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Update on the Taxonomy of Clinically Important Anaerobic Bacteria
Korean J Clin Lab Sci 2022;54:239-248  
Published on December 31, 2022
Copyright © 2022 Korean Society for Clinical Laboratory Science.

Myungsook Kim

Department of Laboratory Medicine, Severance Hospital, Yonsei University College of Medicine, Seoul, Korea
Correspondence to: Myungsook Kim
Department of Laboratory Medicine, Severance Hospital, Yonsei University College of Medicine, 50-1 Yonsei-ro, Seodaemun-gu, Seoul 03722, Korea
E-mail: msvkim@yuhs.ac
ORCID: https://orcid.org/0000-0002-4933-5018
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
Abstract
The taxonomy of bacteria in the field of clinical microbiology is in a state of constant flux. A large-scale revamping of the classification and nomenclature of anaerobic bacteria has taken place over the past few decades, mainly due to advances in molecular techniques such as 16S rRNA and whole genome sequencing (WGS). New genera and species have been added, and existing genera and species have been reclassified or renamed. A major role of the clinical microbiological laboratories (CMLs) is the accurate identification (ID) and appropriate antimicrobial susceptibility testing (AST) for clinically important bacteria, and rapid reporting and communication of the same to the clinician. Taxonomic changes in anaerobic bacteria could potentially affect the choice of appropriate antimicrobial agents and the antimicrobial breakpoints to use. Furthermore, current taxonomy is important to prevent treatment failures of emerging pathogenic anaerobes with antimicrobial resistance. Therefore, CMLs should periodically update themselves on the changes in the taxonomy of anaerobic bacteria and suitably inform clinicians of these changes for optimum patient care. This article presents an update on the taxonomy of clinically important anaerobic bacteria, together with the previous names or synonyms. This taxonomy update can help guide antimicrobial therapy for anaerobic bacterial infections and prevent treatment failure and can be a useful tool for both CMLs and clinicians.
Keywords : Anaerobic bacteria, Taxonomic change, Update
INTRODUCTION

Anaerobic bacteria are considered as etiologic agents in a number of clinical diseases, including aspiration pneumonia, brain abscess, and intra-abdominal infections [1, 2]. As the number of immunocompromised patients has been increased, the clinical importance of anaerobic bacterial infections has been extended [3]. The development of molecular technologies including 16S rDNA sequencing and genome sequencing has led to major changes among taxonomy of anaerobic bacteria, as well as aerobic bacteria, in the fields of clinical microbiology [4, 5]. Taxonomic changes potentially affect interpretation of susceptibility testing and reporting for anaerobes, and tracking of new names is important to work toward better improvement of patient treatment and disease management [6]. The Clinical and Laboratory Standards Institute (CLSI) provides the performance standards for AST stated with changed taxonomy in their updated guidelines, such as Cutibacterium (formerly Propionibacterium) acnes and Clostridiodes (formely Clostridium) difficile [7]. According to CLSI guideline, clinical microbiological laboratory (CML) may not be necessary to perform the AST for all anaerobic bacteria isolated from culture, because their antimicrobial susceptibility patterns are often predictable. However, antimicrobial resistance in anaerobic infections has been associated with poor clinical outcome due to treatment failure. Recently, the importance of the treatment of C. difficile infection has increased in both hospitals and the community, as emerging pathogen with high virulence and resistance of fluoroquinolones [8]. Furthermore, CLSI has published the data of cumulative AST for anaerobes, relatively limited on anaerobic organisms in spite of the clinical importance in guiding empiric therapy. CMLs have problems on identification (ID) of new and unusual species, such as Actinotignum schaalii, a newly recognized uropathogen with resistance of trimethoprime-sulfamethoxazole and ciprofloxacin, and history of treatment failure [9]. This article presents update on taxonomy of clinically important anaerobic bacteria with previous names or synonyms. Current taxonomy is important to perform the accurate organism identification, and antimicrobial susceptibility testing in the aspect of emerging pathogens. The taxonomy update can help guide patient management and prevent treatment failures in both CMLs and clinicians.

