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BACTERIOLOGY,
Jan. 1988, p. 128-131
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Copyright 0 1988, International Union of Microbiological Societies
Vol. 38, No. 1
Proposal for Reclassification of Bacteroides asaccharolyticus ,
Bacteroides gingivalis, and Bacteroides endodontalis in a New
Genus, Porphyromonas
H. N. SHAH1* AND M. D. COLLINS’
Department of Oral Microbiology, London Hospital Medical College, London El 2AD,l and Division of Microbiology,
AFRC Institute of Food Research, Shinfeld, Reading RG2 9AT,= United Kingdom
The asaccharolytic, pigmented Bacteroides, Bacteroides asaccharolyticus, Bacteroides gingivalis, and Bacteroides endodontalis, form a group of relatively homogeneous species which differ markedly in biochemical and
chemical properties from the type species of Bacteroides, Bacteroides fragilis (Castellani and Chalmers), such
that they should not be retained within this genus. Therefore, we propose that Bacteroides asaccharolyticus
(Holdeman and Moore) Finegold and Barnes, Bacteroides gingivalis Coykendhll, Kaczmarek and Slots, and
Bacteroides endodontalis van Steenbergen, van Winkelhoff, Mayrand, Grenier and de Graaff be reclassified in
a new genus, Porphyromonas, as Porphyromonas asaccharolytica comb. nov., Porphyromonas gingivalis comb.
nov., and Porphyromonas endodontalis comb. nov., respectively.
In Bergey ’s Manual of Determinative Bacteriology, 8th
ed. (12), the asaccharolytic, pigmented Bacteroides were
regarded as a single homogeneous taxon, Bacteroides melaninogenicus subsp. asaccharolyticus. As the clinical significance of these microorganisms in oral cavities was recognized, extensive taxonomic studies were carried out.
Heterogeneity was first demonstrated among these bacteria
through studies of their deoxyribonucleic acid (DNA) base
compositions and enzyme polymorphism, and two regions of
variation were reported (29). These findings were substantiated by sodium dodecyl sulfate polypeptide patterns (34) and
DNA-DNA hybridization data (36). As a result of these
studies on the asaccharolytic, pigmented strains, the group
containing strains with high guanine-plus-cytosine (G+C)
contents (52 to 54 mol%) and an electrophoretically fastmigrating malate dehydrogenase (MDH) was reclassified as a
new species, Bacteroides asaccharolyticus (7, 29). Further
differences between B. asaccharolyticus and the group of
strains with low G+C contents (46 to 48 mol%) and a
slow-migrating MDH (29) were revealed by an analysis of
tlheir lipids (26). Strains of B. asaccharolyticus possess very
high levels of 13-methyl-tetradecanoicacid (iso-C,,,, acid)
and menaquinones with 10 isoprene units (MK-lo), whereas
tlhe group of strains with low G+C contents contains significantly lower levels of iso-C,,:, fatty acids and menaquinones
with nine isoprene units (MK-9) (26). The latter group of
strains was subsequently reclassified as Bacteroides gingivalis (4). It is generally believed that most oral, asaccharolytic, black-pigmented Bacteroides strains belong to B. gingivalis, whereas most nonoral or clinical isolates are B.
asaccharolyticus strains. Recently, a third asaccharolytic
species, Bacteroides endodontalis, which was isolated from
infected dental root canals, has been proposed (37). Phenotypically, B. endodontalis appears to be more closely related
to B. asaccharolyticus than to B. gingivalis and possesses a
DNA base composition of ca. 50 to 51 mol% G+C (37). The
MDH of B . endodontalis migrates faster than the MDHs of B.
asaccharolyticus and B. gingivalis (Shah, unpublished data).
B. asaccharolyticus, B. gingivalis, and B . endodontalis
are well-defined species and on the basis of biochemical and
chemical properties form a relatively homogeneous group
* Corresponding author
quite unrelated to the type species of the genus Bacteroides,
Bacteroides fragilis. All of the asaccharolytic, pigmented
bacteroides accumulate major levels of protoheme rather
than protoporphyrin when cells are cultured on blood agar
(3,25, 27). The three species are nonfermentative and utilize
nitrogenous substrates such as Trypticase and Proteose
Peptone as energy sources (28a, 28b). The metabolic end
products from these substrates include significant levels of
n-butyric acid in addition to other volatile fatty acids (11).
Furthermore, particular amino acids, such as aspartate, are
preferentially catabolized (28a, 28b), and strains generally
possess proteolytic activities (16,19). Unlike other members
of the genus Bacteroides, which .contain predominantly
12-methyl-tetradecanoic acid (anteiso-C,,,, acid) as their
long-chain fatty acid, the asaccharolytic, pigmented species
contain mainly 13-methyl-tetradecanoicacid (iso-C,,,, acid).
