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SUPPLEMENT ARTICLE Recent Taxonomic Changes and Terminology Update of Clinically Significant Anaerobic Gram-Negative Bacteria (Excluding Spirochetes) Hannele Jousimies-Somera and Paula Summanen National Public Health Institute, Anaerobe Reference Laboratory, Helsinki, Finland; and Wadsworth Anaerobic Bacteriology Laboratory, Veterans Affairs Medical Center, Los Angeles, California Because of access to 16S rDNA sequencing, changes in the taxonomy and nomenclature of anaerobic gramnegative bacteria have occurred lately. New genera and species have been described, and existing taxa have been reclassified. The present article compiles a list of clinically relevant anaerobes and provides synonyms as well as the old nomenclature used for these bacteria. Although names and classifications of anaerobic bacteria are changing quickly, it is important to keep track of new bacterial names to work toward better description and recognition of bacterium-disease associations. As a result of polyphasic, phylogeny-oriented taxonomic approaches, including16S rRNA nucleotide sequencing, major reorganizations among anaerobic taxa are under way. The present article will briefly update the major recent taxonomic inclusions and changes among clinically significant gram-negative anaerobic bacteria and is based on more detailed reviews elsewhere and on a list of nomenclature published in Clinical Infectious Diseases in 1995, 1997, and 1999 [1–4] (see table 1). BACTEROIDES FRAGILIS GROUP AND SOME OTHER BILE-RESISTANT OR PHYLOGENETICALLY RELATED SPECIES OR GENERA The most pronounced changes have occurred particularly in the genus Bacteroides, which now mainly con- a Deceased. Reprints or correspondence: Paula Summanen, Veterans Affairs Medical Center, Wadsworth Anaerobic Bacteriology Laboratory, Bldg. 304, Rm. E3-224, VAGHLAS 691-151J, Los Angeles, CA 90073 ([email protected]). Clinical Infectious Diseases 2002; 35(Suppl 1):S17–21 2002 by the Infectious Diseases Society of America. All rights reserved. 1058-4838/2002/3505S1-0005$15.00 tains only bile-resistant gram-negative bacilli after the bile-sensitive, saccharolytic pigmented and nonpigmented species were transferred to the genus Prevotella and the pigmented asaccharolytic species to the genus Porphyromonas [5–7]. Other Bacteroides species will most probably be reclassified soon into other existing or new genera. On the basis of phylogenetic data, the bile-resistant Bacteroides distasonis and Bacteroides merdae cluster close to the bile-sensitive Tannerella forsythensis (formerly Bacteroides forsythus) and Porphyromonas, and the bile-resistant Bacteroides splanchnicus most probably to a new genus [2, 8, 9]. Bacteroides tectus and Bacteroides pyogenes (formerly B. tectus DNA homology group II of Love), which are common in infected animal-bite wounds, are related to the B. fragilis group and are bile tolerant but do not readily grow on bacteroides bile esculin agar. We have recently phenotypically and phylogenetically described bile-resistant, pigment-producing gram-negative rods from intestinal sources that, together with Bacteroides putredinis, probably form a new genus with 2–3 species: 1 species is provisionally named “Cholochromatium finegoldii” in honor of Dr. Finegold [10, 11]. Interestingly enough, the bile-sensitive, oral Prevotella heparinolytica and Prevotella zoogleoformans phylogenetically cluster within the B. fragilis group. These Taxonomic Changes and Terminology Update • CID 2002:35 (Suppl 1) • S17 Table 1. Current names, synonyms, or taxonomic position of anaerobic gram-negative bacteria of clinical significance. Current name Bacteroidaceae Bacteroides fragilis group Bacteroides caccae Bacteroides distasonis Bacteroides eggerthii Bacteroides fragilis Bacteroides merdae Bacteroides ovatus Bacteroides stercoris Bacteroides thetaiotaomicron Bacteroides uniformis Bacteroides vulgatus Bacteroides species, other Bacteroides capillosus Bacteroides coagulans Bacteroides putredinis Bacteroides pyogenes a Bacteroides splanchnicus Bacteroides tectus a Bacteroides ureolyticus Fusobacterium Fusobacterium gonidiaformans Fusobacterium mortiferum