Valid and accepted novel bacterial taxa derived from human clinical specimens and taxonomic revisions published in 2022
ABSTRACT
Although some nomenclature changes have caused consternation among clinical microbiologists, the discovery of novel taxa and improving classification of existing groups of organisms is exciting and adds to our understanding of microbial pathogenesis. In this mini-review, we present an in-depth summary of novel taxonomic designations and revisions to prokaryotic taxonomy that were published in 2022. Henceforth, these bacteriology taxonomic summaries will appear annually. Several of the novel Gram-positive organisms have been associated with disease, namely, the Corynebacterium kroppenstedtii-like organisms Corynebacterium parakroppenstedtii sp. nov. and Corynebacterium pseudokroppenstedtii sp. nov. A newly described Streptococcus species, Streptococcus toyakuensis sp. nov., is noteworthy for exhibiting multi-drug resistance. Among the novel Gram-negative pathogens, Vibrio paracholerae sp. nov. stands out as an organism associated with diarrhea and sepsis and has probably been co-circulating with pandemic Vibrio cholerae for decades. Many new anaerobic organisms have been described in this past year largely from genetic assessments of gastrointestinal microbiome collections. With respect to revised taxa, as discussed in previous reviews, the genus Bacillus continues to undergo further division into additional genera and reassignment of existing species into them. Reassignment of two subspecies of Fusobacterium nucleatum to species designations (Fusobacterium animalis sp. nov. and Fusobacterium vincentii sp. nov.) is also noteworthy. As was typical of previous reviews, literature updates for selected clinically relevant organisms discovered between 2017 and 2021 have been included.
INTRODUCTION
Since the inaugural set of taxonomy publications in the Journal of Clinical Microbiology in 2017 (1 – 5), the Journal has supported biennial updates of novel taxa and attempted clarification of revised nomenclature in all major areas of clinical microbiology. Henceforth, the updates for bacteriology will be published annually for more timely clinical applications and will continue to focus on organisms recovered from human clinical material.
Reclassification of organisms and nomenclature changes continues to be a controversial topic among the clinical microbiology community (6). Certainly, there are some examples that have generated confusion and potential harm to patient care and public health reporting, such as the reassignment of some Ochrobactrum spp. to the genus Brucella (7, 8). In these scenarios, rejection of the reclassification can be supported and formal appeals [(nomina rejicienda), 9] seem appropriate.
In other situations, phylogenetic studies of novel organisms have enhanced knowledge of the microbiome, reassigned outliers with unusual phenotypes to novel genera or species designations [e.g., reassignment of the non-toxigenic Corynebacterium diphtheriae biovar Belfantii to Corynebacterium belfantii (10, 11)], and have alerted us to potential emerging pathogens. Two examples of the latter, highlighted in previous reviews, include characterization of Lawsonella clevelandensis, a strictly anaerobic coryneform-like organism associated with various abscess formation including vascular graft infections (12) and Enterobacter bugandensis (13), a cause of neonatal sepsis, now considered the most pathogenic species within the genus Enterobacter (14). What began as a solution to satisfy a laboratory accreditation requirement (15) has blossomed into a project to further our understanding of disease etiology and epidemiology.
In addition to these efforts, Bartlett et al. (16) recently compiled a list of known bacterial organisms to which prior Journal of Clinical Microbiology taxonomy reviews have contributed. The authors’ intent is to maintain a list of known bacterial organisms, to designate them as pathogens and to expand our knowledge of phylogenetic diversity. The authors define organisms recovered from symptomatic individuals as “established” or “putative” pathogens (16). An organism is considered an established pathogen if three or more persons infected with that organism are described in three or more references. Using their comprehensive search strategy and applying the above definitions, the authors noted 1,531 human bacterial pathogens prior to the year 2021 (16). Complete lists of these species can be found on https://github.com/padpadpadpad/bartlett_et_al_2022_human_pathogens.
Herein, we add to previous updates by summarizing novel bacterial taxa and prokaryotic nomenclature revisions published in the year 2022. Taxonomic designations of presented organisms have been accepted by the International Journal of Systematic and Evolutionary Microbiology (IJSEM).
MATERIALS AND METHODS
Valid and effectively published novel and revised taxa pertinent to bacteriology must satisfy two requirements set forth by the International Committee on Systematics of Prokaryotes within The International Code of Nomenclature of Prokaryotes (9). First, original investigations may be primary published in IJSEM. One example is provided in (17). In addition, type strains are to be deposited into recognized culture collections in two separate countries. As of January 2018, whole genome sequencing data relative to the type strain must be deposited in GenBank (18), with the genome accession number included as part of the effective description. Similarity of this sequence is to be assessed versus related taxa.
As an alternative to primary publication in IJSEM, studies may be published in another journal with later acceptance by IJSEM by way of Validation Lists that are published six times per year. For example, Faecalibacterium longum was effectively described in a 2021 publication (19), with subsequent acceptance on Validation List no. 201 (20). To be considered for inclusion on a Validation List, authors must submit a copy of the previously published manuscript to the editorial office of IJSEM for confirmation that all elements necessary for valid publication (including culture collection deposition) have been met. It must be noted that taxa scribed on Validation Lists or within primary publication may be subject to reclassification on the basis of synonym status or transfer to another genus [one example of such progression is found in references (21 – 23)]. We attempt to capture additional revisions in this report.
In such fashion, journals that have recently published studies providing an effective description of human clinical source-derived novel taxa include Antonie Van Leeuwenhoek, Applied and Environmental Microbiology, Archives of Microbiology, Frontiers in Microbiology, ISME Communications, Journal of Global Antimicrobial Resistance, Journal of Microbiology, Microbiology and Immunology, MicrobiologyOpen, Microbiology Spectrum, Microbiome, and Systematic and Applied Microbiology. Journals that have recently published studies reflecting revisions in prokaryotic taxonomy relative to human clinical material include Current Microbiology, Frontiers in Microbiology, and Microorganisms.