The latter taxa also contain MDH and glutamate dehydrogenase but differ from the type species of the genus
Bacteroides., B. fragilis, in lacking enzymes of the hexose
monophosphate shunt-pentose phosphate pathway (viz.,
glucose-6-phosphate dehydrogenase, 6-phosphogluconate
dehydrogenase) (27, 28). All of the asaccharolytic, pigmented species examined so far have DNA base compositions within the range from 46 to 54 mol% G+C. These taxa
also differ from other Bacteroides species studied in lacking
diaminopimelic acid in their cell walls (8, 29).
We have suggested previously that the genus Bacteroides
should be restricted to the type species, B. fragilis, and
related taxa (3, 27). These related taxa include Bacteroides
distasonis, Bacteroides eggerthii, Bacteroides ovatus, Bacteroides thetaiotaomicron, Bacteroides uniformis, and Bacteroides vulgatus and, more recently, Bacteroides caccae,
Bacteroides merdae, and Bacteroides stercoris (14). The
organisms in the “B. fragilis group” have relatively low
G+C contents, ranging from 40 to 48 mol% (13), and the
species are relatively homogeneous biochemically (27, 28).
B. fragilis and related species are saccharolytic and generally produce acetic and succinic acids as the major end
products of glucose metabolism (11). They also differ from
the asaccharolytic, pigmented Bacteroides species in possessing enzymes of the hexose monophosphate shunt-pentose phosphate pathway (27, 28) and in their cellular fatty
128
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VOL. 38, 1988
NOTES
acids (23, 26). Furthermore, the dibasic amino acid of their
peptidoglycan is meso-diaminopimelic acid (29).
Thus, there is now overwhelming biochemical and chemical evidence that the asaccharolytic, pigmented Bacteroides
species differ so markedly from the type species of the genus
Bacteroides, B . fragilis, as to warrant placement in a separate genus. Therefore, we formally propose that the species
presently designated B. asaccharolyticus (7), B. gingivalis
(4), and B. endodontalis (37) be reclassified in a new genus,
Porphyromonas, as Porphyromonas asaccharolytica comb,
nov., Porphyromonas gingivalis comb. nov., and Porphyromonas endodontalis comb. nov., respectively.
Description of Porphyromonas gen. nov. (Por.phy .
ro.mo’nas. Gr. adj. porphyreos purple; Gr. n. monas unit;
N. L. fem.n. Porphyromonas porphyrin cell). The description below is based on our own observations and previous
descriptions of the asaccharolytic, pigmented Bacteroides
species (2,-11, 16, 20, 22, 23, 26-33, 35-38, 42, 43, 45).
Gram-negative, obligately anaerobic, nonsporeforming,
nonmotile rods or coccobacilli. Most cells in broth are small
(0.5 to 0.8 by 1.0 to 3.5 pm), but occasionally longer cells (4
to 6 pm) may be formed. Colonies on blood agar plates are
smooth (rarely rough), shiny, convex, and 1 to 3 mm in
diameter and darken progressively from the edge toward the
center after 6 to 10 days. Eventually the whole colony
becomes black due to protoheme production. Growth is not
significantly affected by carbohydrates. Nitrogenous substrates such as Proteose Peptone, Trypticase, and yeast
extract markedly enhance growth. The optimum temperature for growth is 37°C. Major fermentation products from
BM (29) or PYG (11)medium are n-butyric and acetic acids;
lower levels of propionic, isobutyric, and isovaleric acids are
also produced.
MDH and glutamate dehydrogenase are present; glucose6-phosphate dehydrogenase and 6-phosphogluconate dehydrogenase are absent. Proteolytic activity is variable. Limited ability to ferment amino acids such as aspartate and
asparagine. Indole produced. Nitrate is not reduced to
nitrite. Starch and esculin are not hydrolyzed.
Cell wall peptidoglycan contains lysine as the diamino
acid is absent. The princiacids; 2-keto-3-deoxyoctulosonic
pal respiratory quinones are unsaturated menaquinones with
9 or 10 isoprene units. Both nonhydroxylated and 3-hydroxylated long-chain fatty acids are present. The nonhydroxylated fatty acids are composed of predominantly isomethyl branched types (iso-C,,,, acid) and lower levels of
straight-chain saturated acids. The 3-hydroxylated fatty acids are the straight-chain saturated types.
The DNA base compositions range between 46 to 54 mol%
G+C. The type species is Porphyromonas asaccharolytica.
Description of Porphyromonas asaccharolytica (Holdeman
and Moore) comb. nov. The description below is based on
previous studies (3, 5-11, 15, 18, 23-29, 31, 35, 36, 44) and
our own observations.
Gram-negative, obligately anaerobic, nonsporeforming,
nonmotile rods or coccobacilli. Cells in broth are 0.8 to 1.5
by 1.0 to 3.5 pm, but occasionally longer cells are seen. Cells
from solid media are often coccobacillary. Colonies on blood
agar plates are smooth, shiny, convex, and 1 to 3 mm in
diameter and darken progressively from the edge of the
colony toward the center after 6 to 10 days. Eventually the
whole colony becomes black due to protoheme production.