MAIN ISSUE

1. Anaerobic Gram-positive cocci and other anaerobic cocci

The anaerobic gram-positive cocci (AGPC) are part of the commensal flora of humans and are also associated with a variety of human infections [10]. AGPC belongs to the Firmicutes phylum, and the taxonomy of AGPC has undergone extensive changes of new genera and species (Table 1). Most clinical isolates of AGPC were described in the genus of Peptococcus and Peptostreptococcus. In 1983, four Peptococcus species (P. asaccharolyticus, P, indolicus, P. prevotii and P. magnus) were transferred to the genus Peptostreptococcus leaving Peptococcus niger as the single species in the genus Peptococcus [11]. Since 1998, the genus Peptostreptococcus has been divided into several novel genera. Peptostreptococcus magnus and P. micros were transferred to two new genera, Finegoldia and Micromonas, respectively [12]. The genus Micromonas has more recently been replaced by Parvimonas [13]. For the remained peptostreptococci, three new genera were proposed; Peptoniphilus, Anaerococcus and Gallicola [14]. In addition, two novel genera have been proposed; Anaerosphaera, with the type species A. aminiphila, most closely related to species of the genus Peptoniphilus [15] and Murdochiella, with the type species M. asaccharolytica, most closely related to Parvimonas micra and Finegoldia magna [16]. Among the other AGPC, Streptococcus parvulus has been changed to the genus Atopobium, as A. parvulum [17]; Ruminococcus productus (formerly Peptostreptococcus productus) was reclassified in a new genus Blautia, as B. product [18].

Taxonomic changes of anaerobic gram-positive cocci isolated from humans

Phylum and genus Species or subspecies Previous name(s) or synonym References
Firmicutes
Anaerococcus* A. hydrogenalis Peptostreptococcus hydrogenalis [14]
A. lactolyticus Peptostreptococcus lactolyticus [14]
A. octavius Peptostreptococcus octavius [14]
A. prevotii Peptostreptococcus prevotii [14]
A. tetradius Peptostreptococcus tetradius [14]
A. vaginalis Peptostreptococcus vaginalis [14]
Anaerosphaera* A. aminiphila New species [15]
Atopobium* A. parvulum Streptococcus parvulus [17]
Blautia* B. producta Peptostreptococcus productus, Ruminococcus productus [18]
Finegoldia* F. magna Peptostreptococcus magnus [12]
Gallicola* G. barnesae Peptostreptococcus barnesae [14]
Murdochiella* M. asaccharolytica New species [16]
Parvimonas* P. micra Peptostreptococcus micros, Micromonas micros [12, 13]
Peptococcus P. niger [11]
Peptoniphilus* P. asaccharolyticus Peptostreptococcus asaccharolyticus [14]
P. harei Peptostreptococcus harei [14]
P. indolicus Peptostreptococcus indolicus [14]
P. ivorii Peptostreptococcus ivorii [14]
P. lacrimalis Peptostreptococcus lacrimalis [14]
Peptostreptococcus P. anaerobius [12]

*New genus.



The anaerobic gram-negative cocci (AGNC), including the genera Veillonella, Acidaminococcus, Megasphaera, Anaeroglobus, and Negativicoccus, which was the recently described, have been classified in a single family, the Acidaminococcaceae [19]. Of the genus of Veillonella, V. dispar, V. parvula and V. atypica, have so far been isolated from human flora. Currently, the species V. alcalescens was abolished [20].

2. Anaerobic Gram-positive rods

The anaerobic gram-positive rods (AGPR) are widely distributed among the phylum Actinobacteria and Firmicutes. More recently, taxonomic reclassification of AGPR has undergone changes of new genera within these two phyla (Table 2).