Fusobacterium naviforme Fusobacterium necrogenes Fusobacterium necrophorum F. necrophorum subspecies funduliforme F. necrophorum subspecies necrophorum Fusobacterium nucleatum F. nucleatum subspecies fusiforme F. nucleatum subspecies nucleatum F. nucleatum subspecies polymorphum F. nucleatum subspecies vincentii Fusobacterium periodonticum Fusobacterium russii a Fusobacterium ulcerans Fusobacterium varium Porphyromonas Porphyromonas asaccharolytica Porphyromonas cangingivalis a Porphyromonas canoris a Porphyromonas cansulci a Porphyromonas catoniae Porphyromonas circumdentaria a Porphyromonas crevioricanis a Porphyromonas endodontalis Porphyromonas gingivalis Porphyromonas gulae a Porphyromonas gingivicanis a Porphyromonas levii a Porphyromonas macacae a Prevotella Prevotella bivia Prevotella buccae Prevotella Prevotella Prevotella Prevotella Prevotella Prevotella Prevotella Prevotella buccalis corporis dentalis denticola disiens enoeca heparinolytica intermedia Synonym and/or taxonomic position True Bacteroides B. fragilis group 3452A Related to Porphyromonas species B. fragilis T4-1 B. fragilis subspecies a Taxonomic position of the non–B. fragilis group Bacteroides remains uncertain Possibly related to Rikenella Bacteroides tectus homology cluster II (some strains) Possibly represents a new genus Bacteroides tectum, related to B. fragilis group Bacteroides corrodens, related to Campylobacter Related to F. nucleatum F. pseudonecrophorum Bacteroides asaccharolyticus, Bacteroides melaninogenicus subspecies asaccharolyticus Oribaculum catoniae Bacteroides endodontalis Bacteroides gingivalis P. gingivalis (catalase-positive strains) Bacteroides levii, B. melaninogenicus subspecies levii Bacteroides macacae, Porphyromonas salivosa Bacteroides bivius Bacteroides buccae Bacteroides ruminicola subspecies brevis, Bacteroides capillus, Bacteroides pentosaceus Bacteroides buccalis Bacteroides corporis Mitsuokella dentalis, Hallella seregens Bacteroides denticola Bacteroides disiens New species Bacteroides heparinolyticus, related to B. fragilis group Bacteroides intermedius Bacteroides melaninogenicus, subspecies intermedius (continued) Table 1. (Continued.) Current name Prevotella loescheii Prevotella melaninogenica Prevotella nigrescens Prevotella oralis Prevotella oris Prevotella oulorum Prevotella pallens Prevotella tannerae Prevotella veroralis Prevotella zoogleoformans Other Bacteroidaceae genera Anaerorhabdus furcosus Bilophila wadsworthia Butyrivibrio fibrisolvens Catonella morbi Centipeda periodontii Dialister pneumosintes a Dichelobacter nodosus Johnsonella ignava Leptotrichia buccalis Leptotrichia sanguinegens Mitsuokella multacida Selenomonas Selenomonas artemidis Selenomonas dianae Selenomonas flueggei Selenomonas infelix Selenomonas noxia Selenomonas sputigena Sutterella wadsworthensis Tannerella forsythensis Tissierella praeacuta Campylobacteraceae Campylobacter concisus Campylobacter curvus Campylobacter gracilis Campylobacter hominis Campylobacter rectus Campylobacter showae Campylobacter sputorum Dissimilatory sulphate- or sulphur-reducing bacteria Desulfovibrio desulfuricans “Desulfovibrio fairfieldensis” Desulfovibrio piger Succinivibrionaceae Anaerobiospirillum succiniciproducens Anaerobiospirillum thomasii Gram-negative cocci Veillonellaceae Acidaminococcus fermentans Megasphaera elsdenii Veillonella parvula Veillonella dispar a Synonym and/or taxonomic position Bacteroides loescheii B. melaninogenicus, B. melaninogenicus subspecies melaninogenicus Prevotella intermedia (some strains) Bacteroides oralis Bacteroides oris, B. ruminicola subspecies brevis Bacteroides oulorum, Prevotella oulora New species New species Bacteroides veroralis Bacteroides zoogleoformans, related to B. fragilis group Bacteroides furcosus, related to Porphyromonas species Related to Clostridium subphylum cluster XIVa Related to Clostridium subphylum cluster XIVa Related to Selenomonas species Bacteroides pneumosintes, related to Sporomusa branch of Clostridium subphylum cluster IX Bacteroides nodosus Related to Clostridium subphylum, cluster XIVa Mitsuokella multiacidus Bacteroides multiacidus, related to the Sporomusa branch of Clostridium