All issues of IJSEM published from January 2022 to December 2022 were searched for original articles (along with six Validation Lists) describing valid and effectively published new species or accepted changes in taxonomic nomenclature. Only nomenclature with taxonomic status of “correct name” (per data curated by LPSN—List of Prokaryotic names with Standing in Nomenclature; https://lpsn.dsmz.de) was included. The audit was further filtered by organisms recovered from human clinical specimens. When an initial organism reservoir could not be ascertained, PubMed primary literature searches (United States National Library of Medicine and the National Institutes of Health) attempted to index subsequent literature for further investigation; a number of these supplemental reports are referenced throughout this mini-review.
Some IJSEM publications simply identified isolates as being derived from a specific specimen source (including sterile body sites) but did not provide contextual clinical data. In such scenarios, clinical significance of these taxa was interpreted as “not established.” Further following this paradigm, a number of novel taxa included within this compendium (24 – 26) were derived from blood cultures but were not accompanied by any summary of clinical manifestations of infection. The publication of Agrobacterium tomkonis sp. nov. (27) from cerebrospinal fluid was simply accompanied by commentary stating that this Gram-negative bacillus could act as an opportunistic pathogen. These paucities of provided clinical data may leave pathogenicity and clinical significance assessments of these isolates up to debate. Additional studies and published case reports (28) from reliable, not predatory, journal outlets (29) can assist in the further clinical characterization of novel taxa.
RESULTS AND DISCUSSION
A compilation of novel taxa of potential or established clinical significance recovered from human sources, stratified by Gram reaction, cellular morphology, and oxygen growth requirement, is presented in Table 1. Novel taxa with no clearly established clinical significance to date are located in Table S1. The established phenotypic-based categories within both tables appeal to the practicing medical microbiologist. Taxa are presented in alphabetic order, rather than chronologic order, within each stratification. Table 2 provides taxonomic revisions for organisms originally recovered from human sources. On the basis of recent peer-reviewed publications, Table 3 attempts to retrospectively ascribe clinical and additional relevance to a number of taxa whose significance was inconclusive in previous Journal of Clinical Microbiology compendia (1, 11, 30, 31). Findings that warrant emphasis are discussed below.
TABLE 1
| Scientific name | Family | Sourcea | Clinical relevance | Growth characteristics | Reference(s) |
|---|---|---|---|---|---|
| Gram-positive cocci | |||||
| Arsenicicoccus cauae sp. nov. | Dermatophilaceae | Blood | Not established; isolated from 17-month-old male with fever, diarrhea, nonprojectile vomiting, and abdominal pain in Republic of Korea | Facultative, non-motile, catalase-positive, non-spore-forming Gram-positive coccus; 1.3 mm diameter yellow, creamy, circular, convex colonies on tryptic soy agar with 10% sheep blood; optimal growth at 37°C–40°C; nitrate reduction-, esculin-, urease-, alkaline phosphatase-positive; glucose-, indole-, tyrosine-, fucosidase-, β-galactosidase-negative | 24 |
| Staphylococcus taiwanensis sp. nov. | Staphyloco-ccaceae | Blood | Female patient with gastric cancer in Taiwan with accompanying episode of fever and chills | Facultative, non-motile, catalase-positive, oxidase-negative, coagulase-negative Gram-positive coccus; 2 mm diameter smooth, convex, hemolytic colonies on blood agar incubated at 37°C; bacitracin-resistant, novobiocin- and polymyxin B-susceptible; pyrrolidonyl arylamidase-, urease-, arginine dihydrolase-, D-ribose-positive; β-galactosidase-, nitrate reduction-, D-mannitol-, D-xylose-negative; resistant to oxacillin; susceptible to erythromycin, clindamycin, levofloxacin, vancomycin, tetracycline | 32 |
| Streptococcus ilei sp. nov. | Streptococcaceae | Ileostomy effluent (2) | Not established; isolated from male patient who underwent loop ileostomy in Republic of Korea due to rectal neuroendocrine tumors | Facultative, non-motile, catalase-negative Gram-positive coccus; 0.5–1 mm diameter raised, cream-colored, α-hemolytic colonies on Columbia agar supplemented with 5% sheep blood; optimal growth at 37°C; variable Lancefield A antisera reactions between the two isolates; glycerol-, D-melezitose-, D-mannitol-positive; D-cellobiose-, D-trehalose-, pyruvic acid-, D-trehalose-, alkaline phosphatase-negative | 33 b |
| Streptococcus toyakuensis sp. nov. | Streptoco- ccaceae | Blood | Not established; isolated from a male patient in Japan with bacteremia | Facultative, catalase-negative, non-spore-forming Gram-positive coccus; 0.3- to 0.8-mm diameter α-hemolytic colonies on trypticase soy agar supplemented with 5% sheep blood; optimal growth at 30-37°C; no Lancefield antigens demonstrated; 6-bromo-2-naphthyl-aD-galactopyranoside-, N-acetyl-β-glucosaminidase-positive; 2-naphthyl phosphate-, D-lactose-, D-trehalose-, D-raffinose-, alkaline phosphatase-, β-lactamase-negative; broth microdilution testing generated MIC values indicating resistance to benzylpenicillin, cefotaxime, imipenem, levofloxacin, azithromycin | 25 c |
| Gram-positive bacilli | |||||
| Corynebacterium parakroppenstedtii sp. nov. | Corynebacteriaceae | Breast (23) | Purulent material, tissue, puncture fluid, secretions from patients with mastitis, granulomatous lobar mastitis, and suppurative mastitis in China | Non-motile, non-spore-forming, coryneform, lipophilic, catalase-positive Gram-positive bacillus; <1 mm diameter non-hemolytic, gray, smooth, circular colonies on Columbia blood agar at 35°C; pyrazinamidase-, glucose-positive; nitrate reduction-, urease-, alkaline phosphatase-, sucrose-, ribose-, xylose-negative; 56% of isolates utilize esculin; 82% of strains resistant to erythromycin, clindamycin; all strains susceptible to vancomycin, penicillin, cefepime | 34 c |