Taxonomic changes of anaerobic gram-positive rods isolated from humans

Phylum and genus Species or subspecies Previous name(s) or synonym References
Actinobacteria
Actinobaculum* A. massiliense Actinomyces massiliae [23]
A. suis Actinomyces suis [24]
Actinomyces A. johnsonii New species, A. naeslundii genospecies WVA 963 [21]
A. naeslundii A. naeslundii genospecies 1 [21]
A. oris New species, A. naeslundii genospecies 2 [21]
Actinotignum* A. sangunis New species [22]
A. schaalii Actinobaculum schaalii [22]
A. urinale Actinobaculum urinale [22]
Alloscardovia* A. omnicolens New species [26]
Bifidobacterium B. logum subspecies infantis New subspecies, B. infantis [28]
B. logum subspecies longum New subspecies, B. logum [28]
B. logum subspecies suis New subspecies, B. suis [28]
Collinsella* C. aerofaciens Eubacterium aerofaciens [29]
Cutibacterium* C. acnes Propionibacterium acnes [25]
C. avidum Propionibacterium avidum [25]
C. granulosum Propionibacterium granulosum [25]
C. humersii Propionibacterium humersii [25]
Paraeggerthella* P. hongkongenesis Eggerthella hongkongenesis [30]
Parascardovia* P. denticola Bifidobacterium denticolens [27]
Pseudopropionibacterium* P. propionicum Propionibacterium propionicum [25]
Scardovia* S. inopinata Bifidobacterium inopinatum [27]
Firmicutes
Anaerostipes* A. hadrus Eubacterium hadrum [32]
Atopobium A. minutus Lactobacillus minutus [17]
A. rimae Lactobacillus rimae [17]
Clostridioides* C. difficile Clostridium difficile [34]
Clostridium C. maximum Sarcina maxima [31]
C. moniliforme Eubacterium moniliforme [31]
C. tarantellae Eubacterium tarantellae [31]
C. ventriculi Sarcina ventriculi [31]
Dorea D. formicigenerans Eubacterium formicigenerans [33]
Eubacterium E. sulci Fusobacterium sulci [55]
Filifactor F. alocis Fusobacterium alocis [55]
Hathewaya* H. histolytica Clostridium histolyticum [31]
H. limosa Clostridium limosum [31]
H. proteolytica Clostridium proteolyticum [31]
Hungatella* H. hathewayi Clostridium hathewayi [37]
Paeniclostridium* P. sordellii Clostridium sordellii [36]
Paraclostridium* P. bifementans Clostridium bifementans [36]
Terrisporobacte* T. glycolicus Clostridium glycolicum [35]

*New genus.



1) Phylum Actinobacteria

The genera Actinomyces, Actinobaculum, Actinotignum, Mobiluncus, and Varibaculum belong to the family Actinomycetaceae. Important taxonomic reclassification has occurred within the genus Actinomyces, such that A. naeslundii has been reclassified within the genus Actinomyces, which is previously considered “A. naeslundii genospecies I”, and Actinomyces oris and A. johnsonii have been represented as novel species [21]. Actinobaculum schaalii and A. urinale of the genus Actinobaculum have been reclassified into the novel genus Actinotignum and Actinotignum sangunis has been described as a novel species [22]. Recently, Actinotignum schaalii is recognized as an uropathogen with resistance of antimicrobials, but other Actinotignum species are less associated with human infections [9]. Actinobaculum massiliense and A. suis (previously named Actinomyces massiliae and A. suis are remained in the genus Actinobaculum [23, 24].

The genus Propionibacterium contains bacteria isolated from human sources and dairy products. Recently, important taxonomic reclassification has occurred in the cutaneous species of the genus. P. acnes, P. granulosum, P. avidum, and P. humersii have been reclassified into the novel genus Cutibacterium. P. propionicum has been reclassified as Pseudopropio-nibacterium propionicum [25]. Bifidobacterium and the closely related genera Alloscardovia [26], Para-scardovia, and Scardovia [27] belong to the family Bifidobacteriaceae. There are currently 50 Bifido-bacterium species, of which 11 species have been isolated from the human gut and oral cavity. B. logum including the former species B. infantis and B. suis is reclassified as three subspecies [28].