subphylum cluster IX Related to Sporomusa branch of Clostridium subphylum cluster IX Campylobacter (Bacteroides) gracilis (some strains) Bacteroides forsythus Bacteroides praeacutus, related to Clostridium subphylum cluster XII Wolinella curva B. gracilis (some strains) New species Wolinella recta Provisional new species Desulfomonas pigra New family New species Related to Sporomusa branch of Clostridium subphylum cluster IX Veterinary origin. examples underscore the fact that phenotypic characteristics, which have been formerly considered as useful taxonomic markers, do not necessarily concur with phylogenetic clustering [2]. PREVOTELLA AND PORPHYROMONAS The gram-negative pigmented Prevotella species common in oral flora and oral-associated infections now include 8 species, Taxonomic Changes and Terminology Update • CID 2002:35 (Suppl 1) • S19 the latest inclusions being Prevotella nigrescens, Prevotella tannerae, and Prevotella pallens. The nonpigmented former Mitsuokella dentalis and Hallella seregens, which are often associated with endodontic and, occasionally, with other oral infections, have been renamed as one species, Prevotella dentalis. Prevotella enoeca is another recently described nonpigmented species. Prevotella ruminicola, Prevotella brevis, Prevotella bryantii, and Prevotella albensis are recently described species of animal origin that were formerly included in B. ruminicola. The genus Porphyromonas, of which Porphyromonas gingivalis and Porphyromonas endodontalis are the key pathogens in adult periodontitis and endodontic infections, respectively, currently include 12 pigmented and 1 nonpigmented species, Porphyromonas catoniae. Of these, only 4 are of human origin. P. catoniae (formerly Oribaculum catoniae) is an indole-negative, nonpigmented species and, more often than other oral Porphyromonas species, produces b-lactamase. It is a common inhabitant of the healthy oral cavity in children and adults but has been occasionally isolated from oral-associated infections as well [12]. Porphyromonas gulae, the former catalase-positive P. gingivalis, which is common in the oral cavities of dogs and cats and is therefore a potential finding from infected bite wounds, is the most recent inclusion in the Porphyromonas genus [13]. Several new groups such as Porphyromonas levii–like organisms common in chronic suppurations and leg ulcers in patients with peripheric ischemia, and P. endodontalis–like organisms from intestinal sources, are awaiting inclusion in the genus Porphyromonas [2]. Rapid laboratory identification of these Prevotella and Porphyromonas species can be done by means of preformed enzyme substrate tablets or kits [14–16]. bile-resistant variants, more often found in infections below the waist, belong to a new genus Sutterella as Sutterella wadsworthensis [18]. These organisms are microaerophilic and resistant to bile and several antimicrobial agents including metronidazole, the latter being a feature of value in species differentiation [15, 16]. A relatively new catalase-positive species, Campylobacter showae stems from oral samples and the latest inclusion into this genus, Campylobacter hominis, from the intestinal tract [19]. CAPNOCYTOPHAGA, LEPTOTRICHIA, AND DYSGONOMONAS The oral cavity–associated Capnocytophaga hemolytica and Capnocytophaga granulosa (often causing mucositis in immunocompromised patients) as well as the so far nonoral Leptotrichia sanquinegens are new species among the capnophilic taxa. These organisms often are resistant to b-lactam antibiotics and aminoglycosides. Dysgonomonas is a new genus with slow-growing and fastidious, facultative gram-negative rods that consequently easily escape recognition in aerobic culture. Two species, Dysgonomonas gadei (formerly CDC DF-3–like organisms; requires hemin) and Dysgonomonas capnocytophagoides (formerly CDC DF-3 organisms), which display resistance to several antimicrobial agents, including cephalosporins, fluoroquinolones, and macrolides, have been isolated from gall bladder and blood cultures, wounds, and abscesses, respectively [20]. SOME MOTILE RODS FUSOBACTERIUM Fusobacterium nucleatum, the most commonly encountered gram-negative organism