Because of access to 16S rDNA sequencing, changes in the taxonomy and nomenclature of anaerobic gram-negative 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).
Current names, synonyms, or taxonomic position of anaerobic gram-negative bacteria of clinical significance.
The most pronounced changes have occurred particularly in the genus Bacteroides, which now mainly contains 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 examples underscore the fact that phenotypic characteristics, which have been formerly considered as useful taxonomic markers, do not necessarily concur with phylogenetic clustering [2].
The gram-negative pigmented Prevotella species common in oral flora and oral-associated infections now include 8 species, 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 β-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].
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).
The bile-sensitive former B. gracilis, which is often isolated from infections above the waist, now are Campylobacter gracilis; the 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].
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 β-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].
“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.
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