| Corynebacterium pseudokroppenstedtii sp. nov. | Corynebacteriaceae | Breast (4) | Purulent material, tissue, puncture fluid, secretions from patients with mastitis, granulomatous lobar mastitis, and suppurative mastitis in China | Non-motile, non-spore-forming, coryneform, lipophilic, catalase-positive Gram-positive bacillus; <1 mm diameter non-hemolytic, grayish, smooth, circular, convex colonies on Columbia blood agar at 35°C; pyrazinamidase-, glucose-positive; nitrate reduction-, urease-, alkaline phosphatase-, sucrose-, ribose-, xylose-negative; 100% of isolates utilize esculin; all strains resistant to erythromycin, clindamycin, ciprofloxacin, levofloxacin; all strains susceptible to penicillin, vancomycin, cefepime | 34 c |
| Gulosibacter hominis sp. nov. | Microbacteriaceae | Ear (3), one of which was reported as middle ear | Isolated from ear sample or ear swabs of patients in Switzerland reported to have ear infection | Aerobic, non-motile, catalase-positive, oxidase-negative Gram-positive bacillus; 1 mm diameter non-pigmented, low convex, round, non-hemolytic colonies on Columbia sheep blood agar; optimal growth at 28°C; frequent inter-isolate biochemical variability; common positive reactions for alanine arylamidase, growth at 40°C, growth in brain heart infusion (BHI) broth at pH 6; common negative reactions for nitrate reduction, acid phosphatase, growth on L-tyrosine, growth on Tween 60 agar; decreased MIC values reported for amoxicillin-clavulanic acid, cefuroxime; increased MIC values reported for trimethoprim-sulfamethoxazole; one isolate had reported MIC values of >256 mg/L for erythromycin, clindamycin | 35 b |
| Nocardia sputi sp. nov. | Nocardiaceae | Sputum (2) | Not established; isolated from two patients with pulmonary infections in China | Aerobic, non-motile, catalase-positive, oxidase-negative Gram-positive actinomycete; convex, rough, dry, white colonies with irregular edges on BHI-5% sheep blood agar; optimal growth at 35°C; poor growth on chocolate agar or BHI agar; no growth at 45°C; D-fructose-positive; trypsin-, cellobiose-, D-glucose- D-xylose-negative; susceptible to amikacin, clarithromycin, trimethoprim-sulfamethoxazole; decreased susceptibility to ciprofloxacin, amoxicillin-clavulanic acid, minocycline | 36 |
| Pseudoclavibacter triregionum sp. nov. | Microbacteriaceae | Blood | Not established; isolated from pediatric patient in Switzerland | Aerobic, non-motile, catalase-positive, oxidase-negative Gram-positive bacillus; 1 mm diameter white, low convex, round, non-hemolytic colonies on Columbia sheep blood agar; optimal growth at 28°C; positive reactions for growth at 37°C, 40°C, 45°C; negative reactions for growth in 5% NaCl, pyrrolidonyl arylamidase, alkaline phosphatase, leucine arylamidase, leucyl glycine arylamidase; increased MIC values reported for trimethoprim-sulfamethoxazole, gentamicin | 26 d |
| Gram-negative bacilli | |||||
| Burkholderia orbicola sp. nov. | Burkholderi-aceae | Thirty isolates discussed in publication, including pharyngeal exudate (2), sputum (16), blood (1) | Several implicated in cystic fibrosis, pneumonia, cepacia syndrome; clinical isolates recovered in Mexico, United States, Australia, Belgium, Canada | Aerobic, motile Gram-negative bacillus; 1- to 3 mm diameter circular, convex, opaque, creamy, non-pigmented colonies on tryptic soy agar incubated at 30-42°C; growth on MacConkey agar; majority of isolates assimilate D-maltose, D-mannitol, D-mannose, D-sorbitol, malonate; majority of strains possess β-N-acetyl-glucosaminidase, gamma-glutamyl-transferase, phosphatase; resistant to cefotaxime, ceftriaxone, cefepime, amikacin; susceptible to trimethoprim-sulfamethoxazole, meropenem | 37 d |
| Franklinella schreckenbergeri gen. nov., sp. nov. | Comamonadaceae | Skin and soft tissue (2), dialysis liquid archival isolates at Canadian reference laboratory | One skin and soft tissue isolate derived from cellulitis; isolates have been characterized as CDC group NO-1-like organisms | Aerobic, non-motile, oxidase-negative, catalase-positive, non-spore-forming Gram-negative bacillus, some with vacuoles or beading; 1- to 4 mm diameter gray-white or yellowish colonies on sheep blood agar; optimal growth at 35°C; no growth on MacConkey agar; triple sugar iron agar reaction of K/no change; nitrate reduction-positive; xylose-, mannitol-, maltose-, fructose-negative; susceptibility to most antimicrobial agents | 38, 39 |
| Leclercia pneumoniae sp. nov. | Enterobact-eriaceae | Tracheal secretions and blood | Isolated from infant with pneumonia and septicemia in Germany | Facultative Gram-negative bacillus; 2- to 3 mm diameter, circular, convex, smooth, gray colonies on Columbia blood agar; optimal growth at 30-40°C; sucrose-, urease-, ornithine-, lysine-, arginine-, mannitol-negative; glucose-, indole-, maltose-, β-galactosidase-, trehalose-positive; susceptible to ciprofloxacin, imipenem, piperacillin, ceftazidime | 40 |
| Pseudomonas paraeruginosa sp. nov. | Pseudomonadaceae | Archival isolate from outer ear infection was subject to ancillary phenotypic characterization | Not established; genome sequences of ~35 isolates were characterized | Aerobic, motile (via swimming motility) Gram-negative bacillus; growth range 15-42°C; pyoverdine, pyocyanin production; casein hydrolysis-, gelatinase-, elastase-, arginine dihydrolase-positive; best differentiated from Pseudomonas aeruginosa via genotypic methods; susceptible to tobramycin, piperacillin, meropenem; less virulent than P. aeruginosa due to lack of twitching motility (41) | 42 |
