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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.
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