in oral infections, currently has 5 subspecies and is very heterogeneous; (phylo)genetic analyses place Fusobacterium periodonticum within F. nucleatum. The validity of the current subspecies of F. nucleatum has been challenged by several study groups and remains to be confirmed [2]. The former Fusobacterium alocis and Fusobacterium sulci have been reclassified as Filifactor alocis and Eubacterium sulci because they cluster among the respective gram-positive genera [17]. The bile-resistant Fusobacterium varium, which is rarely isolated from oral sites, currently includes Fusobacterium pseudonecrophorum. A more detailed report of the fusobacterial taxonomy is given in D. Citron’s article (in this supplement, pp. S22-7). CAMPYLOBACTER AND SUTTERELLA The bile-sensitive former B. gracilis, which is often isolated from infections above the waist, now are Campylobacter gracilis; the S20 • CID 2002:35 (Suppl 1) • Jousimies-Somer and Summanen “Desulfovibrio fairfieldensis” from nonoral sites is a new provisionally named species among the genus Desulfovibrio (motile) that recently has been proposed to include also the former Desulfomonas pigra, as Desulfovibrio piger (nonmotile) [21, 22]. These sulfate-reducing bacteria usually reside in the intestines and have been isolated from blood culture, liver abscess, urine, and possibly from diseased periodontal pockets, together with a newly described Desulfomicrobium orale [21]. Anaerobiospirillum thomasii (possible zoonotic source) is a recently described spiral, motile organism that has been also isolated from humans with diarrhea. It was recently proposed that this species be included in a new family Succinivibrionaceae together with Succinivibrio dextrinosolvens and Succinimonas amylolytica, which are starch digesters from the rumen of sheep and cattle and with some other vibrios [23]. Phylogenetic analyses have shown further that oral-associated Centipeda periodontii, which is related to Selenomonas species, Dialister pneumosintes (often misidentified as Veillonella), and gut-associated Mitsuokella multiacida all belong to the Sporomusa branch of Clostridium subphylum, cluster IX. This cluster also harbors all genera in the family Veillonellaceae. The gram-negative Catonella morbi and Johnsonella ignava, together with Butyrivibrio fibrisolvens, phylogenetically cluster to Clostridium subphylum cluster XIVa [24, 25]. Although the taxonomy and nomenclature of anaerobic bacteria is in rapid phase of changes, it is important to keep track of new bacterial names to aim at better description and recognition of the bacterium-disease associations. The clinical microbiology laboratory should continue to report the former names along with the new ones for long enough periods to allow clinicians to become acquainted with them. For laboratory tests to help with the identification of the new taxa, the latest edition of the ASM’s Manual of Clinical Microbiology and the Wadsworth-KTL Anaerobic Bacteriology Manual [15, 16] can be of help. References 1. Jousimies-Somer HR. Update on the taxonomy and the clinical and laboratory characteristics of pigmented anaerobic gram-negative rods. Clin Infect Dis 1995; 20(Suppl 2):S187–91. 2. Jousimies-Somer HR. Recently described clinically important anaerobic bacteria: taxonomic aspect and update. Clin Infect Dis 1997; 25:S78–87. 3. Finegold SM, Jousimies-Somer HR. Recently described clinically important anaerobic bacteria: medical aspects. Clin Infect Dis 1997; 25: S88–93. 4. Jousimies-Somer H, Summanen P. Microbiology terminology update: clinically significant anaerobic gram-positive and gram-negative bacteria (excluding spirochetes). Clin Infect Dis 1999; 29:724–7. 5. Shah HN, Collins MD. Proposal for reclassification of Bacteroides asaccharolyticus, Bacteroides gingivalis, and Bacteroides endodontalis in a new genus, Porphyromonas. Int J Syst Bacteriol 1988; 38:128–31. 6. Shah HN, Collins MD. Proposal to restrict the genus Bacteroides (Castellani and Chalmers) to Bacteroides fragilis and closely related species. Int J Syst Bacteriol 1989; 39:85–7. 7. Shah HN, Collins MD. Prevotella, a new genus to include Bacteroides melaninogenicus and related species formerly classified in the genus Bacteroides. Int J Syst Bacteriol 1990; 40:205–8. 