| Spodiobacter cordis gen. nov., sp. nov. | Flavobacteriaceae | Blood (2) | Isolated from patients with infective endocarditis in Japan; phenotypic data presented in (43) | Aerobic, non-motile, oxidase-positive, catalase-negative, non-spore-forming Gram-negative bacillus; 1.5- to 2 mm diameter convex, circular colonies on tryptic soy agar; optimal growth at 37°C; enhanced growth observed in CO2-enriched atmosphere; no growth on MacConkey agar; nitrate reduction-, trypsin-, cystine arylamidase-positive; urease-, indole-, arginine dihydrolase-, gelatin-, α-chymotrypsin-, α-glucosidase-negative reportedly susceptible to ampicillin, piperacillin, cefotaxime, ceftazidime, aztreonam, minocycline, carbapenem agents | 44 b |
| Vandammella animalimorsus gen. nov., sp. nov. | Comamonadaceae | Skin and soft tissue (7), peritoneal dialysate archival isolates at Canadian reference laboratory | Skin and soft tissue isolate derived from deep wound (1); animal bite wounds (4); isolates were previously characterized as CDC group NO-1 (45) | Aerobic, non-motile, oxidase-variable, catalase-positive, non-spore-forming Gram-negative bacillus, some with vacuoles or bipolar staining; 0.5- to 1 mm diameter gray-white or yellowish colonies on sheep blood agar; optimal growth at 35°C; no growth on MacConkey agar; triple sugar iron agar reaction of K/no change; nitrate reduction-variable; xylose-, mannitol-, maltose-, fructose-negative; susceptibility to most antimicrobial agents; isolate-specific decreased susceptibility to aztreonam, ceftazidime | 38 |
| Vibrio paracholerae sp. nov. | Vibrionaceae | Twenty-three total isolates, including 12 from clinical sources; archival isolates date back over 100 y (46) | Majority of isolates from United States surveillance collection; three diarrheal isolates derived from patients in Thailand and Mozambique | Motile-, oxidase-positive, curved Gram-negative bacillus; creamy-white, circular colonies isolated on tryptic soy agar, yellow colonies observed on thiosulfate citrate bile salts sucrose agar; growth observed at 30°C; tolerates up to 6% NaCl; α-cyclodextrin-, pectin-, acetoin-positive; monomethyl succinate-, N-acetyl-D-galactosamine-, D-glucuronic acid-negative; 60% of strains possess β-lactamase | 47 b |
| Gram-positive anaerobe | |||||
| Peptoniphilus nemausensis sp. nov. | Peptoniphilaceae | Periprosthetic fluid (1), tissue (4) | Surgical site infection of patient in France following revision of a total hip prosthesis | Bligately anaerobic, non-motile, catalase-negative, non-spore-forming Gram-positive coccus; 1 mm diameter grayish, circular, entire, opaque, umbonate, non-hemolytic colonies on blood agar; resistant to colistin; susceptible to vancomycin, kanamycin; esculin hydrolysis-, proline arylamidase-positive; urease-, gelatinase-, indole-, nitrate reductase-, leucine arylamidase-negative; reported susceptibility to penicillin, imipenem, clindamycin, tetracycline, metronidazole; reported resistance to levofloxacin, ciprofloxacin | 48 b |
a
Number of isolates from clinical source is 1, except where shown in parentheses.
b
Taxonomic designation subsequently accepted in Validation List no. 203 (49).
c
Taxonomic designation subsequently accepted in Validation List no. 207 (50).
d
Taxonomic designation subsequently accepted in Validation List no. 206 (51).
TABLE 2
| Former name | Revised name | Other information | Reference(s) |
|---|---|---|---|
| Gram-positive bacilli | |||
| Bacillus clausii | Shouchella clausii comb. nov. | Initial description of the former B. clausii found in (52) and accepted (53); synonym designation of Alkihalophilus clausii found in (54); case report of bacteremia with the former B. clausii following probiotic use found in (55) | (56)a |
| Bacillus dielmonensis | Neobacillus dielmonensis comb. nov. | Initial description of the former B. dielmonensis found in (57); isolated from skin of healthy female | (58) |
| Bacillus pseudofirmus | Alkalihalophilus pseudofirmus comb. nov. | Initial description of the former B. pseudofirmus found in (52) and accepted (53); isolated from endometrial lavage cultures of patients with endometrial hyperplasia or endometrial cancer (59) | (56)a |
| Streptacidiphilus bronchialis | Peterkaempfera bronchialis comb. nov. | Initial description of the former S. bronchialis found in (11, 60); isolated from bronchial lavage specimen | (61) |
| Gram-negative bacilli | |||
| Kalamiella piersonii | Pantoea piersonii sp. nov. | Initial description of the former K. piersonii found in (62) and accepted (63); reports of infection and multi-drug resistance with the former K. piersonii described in (64, 65) | (66)b |
| Pseudomonas nosocomialis | Stutzerimonas nosocomialis comb. nov. | Initial description of the former P. nosocomialis from clinical specimens found in (11, 67) | (68)c |
| Gram-negative anaerobes | |||
| Fusobacterium nucleatum subsp. animalis | Fusobacterium animalis sp. nov. | Initial subspecies designation of the former F. nucleatum subsp. animalis found in (69); organism has been isolated from subgingival plaque (70); revision reflects elevation of rank to species | (71)d |
| Fusobacterium nucleatum subsp. vincentii | Fusobacterium vincentii sp. nov. | Initial subspecies designation of the former F. nucleatum subsp. vincentii found in (72); organism originally isolated from Vincent’s angina and necrotizing ulcerative gingivitis; revision reflects elevation of rank to species | (71)d |
| Pusillimonas faecalis | Pusillibacter faecalis gen. nov., sp. nov. | Initial description of the former Pusillimonas faecalis found in (31, 73); revision necessary due to duplication of a previously-published genus epithet | (74) |
a
Taxonomic designation subsequently accepted in Validation List no. 203 (49).
b
Taxonomic designation subsequently accepted in Validation List no. 206 (51).
c
Taxonomic designation subsequently accepted in Validation List no. 208 (75).
d
Taxonomic designation subsequently accepted in Validation List no. 204 (76).