The genus Atopobium was proposed for Lactobacillus minutus, Lactobacillus rimae and Streptococcus parvulus, reclassified as A. minutus, A. rimae and A. parvulum [17]. The genus Collinsella has been proposed for Eubacterium aerofaciens with one species, Collinsella aerofaciens [29]. Other genus Eggerthella includes E. lenta and E. sinensis, and E. hongkongenesis is now reclassified as the only member of the novel genus Paraeggerthella [30].

2) Phylum Firmicutes

The genus Lactobacillus belongs to the order Lacto-bacillales and family Lactobacillaceae. Although numerous others have been assigned to other genera, the phylogenetic relationship between the diverse species is complicated and poorly defined not yet.

The genus Eubacterium is phylogenetically diverse, and many Eubacterium species, which have been assigned to other genera, are now widely distributed within the phylum Firmicutes. Eubacterium moniliforme and E. tarantellae was reclassified to the genus Clostridium as C. moniliforme and C. tarantellae, and additionally Sarcina maxima and S. ventriculi was reclassified as Clostridium maximum and C. ventriculi [31]. The family Lachnospiraceae includes a number of former members of the genus Eubacterium. Eubacterium hadrum was reclassified as Anaerostipes hadrus, E. formicigenerans as Dorea formicigenerans [32, 33].

Among the genus Clostridium, Clostridium difficile and C. mangenotii were reclassified to the new genus Clostridioides, as Clostridioides difficile and Clostridioides mangenotii [34]. C. glycolicum was reclassified to the new genus Terrisporobacte, also changed to T. glycolicus [35]; C. bifementans, and C. sordellii were reclassified to the new genus Paraclostridium and Paeniclostridium, respectively [36]; C. hathewayi was reclassified to Hungatella hathewayi [37]; Clostridium histolyticum, C. limosum and C. proteolyticum were reclassified to the new genus Hathewaya as H. histolytica, H. limosa and H. proteolytica [31].

3. Anaerobic Gram-negative rods

Most of anaerobic gram-negative rods (AGNR) belong to the phylum Bacteroidetes, including the families Bacteroidaceae, Porphyromonadaceae, Prevotellaceae, and Rikenellaceae, and to the phylum Fusobacteria including the families Fusobacteiacea and Leptotri-chiaceae. The taxonomic changes have occurred within the phylum Bacteroidetes, especially those of the genus Bacteroides; new species have been described and some species have been transferred to other genera, since 2006 (Table 3).

Taxonomic changes of anaerobic gram-negative rods isolated from humans

Phylum and genus Species or subspecies Previous name(s) or synonym References
Bacteroidetes
Bacteroides B. fragilis group [38]
Parabacteroides P. chongii New species [44]
P. distasonis Bacteroides distasonis [41]
P. godonii New species [42]
P. goldsteinii Bacteroides goldsteinii [41]
P. johnsonii New species [43]
P. merdae Bacteroides merdae [41]
Porphyromonas P. asaccharolytica Bacteroides asaccharolyticus [40]
Bacteroides melaninogenica subspecies asaccharolytica [40]
P. endodontalis Bacteroides endodontalis [40]
P. gingivalis Bacteroides gingivalis [40]
P. pasteri New species [49]
P. pogonae New species [50]
Prevotella P. bivia Bacteroides bivius [39]
P. buccae Bacteroides buccae, Bacteroides ruminicola subspecies brevis [39]
Bacteroides capillus, Bacteroides pentosaceus
P. buccalis Bacteroides buccalis [39]
P. corporis Bacteroides corporis [39]
P. dentalis Mitsuokella dentalis, Hallella seregens [47]
P. denticola Bacteroides denticola [39]
P. disiens Bacteroides disiens [39]
P. heparinolytica Bacteroides heparinolyticus, related to B. fragilis group [39]
P. intermedia Bacteroides intermedius [39]
Bacteroides melaninogenica subspecies intermedius
P. micans New species [45]
P. loescheii Bacteroides loescheii [39]
P. melaninogenica Bacteroides melaninogenica [39]
Bacteroides melaninogenica subspecies melaninogenicus
P. nanceiensis New species [46]
P. oralis Bacteroides oralis [39]
P. oris Bacteroides oris, Bacteroides ruminicola subspecies brevis [39]
P. oulorum Bacteroides oulorum, Prevotella oulora [39]
P. veroalis Bacteroides veroalis [39]
P. zoogleoformans Bacteroides zoogleoformans, related to B. fragilis group [39]
Fusobacteria
Fusobacterium F. equinum New species [54]
F. nucleatum subspecies animalis [52]
F. nucleatum subspecies necleatum [52]
F. nucleatum subspecies polymorphum [52]
F. nucleatum subspecies vincentii Later synonym of F. nucleatum subspecies fusiform [52]
F. pseudoperiodonticum New species [56]
Dialister D. invisus New species [57]
D. pneumosintes Bacteroides pneumosintes [57]
Selenomonas* S. sputigena [58]
Proteobacteria
Bilophila* B. wadsworthia New species [60]
Sutterella* S. wadsworthensis Campylobacter gracilis, Bacteroides gracilis [59]