8. Paster BJ, Dewhirst FE, Olsen I, Fraser GIJ. Phylogeny of Bacteroides, Prevotella, and Porphyromonas spp. and related bacteria. J Bacteriol 1994; 176:725–32. 9. Sakamoto M, Suzuki M, Umeda M, Ishikawa M, Benno Y. Reclassification of Bacteroides forsythus (Tanner et al. 1986) as Tannerella forsythensis gen. nov., comb. nov. Int J Syst Evol Microbiol 2002; 52:841–9. 10. Rautio M, Lönnroth M, Saxen H, et al. Characteristics of an unusual anaerobic pigmented gram-negative rod isolated from normal and inflamed appendices. Clin Infect Dis 1997; 25(Suppl 2):S107–10. 11. Rautio M, Eerola E, Jalava J, Jousimies-Somer H. Phylogenetic description of a bile-resistant pigmenter, probably conforming to a new genus and species. Rev Med Microbiol 1997; 8(Suppl 1):S103. 12. Könönen E, Väisänen M-L, Finegold SM, Heine R, Jousimies-Somer H. Cellular fatty-acid analysis and enzyme profiles of Porphyromonas catoniae—a frequent colonizer of the oral cavity in children. Anaerobe 1996; 2:329–35. 13. Fournier D, Mouton C, Lapierre P, Kato T, Okuda K, Ménard C. Porphyromonas gulae sp. nov., an anaerobic gram-negative coccobacillus from the gingival sulcus of various animal hosts. Int J Syst Evol Microbiol 2001; 51:1179–89. 14. Hudspeth MK, Hunt Gerado S, Citron DM, Goldstein EJC. Growth characteristics and a novel method for identification (the WEE-TAB System) of Porphyromonas species isolated from infected dog and cat bite wounds in humans. J Clin Microbiol 1997; 35:2450–3. 15. Jousimies-Somer HR, Summanen P, Baron EJ, Citron DM, Wexler HM, Finegold SM. Wadsworth-KTL anaerobic bacteriology manual. 6th ed. Belmont, CA: Star Publishing, 2002. 16. Jousimies-Somer H, Summanen P, Finegold SM. Bacteroides, Porphyromonas, Prevotella, Fusobacterium, and other anaerobic gram-negative bacteria. In: Murray P et al., eds. Manual of clinical microbiology. 7th ed. Washington, DC: American Society for Microbiology, 1999. 17. Jalava J, Eerola E. Phylogenetic analysis of Fusobacterium alocis and Fusobacterium sulci based on 16S rRNA gene sequences: proposal of Filifactor alocis (Cato, Moore and Moore) comb. nov. and Eubacterium sulci (Cato, Moore and Moore) comb. nov. Int J Syst Bacteriol 1999;49: 1375–9. 18. Molitoris E, Wexler HM, Finegold SM. Sources and antimicrobial susceptibilities of Campylobacter gracilis and Sutterella wadsworthensis. Clin Infect Dis 1997; 25(Suppl 2):S264–5. 19. Lawson AJ, On SLW, Logan JMJ, Stanley J. Campylobacter hominis sp. nov., from the human gastrointestinal tract. Int J Syst Evol Microbiol 2001; 51:651–60. 20. Hofstad T, Olsen I, Eribe ER, Falsen E, Collins MD, Lawson PA. Dysgonomonas gen. nov. to accommodate Dysgonomonas gadei sp. nov., an organism isolated from a human gall bladder, and Dysgonomonas capnocytophagoides (formerly CDC group DF-3). Int J Syst Evol Bacteriol 2000; 50:2189–95. 21. Langendijk PS, Kulik EM, Sandmeier H, Meyer J, van der Hoeven JS. Isolation of Desulfomicrobium orale sp. nov. and Desulfovibrio strain NY682, oral sulfate-reducing bacteria involved in human periodontal disease. Int J Syst Evol Bacteriol 2001; 51:1035–44. 22. Loubinoux J, Valente FMA, Pereia IAC, Costa A, Grimont PAD, Le Faou AE. Reclassification of the only species of the genus Desulfomonas, Desulfomonas pigra, as Desulfovibrio piger comb. nov. Int J Syst Evol Microbiol 2002; 52:1305–8. 23. Hippe H, Hagelstein A, Kramer I, Swiderski J, Stackebrandt E. Phylogenetic analysis of Formivibrio citricus, Propionivibrio dicarboxylicus, Anaerobiospirillum thomasii, Succinimonas amylotytica and Succinivibrio dextrinosolvens and proposal of Succinivibrionaceae fam. nov. Int J Syst Evol Bacteriol 1999; 49:779–82. 24. Collins MD, Lawson PA, Willems A. The phylogeny of the genus Clostridium: proposal of five new genera and eleven new species combinations. Int J Syst Bacteriol 1994; 44:812–26. 25. Willems A, Amat-Marco M, Collins MD. Phylogenetic analysis of Butyrivibrio strains reveals three distinct groups within the Clostridium subphylum of the gram-positive bacteria. Int J Syst Bacteriol 1996; 46: 195–9. Taxonomic Changes and Terminology Update • CID 2002:35 (Suppl 1) • S21