TABLE 3
| Taxon | JCM Compendium | Human source initially reported | Clinical/applied science update (example) | Reference |
|---|---|---|---|---|
| Alloprevotella rava | 2017 | Subgingival plaque | Osteomyelitis of jaw; four other organisms isolated from tissue specimens | (77) |
| Porphyromonas pasteri | 2017 | Saliva | Increased abundance in cystic fibrosis patients experiencing long-term lung function decline | (78) |
| Butyricimonas faecihominis | 2017 | Feces | Co-bacteremia with Eubacterium callanderi in post-appendicular peritonitis | (79) |
| Vogesella urethralis | 2023 | Urine | Fatal aspiration pneumonia and bacteremia | (80) |
| Pseudocitrobacter vendiensis | 2023 | Perineal swab | Multiple bloodstream infections in patients on hemodialysis unit; carbapenem resistance | (81) |
| Pandoraea nosoerga | 2023 | Not specified | Fatal pneumonia and bacteremia in cystic fibrosis patient post-liver/lung transplant | (82) |
a
These references reflect what is in Table 1.
Novel taxa
Among the novel Gram-positive cocci that were described in 2022, three have been isolated from the blood of patients. Arsenicicoccus cauae sp. nov. was recovered from the blood of a febrile child with gastroenteritis (24). It is not clear if this organism was responsible for the gastrointestinal symptoms or was merely recovered due to gut translocation. Arsenicicoccus spp. have acquired their name from their ability to reduce arsenic. The other three species designations in this genus, namely, bolidensis, dermatophilus, and piscis, have been recovered primarily from the environment (soil) and have caused disease in fish and flamingos (24).
Staphylococcus taiwanensis sp. nov. (32) was recovered from a patient with cancer who presented with fever and chills. MALDI-TOF MS using a commercial system failed to identify the organism. Genome sequence analysis revealed that the isolate carried the staphylococcal cassette chromosome determinants mec and mecA. Phenotypic susceptibility testing on an automated instrument confirmed resistance to oxacillin [minimum inhibitory concentration (MIC) ≥ 4 µg/mL] and susceptibility to a variety of other agents as listed in Table 1.
Two novel Streptococcus spp. were also characterized. Streptococcus toyakuensis sp. nov. was recovered from a blood culture of a Japanese man with bacteremia with no obvious source of infection (25). This novel alpha-hemolytic Streptococcus is noteworthy for its multi-drug resistance. Phenotypic susceptibility testing on a commercial platform demonstrated resistance to β-lactams, macrolides, and quinolones—similar to some strains of the Streptococcus mitis group to which S. toyakuensis sp. nov. is closely related (25). Acquired resistance genes were sought by whole genome sequencing using ResFinder v4.1. Macrolide resistance was determined by the presence of mef(A) and mrs(D). Macrolide-lincosamide-streptogramin B resistance and tetracycline resistance likewise were caused by the presence of ermB and tet(M), respectively, whereas quinolone and β-lactam resistance genes were not detected (25). With respect to the observed quinolone resistance, amino acid sequencing revealed that serine residues at position 81 of GyrA and position 79 of ParC (important to quinolone resistance in alpha-hemolytic streptococci) were replaced by tyrosine and isoleucine, respectively. As is the case for the S. mitis group and other streptococci, S. toyakuensis sp. nov. is β-lactamase negative and β-lactam resistance was mediated by amino acid substitutions in penicillin-binding proteins (PBPs), namely, PBP1a, PBP1b, PBP2b, and PBP2x (25).
In the manuscript by Hyun et al. (33), the authors characterized two isolates of alpha-hemolytic Gram-positive cocci recovered from ileostomy effluent of a man from the Republic of Korea and determined that the organism was unique enough from other viridans group streptococci to be classified as its own species, which they named Streptococcus ilei sp. nov. In addition, the authors determined that this organism is found in the microbiome of numerous human body compartments with highest abundance in the oral cavity. Although it appears to be a component of the human microbiome, pathogenicity assessment (including genomics, animal studies, and assessment of cytotoxicity in various human cell lines) established this organism as a potential human pathogen (33).
Lipophilic Corynebacterium spp., most notably Corynebacterium kroppenstedtii, play a significant role in granulomatous and suppurative mastitis in women (83, 84). Luo et al. (34) set out to characterize 27 C. kroppenstedtii-like organisms recovered from women presenting with mastitis at their institution over a 3-year period. The authors’ comprehensive investigation included phenotypic characterization, MALDI-TOF MS identification, partial 16S rRNA analysis, rpoB and fusA sequencing, and whole genome sequencing. Their characterization identified two distinct genomospecies which they subsequently named C. parakroppenstedtii sp. nov. and C. pseudokroppenstedtii sp. nov. Most of the organisms from the 27 cases were recovered in pure growth. Thirteen patients had tissue available for histologic analysis; 12 of them had granulomatous mastitis and 1 had supportive mastitis (34).
In the study by Vandamme et al. (35) that characterized three irregular Gram-positive bacilli isolated from ear samples of patients with ear infections, the authors determined the organisms to be most closely related to members of the Gulosibacter genus. They named the new strains Gulosibacter hominis sp. nov. Gulosibacter spp. are frequently recovered from the environment and, until this publication, were not believed to be part of the normal human microbiota. In the paper from Vandamme and colleagues, the authors noted that multiple 16S rRNA gene fragments of uncultivated bacteria in three human skin microbiome studies were >99.5% identical to the novel Gulosibacter spp. recovered from their patients, suggesting that G. hominis sp. nov. may be a member of the human skin microbiome. In support of this assertion is the observation that G. hominis sp. nov. lacks both resistance determinants and virulence factors, thereby suggesting a non-pathogenic role or, at most, the potential to cause only opportunistic infections (35).