*New genus.



1) Bacteroides and Parabacteroides

The genus Bacteroides, consisting of saccharolytic, bile-resistant, and nonpigmented species, is limited to species within the Bacteroides fragilis group, which now more than 20 species. The other species within the B. fragilis group are more resistant to many antimicro-bials than B. fragilis and exclusion of the more resistant species in a published data of susceptibility may provide misleading results [38]. Some former Bacteroides species have been reclassified in the genus Prevotella and Porphylomonas [39, 40]. The genus ParaBacteroides consists of three former Bacteroides species, which are P. distasonis, P. goldsteinii, and P. merdae, and in addition, P. gordonii and P. johnsonii [41-43]. The latest new species is P. chongii, isolated from blood of a patient with peritonitis [44].

2) Prevotella and Porphyromonas

The genus Prevotella consists of moderately saccha-rolytic, bile-sensitive, predominantly oral species of formerly classified in the genus Bacteroides [39]. Novel Prevotella species, P. micans and P. nanceiensis, have been isolated not only from the oral cavity, but also from other sites of the body [45, 46]. The nonpigmented former Mitsuokella dentalis and Hallella seregens, which are associated with endodontic and other oral infections, have been reclassified as Prevotella dentalis [47].

The genus Porphylomonas consists of asaccharolytic, pigmented species of formerly classified in the genus Bacteroides [40]. Among Porphyromonas species which are frequently detected in humans, P. gingivalis and P. endodontalis (formerly Bacteroides gingivalis and B. endodontalis) are closely related to the acute symptoms in endodontic infections [48]. The newly described species of human origin are P. pasteri, isolated from human saliva [49], and P. pogonae isolated from clinical specimens [50].

3) Fusobacterium

Based on the 16S-23S rDNA internal transcribed spacer regions (ITS), Fusobacterium species were composed of three phylogenetic clusters; the first cluster (all nonoral) included F. mortiferum, F. varium, and F. ulcerans; the second cluster (all oral) contained. F. nucleatum subspecies, F. naviforme, F. simiae, and F. periodonticum; the third cluster (all invasive potential) included F. necrophorum subspecies and F. gonidia-formans [51]. F. nucleatum, the most commonly encoun-tered in oral infection, is very heterogenous and currently classified as four subspecies including subsp. nucleatum, polymorph, vincentii, and animalis. F. nucleatum subspecies fusiform is a later synonym of subspecies vincentii [52]. In more recent, analyses using the genome sequences strongly suggest that four F. nucleatum subspecies should be reclassified as Fusobacterium species [53]. Fusobacterium equinum, a new species that is phenotypically similar to F. necrop-horum, has been described from the normal oral cavity [54]. The Fusobacterium alocis and F. sulci, belonged to Clostridium cluster XI, have been reclassified as Filifactor alocis and Eubacterium sulci, respectively [55]. The latest proposed new species is F. pseudope-riodonticum isolated from oral cavity based on the whole-genome analysis, most closely related to F. periodonticum [56].

