the successful culture propagation of what was formerly classified as “Candidatus Helicobacter heilmannii” from feline gastric mucosa resulted in its assignment to the taxon Helicobacter heilmannii sp. nov. (46). While most descriptions of this organism are associated with veterinary bacteriology, evidence does exist for the presence of this organism in human tissue (reviewed in reference 47).
Aeromonas hydrophila subsp. dhakensis and Aeromonas aquariorum were reclassified in 2013 under the singular taxon Aeromonas dhakensis sp. nov. comb. nov. (48). Formal acceptance by the IJSEM was granted in 2015 (49). The initial characterization of A. hydrophila subsp. dhakensis occurred in the context of diarrheal illness in Bangladesh (50). In addition to gastroenteritis, reports have suggested a significant distribution of (the former) A. aquariorum extraintestinal infections in a variety of geographic locations (51, 52). Chen et al. (53) reviewed 80 cases of Aeromonas spp. wound infections in Taiwan. It was found that 46.3% of these infections were caused by A. dhakensis, while 16.3% were of A. hydrophila etiology. Compared to other Aeromonas spp., A. dhakensis was also associated with antecedent environmental water exposure, biofilm formation, and increased in vitro cytotoxicity. Furthermore, the organism generated increased MIC values for ceftriaxone, gentamicin, and imipenem.
Wautersiella falsenii was reclassified in 2014 as Empedobacter falsenii comb. nov. (54). Twenty-six human isolates from Belgium (including blood, ear discharge, oral cavity, pleural fluid, pus, respiratory tract, wound, and vaginal swab) contributed to the initial W. falsenii designation (55). Again, clinical manifestations of illness were not described in this report. van der Velden et al. (56) presented the case of a febrile 1-year-old girl with pyelonephritis caused by W. falsenii. The identification of the organism was facilitated by MALDI-TOF MS and confirmed by partial-gene 16S rRNA sequencing. An intravenous 2-week ciprofloxacin regimen brought about clinical and microbiologic improvement. Traglia et al. (57) described the isolation of E. falsenii from a cervical neck abscess specimen obtained from an 18-year-old female with acute otitis media. Similar to the previous clinical report (56), the E. falsenii isolate exhibited decreased susceptibilities to colistin, ceftazidime, piperacillin-tazobactam, representative carbapenems, and additional β-lactam/β-lactamase inhibitor combinations.
POTENTIAL EMERGING PATHOGENS
While not included within the formal tables of this review, the following encompass examples of new taxa that could conceivably transcend into the realm of human clinical disease. Rickettsia buchneri sp. nov. (58) is a Gram-negative bacillus isolated from ovaries of the Ixodes scapularis vector already known to deliver a number of bacterial and parasitic species to accidental human hosts. Mediannikov et al. (59) isolated and characterized the Gram-negative bacillus Bartonella senegalensis sp. nov. from the soft tick Ornithodoros sonrai, a vector of relapsing fever. This novel taxon was subsequently approved by IJSEM (60). Klebsiella michiganensis sp. nov. (61) is a newly characterized Gram-negative bacillus isolated from a toothbrush holder, with taxonomy subsequently accepted by IJSEM (62). Brady et al. (63) described taxonomic reclassification of Enterobacter oryzae and Enterobacter turicensis as Kosakonia oryzae comb. nov. and Cronobacter zurichensis nom. nov., respectively, with subsequent acceptance by IJSEM (64). In antecedent publications, the former E. oryzae and E. turicensis were recovered from wild rice (65) and fruit powder (66), respectively. Stephan et al. (67) published the taxonomic reclassification of Enterobacter pulveris as Franconibacter pulveris comb. nov. Isolation of this organism from infant formula was previously described (68). These organisms with inferred pathogenic potential provide the basis for follow-up database searches in future Journal of Clinical Microbiology taxonomy compendia.
In summary, over the 4-year period of this review, both the expansion of new technologies and the characterization of the human microbiome have led to the discovery of a broad range of bacterial organisms that are part of the normal human microbiota. In addition, the new tools have enabled a more comprehensive assessment of closely related pathogens and the discovery of novel clinically significant organisms. We attempted to highlight those pathogens and, where possible, to describe their epidemiologic and clinical niches.
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