Like Gulosibacter spp., Pseudoclavibacter spp. are members of the family Microbacteriaceae and are plump, short Gram-positive bacilli. A novel species of Pseudoclavibacter, designated as Pseudoclavibacter triregionum sp. nov. (referring to the frontier regions of France, Germany, and Switzerland), was recovered from the blood of a child, but its significance in causing disease is unclear (26). P. triregionum sp. nov. has distinct phenotypic characteristics compared with other species in the genus. It demonstrates growth at 45°C and has poor biochemical reactivity (Table 1). Like the novel G. hominis sp. nov. described above by the same authors, P. triregionum sp. nov. generates a distinct spectrum by MALDI-TOF MS analysis. Once these spectra are added to commercial databases, this taxon will be readily identified by clinical laboratories to the species level affording a greater opportunity to learn more about its clinical significance.
The third novel Gram-positive bacillus to be isolated from human clinical material is Nocardia sputi sp. nov. recovered from two patients in China with pulmonary infections (36). This new species is most closely related to Nocardia beijingensis and Nocardia araoensis, the latter species of which was also isolated from a respiratory sample. Phenotypic characteristics of N. sputi sp. nov. are listed in Table 1. Similar to other Nocardia spp., N. sputi sp. nov. isolates were susceptible to trimethoprim-sulfamethoxazole but displayed intermediate resistance to amoxicillin-clavulanic acid, ciprofloxacin, and minocycline.
In a review of novel Gram-negative bacillus taxa, five new genus designations were established and accepted, namely, Franklinella (38), Huaxiibacter (85), Sandaracinobacteroides (86), Spodiobacter (43, 44), and Vandammella (38). Bernard et al. performed 16S rRNA and whole genome sequencing on 11 isolates within a Gram-negative bacillus reference collection that were derived from human sources, including dialysates and bite wound infection. Isolates provisionally classified as CDC group NO-1 (non-oxidizer) organisms were granted the taxonomic designation Vandammella animalimorsus gen. nov., sp. nov., while CDC group NO-1-like organisms were named Franklinella schreckenbergeri gen. nov., sp. nov. (38). The two taxa are rather similar phenotypically, with the potential exception of oxidase and nitrate reduction reactions for V. animalimorsus gen. nov., sp. nov. Genomes from F. schreckenbergeri gen. nov., sp. nov. were noted to be smaller than those from V. animalimorsus gen. nov., sp. nov. Both organisms have been observed in canine and feline oral microbiomes.
Spodiobacter cordis gen. nov., sp. nov. was isolated from blood cultures of two patients in Japan afflicted with infective endocarditis at separate hospitals (43). This taxon was phylogenetically differentiated from the Bergeyella-Chryseobacterium-Riemerella branch of the family Flavobacteriaceae. Both isolates were reportedly resistant to fosfomycin, gentamicin, amikacin, ciprofloxacin, and levofloxacin via a broth microdilution procedure; interpretive criteria were not presented. Huaxiibacter chinensis gen. nov., sp. nov. (85) was recovered from a patient in China who was being managed for pneumonia. This novel member of the Enterobacteriaceae family (87) was initially identified as Enterobacter cloacae complex by an automated identification system (including positive arginine dihydrolase and ornithine decarboxylase reactions) but was subsequently demonstrated to be β-galactosidase and Voges-Proskauer negative. Broth microdilution susceptibility data revealed elevated MIC values for aztreonam, third- and fourth-generation cephem agents, and carbapenems. Unfortunately, no additional data were presented either for the clinical status of the patient or for the abundance or predominance of the isolate in the context of normal respiratory flora.
Another novel taxon within Enterobacteriaceae, Leclercia pneumoniae sp. nov., was initially isolated from endotracheal secretions and blood of a newborn in Germany who developed pneumonia during hospitalization (40). The isolate exhibited reduced MIC values to agents in several antimicrobial (sub)classes, including penicillins, carbapenems, fluoroquinolones, cephems, tetracyclines, and aminoglycosides. No data on clinical course were provided. L. pneumoniae sp. nov. can be phenotypically differentiated from Leclercia adecarboxylata by its inability to utilize mannitol and sucrose.
Two papers discuss a pair of oxidase-positive, non-glucose-fermentative Gram-negative bacillus taxa that emanated from a previous designation. The taxon Burkholderia orbicola sp. nov. (37) has been established to replace the non-validly published designation “Burkholderia servocepacia” (88). The genesis of the (former) species name was the observation that these bacterial strains exhibited beneficial biocontrol properties (L. “servo,” to watch over). However, further study revealed that isolates derived from pharyngeal exudate, blood, and sputum contribute to opportunistic infection in the context of cystic fibrosis, cepacia syndrome, and pneumonia. Rudra et al. (42) performed comprehensive phylogenetic studies on 212 Pseudomonas aeruginosa genomic sequences and determined that approximately 30% comprised an outlier clade, constituting a novel species. Such sequences were associated with novel taxon Pseudomonas paraeruginosa sp. nov. Two reference archive isolates consistent with the outlier clade (one of which was associated with outer ear infection) were purchased and cultivated for phenotypic characterization. In general, P. paraeruginosa sp. nov. was best differentiated from P. aeruginosa by genotypic methods, though it was posited that P. paraeruginosa was generally less virulent.
Finally, the designation of Vibrio paracholerae sp. nov. (47) stemmed from diversity analysis of Vibrio cholerae strains in native aquatic environments in Bangladesh and the United States east coast. A cluster of related lineages was documented at high abundance in Bangladesh, while absent in United States waters, and was demonstrated to be distinct from V. cholerae. Retrospective and historic analysis subsequently revealed that such V. paracholerae sp. nov. isolates have been associated with septicemia and diarrhea in multiple regions of the world (including the United States) and have circulated with pandemic V. cholerae strains for several decades.