4) Other anaerobic gram-negative rods

Among the genus Dialister, D. invisus and D. pneu-mosintes (formerly Bacteroides pneumosintes) isolated from the oral cavity [57]. Selenomonas sputigena of the genus Selemonas, as type species, is found in specimens from oral infections [58]. Sutterella wadsworthensis, new species of the genus Sutterella, formerly Campylo-bacter gracilis (Bacteroides gracilis), has been isolated from clinical specimens [59]. The genus Bilophila in the family Desulfovibrionaceae includes one human species, Bilophila wadsworthia, which is a important pathogen in humans [60].

CONCLUSION

Anaerobic bacteria are part of the commensal micro-biota of humans in multiple sites of the body as opportunistic pathogens in many infections. The anaerobic taxonomy has undergone considerable changes over the years, mainly due to the increased widespread use of molecular technologies, including 16S rRNA sequencing and WGS. Existing genera and species have been reclassified or renamed and new genera and species have been added, resulting in changes of taxonomy. A subset of these changes is relevant to the field of anaerobic clinical microbiology, particularly in the context of accurate ID and appropriate AST, and epidemiology of emerging infections. The taxonomic updates are necessary to keep track of new names to aim at better description and recognition of the bacterium-disease associations. As the large percentage of the new species described are based on a single isolate of a new species, which was recovered from stool of a healthy person, taxonomic updates are necessary to determine the clinical impor-tance. Furthermore, Current taxonomy is important to work toward better improvement of patient treatment and disease management, because antimicrobial resistance and misidentification of emerging pathogenic anaerobes, such as A. schaalii and Cutibacterium difficile, can be caused the inappropriate empiric therapy. Therefore, CML should periodically update the taxonomic changes of anaerobic bacteria and properly inform clinicians of these changes. This article presents taxonomic changes of clinically important anaerobic bacteria. The update on taxonomy of anaerobic bacteria can help both CML and clinician guide empiric therapy for patient care and prevent treatment failure.

요 약

임상미생물학 분야에서 세균의 분류는 끊임없이 변화하는 상태에 있다. 무산소성 세균의 대규모 분류와 명명법은 지난 수십 년 동안 발생되었는데, 주로 16S rRNA 염기서열 분석 및 전체 게놈 염기서열(WGS) 분석과 같은 분자 기술의 발전 때문이다. 새로운 균속과 균종이 추가되었고, 기존 균종과 균속은 재분류되었거나 재명명되었다. 임상미생물검사실의 주요 역할은 임상적으로 중요한 세균의 정확한 동정 및 적절한 감수성 시험, 그리고 신속한 보고 및 임상의와의 의사 소통이다. 무산소성 세균의 분류학적 변화는 진단적으로 적절한 보고 항균제의 선택과 항균제 감수성 해석 기준의 적용에 잠정적으로 영향을 미칠 수 있다. 이는 신흥 병원성 무산소성 세균의 항균제 내성 및 잘못된 동정은 환자 치료에 있어서 부적절한 경험적 치료를 유발할 수 있기 때문이다. 따라서, 임상미생물검사실은 주기적으로 무산소성 세균의 분류학적 변경 사항을 업데이트하고, 임상의에게 이러한 변경 사항을 적절하게 알려야 한다. 이 논문에서는 임상적으로 중요한 무산소성 세균의 분류에 관한 업데이트을 제시하였고, 이전의 균명 또는 동의어을 함께 기술하였다. 무산소성 세균의 분류 업데이트는 무산소성 세균 감염에 대한 항균제 요법을 안내하고, 치료 실패를 예방하는데 임상미생물검사실과 임상의 모두에게 도움이 될 수 있다.

Acknowledgements

None

Conflict of interest

None

Author’s information (Position)

Kim M, M.T.

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