To begin a discussion on novel anaerobic prokaryotic taxa, we will focus on two publications. A report from Hitch et al. (89) describes a total of 28 novel taxa [ultimately accepted by two IJSEM Validation Lists (76, 90)] that were derived from human gastrointestinal isolates with uncertain clinical significance archived in multiple collections (91, 92). The primary focus of the study was to assess functionality of a bioinformatic tool capable of computing elements necessary for a unique microbial protologue, i.e., a standardized format for describing a novel taxon in a clear and concise manner (93). Hitch et al. selected a combined 16S rRNA gene sequence- and metagenomic-based approach for this analysis, in part, because culture isolates were not deposited in some instances. In addition, the authors posited that protologue generation via conventional means can be time-consuming and that bioinformatic characterization can allow for a more harmonized presentation of taxon traits. As a result, we are unable to present phenotypic characterization of these 28 taxa, including Gram reaction. However, within Table S1, categorization by Gram reaction was attempted for half of these taxa because they possess genus designations which have additional species-level members for which in-depth phenotypic characterizations have been published in peer-reviewed literature [one example being Agathobaculum butyriciproducens Gram reaction and atmospheric requirements (94) that could serve as an analog for baseline traits that may be associated with Agathobaculum ammoniilyticum sp. nov. published by Hatch et al. (89)].
The 14 other novel taxa from this publication were of novel genus designation, meaning that no comparator organisms were available for Table S1 categorization. It should be noted that family designations, though available for these novel taxa, were non-contributory to Table S1 assignment. For example, families Lachnospiraceae and Oscillospiraceae are known to house both Gram-positive and Gram-negative organisms [references (95, 96) and (94, 97) provided as examples for the respective families]. As a result, an additional category was created within Table S1 for novel anaerobic genera for which a Gram reaction is unknown.
Liu et al. (98) published 44 novel anaerobic taxa of unknown clinical significance in a 2021 report that were accepted by ISJEM Validation List no. 205 (90). Each genus/species designation was accompanied by phenotypic characterizations but without Gram stain reaction. In a similar fashion to that described previously, additional species members within a listed genus were researched in order to predict Gram reaction and growth environment. A total of 19 and 15 designations are thus presented in the Gram-positive anaerobe and Gram-negative anaerobe categories of Table S1, respectively. The remaining 10 gen. nov. designations were then placed into the additional anaerobic category.
Greater than 85% of presented anaerobic taxa in our report were not characterized by Gram reaction. Of the remaining 11 taxa (four Gram positive, seven Gram negative), only one appears to have clinical significance at this time. Peptoniphilus nemausensis sp. nov. (48) is an anaerobic Gram-positive coccus that was isolated from four periprosthetic tissue specimens and one periprosthetic fluid specimen in the context of surgical site infection. A previous report (99) noted that a French patient underwent revision of a total hip prosthesis, with admission to a rehabilitation center 1 week later. Approximately 1 month after admission, infection was suspected and the bacterium was cultivated from the aforementioned specimens, but not from three bone specimens. No other microbes were isolated from these specimens. Initial susceptibility testing revealed low MIC values for imipenem, rifampin, amoxicillin, amoxicillin-clavulanic acid, metronidazole, and clindamycin. The patient achieved favorable outcome following a 3-month regimen of clindamycin and rifampin.
Taxonomic revisions
As mentioned in the last iteration of the taxonomy updates published in early 2022, the genus Bacillus has undergone division into several novel genera based upon extensive phylogenetic studies (31, 54). Six new genera were added to a growing list in 2020—Peribacillus gen nov., Cytobacillus gen. nov., Mesobacillus gen. nov., Neobacillus gen. nov., Metabacillus gen. nov., and Alkalihalobacillus gen. nov. As more studies and novel organisms are discovered, changes within the existing genera and the addition of new ones continue to occur as outlined in Table 2. Bacillus clausii has been recovered from several patients with bacteremia following probiotic use, and in all cases, the patients were quite symptomatic. All patients were either immunocompromised or had significant co-morbidities (55). In 2020, this organism was reclassified as Alkalihalobacillus clausii (54) and most recently has been incorporated into a novel genus as Shouchella clausii comb nov. when additional phylogenetic studies determined that the genus Alkalihalobacillus required reclassification (56). In total, 11 species of Alkalihalobacillus were transferred to Shoucella gen. nov. (56). The other former Bacillus spp. in Table 2, Neobacillus dielmonensis comb. nov. and Alkalihalophilus pseudofirmus comb. nov., were recovered during studies of the microbiome of skin and endometrium of patients with cancer, respectively (57, 59). Their contributions to disease require additional studies.
Streptacidophilus spp. are aerobic actinomycetes closely related to Streptomyces spp. and, like Streptomyces spp., are frequently found in soil. Streptacidiphilus bronchialis was originally recovered from a bronchoalveolar lavage fluid from an elderly man (60). In 2022, Madhaiyan et al. (61) used genome sequence-derived tools to further elucidate taxa of the family Streptomycetaceae. This led to the creation of several novel genera, including Peterkaempfera gen. nov. to which Strepacidiphilus griseoplanus and Strepacidiphilus bronchialis were reassigned (61).
Taxonomic revisions to selected Gram-negative organisms merit additional discussion. The former Kalamiella piersonii, documented genotypically and phenotypically as a multi-drug resistant bacterium (64, 65), is now named Pantoea piersonii sp. nov. (66). Gomila et al. (68) constructed a core-genome phylogeny of 200 strains in the recently proposed Stutzerimonas genus (76, 100) to corroborate the revised taxonomy of Pseudomonas nosocomialis to Stutzerimonas nosocomialis comb. nov. However, this validly published designation currently holds a taxonomic status of orphaned species (https://lpsn.dsmz.de/). Orphaned species can be defined as a status used for names whose currently assigned parent taxon is not regarded as the correct name. Such species names are conditionally illegitimate per Rule 51a of the International Code of Nomenclature of Prokaryotes. In this instance, the genus name is regarded as a synonym of another genus name and a new combination has not yet been proposed (https://lpsn.dsmz.de; M. Göker, personal communication). A 2017 publication from Kook et al. (71) proposed the elevation of four subspecies of Fusobacterium nucleatum (i.e., subspecies animalis, subspecies nucleatum, subspecies polymorphum, and subspecies vincentii) to species designations. Two of these rank elevations (Fusobacterium animalis sp. nov., Fusobacterium vincentii sp. nov.) were accepted in 2022 per IJSEM Validation List no. 204 (76).
Recently ascribed and additional clinical significance
Lastly, as in previous editions of this compendium (11, 30, 31), we provide literature updates for selected organisms for which clinical relevance was initially deemed to be not established. Three anaerobic organisms warrant additional discussion. Ulger Toprak et al. (77) reported first-time recovery of Alloprevotella rava from defective bone and surrounding tissue in the context of chronic mandibular osteomyelitis. Potential clinical significance should be viewed in light of concomitant recovery of Veillonella parvula, Prevotella nigrescens, Klebsiella oxytoca, and Corynebacterium durum from the same specimen. The Gram-negative bacillus Porphyromonas pasteri was targeted in a study (78) investigating the potential role for anaerobic bacteria in long-term lung function decline in cystic fibrosis patients. In a prospective cohort of 70 adults followed over an 8-year period, amongst anaerobic bacteria present in a sputum microbiome, P. pasteri and Prevotella nanceiensis were associated with annual decreases of forced expiratory volume approximating 52.3 mL/year and 67.9 mL/year, respectively. An initial report of bloodstream infection caused by Butyricimonas faecihominis in the context of a perforated appendix was published by Kamel et al. (79). This Gram-negative bacillus was isolated from two sets of blood cultures, while the anaerobic Gram-positive bacillus Eubacterium callanderi was isolated from a single set. The B. faecihominis was interpreted as resistant to penicillin and clindamycin per EUCAST v8.0 breakpoints for Gram-positive and Gram-negative anaerobes. Treatment with amoxicillin-clavulanic acid rendered a favorable outcome.
Vogesella urethralis was first reported from a human clinical urine specimen in 2020 (101). Since that time, Matsuda et al. (80) documented this Gram-negative bacillus causing aspiration pneumonia and bacteremia. An 82-year-old patient with past medical history significant for chronic renal failure, emphysema, and chronic pulmonary aspergillosis was admitted for dyspnea on exertion and increased sputum production. Thoracic CT revealed new infiltrative and ground glass opacities in bilateral lung bases. Both V. urethralis and Klebsiella oxytoca were recovered from baseline sputum culture, though V. urethalis was reported as the predominant organism. V. urethralis was additionally recovered from two sets of blood cultures performed upon admission. Aspiration pneumonia re-developed on hospital day 15 despite piperacillin-tazobactam therapy, and the patient expired on day 18.
Nine cases of Pseudocitrobacter vendiensis bacteremia were reported from a single hemodialysis unit in Brazil over a 9-month interval (81). All isolates harbored a plasmid-mediated IMP-1 metallo-β-lactamase [phenotypic resistance to ampicillin, cefepime, ceftazidime, ceftriaxone, chloramphenicol, and trimethoprim-sulfamethoxazole, as well as meropenem, imipenem, and ertapenem (all carbapenem MIC > 32 µg/mL)] and were initially identified as either Enterobacter cloacae or Pantoea spp. by a commercial identification system. Patients were successfully treated with amikacin.
Peyclit et al. (82) provided a case report of a 26-year-old female cystic fibrosis patient who succumbed to a highly resistant Pandoraea nosoerga bacteremic pneumonia following a liver-lung transplant. Both the patient and her brother, also suffering from cystic fibrosis, were colonized with P. nosoerga prior to transplantation. Despite pre-transplantation perioperative antimicrobial prophylaxis of piperacillin-tazobactam and tigecycline, left lung ischemia and septic shock were noted on day 5 post-transplant. Combination meropenem and tigecycline brought about an initial good response. However, a second septic shock episode followed on day 14 post-transplant, prompting a regimen of doxycycline, rifampicin, risperidone, and daily chlorhexidine bathing. Following expiration at day 25, whole genome sequencing determined that clinical deterioration of the patient was caused by a pre-transplantation P. nosoerga strain that was shared with her brother.
CONCLUSION
Despite an increasing number of reports in the literature, some of which are accepted by IJSEM, that provide limited phenotypic characterizations relative to novel taxon designations, the Journal of Clinical Microbiology remains steadfast in providing summaries of microbial revisions to bench-level, supervisory-level, and doctoral-level medical microbiologists. Like it or not (102, 103), taxonomic and nomenclature changes are going to continue to inundate our discipline and culture due, in part, to advances in phylogenetic, microbiome, and diagnostic sciences. Clinical and Laboratory Standards Institute is poised to officially release the M64 guideline in early 2024, designed to serve as a resource for clinical and veterinary microbiology laboratories in the implementation of taxonomy nomenclature changes into routine clinical practice.
ACKNOWLEDGMENTS
This report was not subject to influence from any funding agency in the public, commercial, or not-for-profit sectors.
SUPPLEMENTAL MATERIAL
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Information & Contributors
Information
Published In
Journal of Clinical Microbiology
Volume 61 • Number 11 • 21 November 2023
eLocator: e00838-23
Editor: Romney M. Humphries, Vanderbilt University Medical Center, Nashville, Tennessee, USA
PubMed: 37889007
Copyright
© 2023 American Society for Microbiology. All Rights Reserved.
History
Published online: 27 October 2023
Keywords
Contributors
Editor
Romney M. Humphries
Editor
Vanderbilt University Medical Center, Nashville, Tennessee, USA
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Citation
2023.
Valid and accepted novel bacterial taxa derived from human clinical specimens and taxonomic revisions published in 2022. J Clin Microbiol
61:e00838-23.
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