Nitrogenous substrates such as Proteose Peptone, Trypticase, and yeast extract markedly enhance growth. Addition
of 0.4 to 0.6% NaCl to media supplemented with the latter
hydrolysates enhances growth.
129
Major fermentation products from BM or PYG medium
are n-butyric and acetic acids; lower levels of propionic,
isobutyric, and isovaleric acids are also produced. Phenylacetic acid is not produced. Proteolytic activity is low, but
gelatin liquefaction is positive and fibrinolytic activity is
present. Indole is produced. a-Fucosidase is produced.
Nitrate is not reduced to nitrite. Starch and esculin are not
hydrolyzed. Cells do not agglutinate sheep erythrocytes.
MDH and glutamate dehydrogenase are present; glucose-6phosphate dehydrogenase and 6-phosphogluconate dehydrogenase are absent.
The cell wall peptidoglycan contains lysine; 2-keto-3deoxyoctulosonic acid is absent. The principal respiratory
quinones are menaquinones with 10 isoprene units. Both
nonhydroxylated and 3-hydroxylated fatty acids are present.
The nonhydroxylated fatty acids are composed of predominantly iso-methyl branched types, with iso-C,,:, acid predominating.
The DNA base compositions range between 52 and 54
mol% G+C.
The type strain is strain ATCC 25260.
Description of Porphyromonas gingivalis (Coykendall, Kaczmarek and Slots) comb. nov. The description below is based
on previous studies (1, 3-5, 8-11, 15-19, 21, 23, 25-29, 31,
33, 35, 36, 38, 39; G . Sundqvist, Ph.D. thesis, Umea University of Odontology, Umea, Sweden, 1976) and our own
observations.
Gram-negative, obligately anaerobic, nonsporeforming,
nonmotile rods or coccobacilli. Cells in broth are 0.5 by 1to
2 pm. Cells from solid media are coccobacilli or very short
rods. Colonies on blood agar plates are smooth (occasionally
rough), shiny, convex, and 1to 2 mm in diameter and darken
from the edge of the colony toward the center between 4 and
8 days. Nonpigmented colonies rarely occur. Protoheme is
the major porphyrin produced, but traces of protoporphyrin
also occur. Growth is markedly affected by the presence of
protein hydrolysates such as Trypticase, Proteose Peptone,
and yeast extract. Several amino acids, such as aspartate,
arginine, cystine, histidine, serine, tryptophan, leucine, methionine, phenylalanine, and isoleucine, are utilized. Growth
is enhanced by 0.5 to 0.8% NaC1.
Major fermentation products from BM or PYG medium
are n-butyric and acetic acids; lower levels of propionic,
isobutyric, isovaleric, and phenylacetic acids are also produced. Proteases (for example, a trypsinlike enzyme and
collagenase) are present. Indole is produced. a-Fucosidase
is not produced. Nitrate is not reduced to nitrite. Starch and
esculin are not hydrolyzed. Cells agglutinate sheep erythrocytes. MDH and glutamate dehydrogenase are present;
glucose-6-phosphate dehydrogenase and 6-phosphogluconate dehydrogenase are absent.
Cell wall peptidoglycan contains lysine as the diamino
acid; 2-keto-3-deoxyoctulosonicacid is absent. The principal
respiratory quinones are menaquinones with nine isoprene
units. Both nonhydroxylated and 3-hydroxylated fatty acids
are present. The nonhydroxylated fatty acids are composed
of predominantly iso-methyl branched types, with iso-C,,,,
acid predominating.
The DNA base compositions range between 46 to 48 mol%
G+C.
The type strain is strain ATCC 33277.
Description of Porphyromonas endodontalis (van Steenbergen, van Winkelhoff, Mayrand, Grenier and de Graaff)comb.
nov. The description below is based on previous studies (3,
37, 40-42; Sundqvist, Ph.D. thesis) and our own observations.
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130
INT. J. SYST.BACTERIOL.
NOTES
TABLE 1. Biochemical and chemical characteristics useful in distinguishing the genus Porphyromonas from the B . fragilis group and
some other nonfermentative or weakly fermentative taxa
Taxon
Metabolism"
Major end
products from
PYGb
Presence o f C
MDH
GDH
G6PDH
6PGDH
~~
Porphyromonas
Anaerorhabdus
Bacteroides coagulans
B . fragilis group
Bacteroides putredinis
13acteroides ureolyticus
Rikenella
Tissierella
-
NF
NF
NF
F
NF
NF
NF
NF
Major
long-chain
fatty acids
+
ND
-
+
Menaquinones
~SO-C~~:~
c18:0~c18:1
C16:0,C18:1
anteiso-C,,,,
iso-C,,,,
C18:l
iso-C1s:o
iso-C1s,o
+ND'
+
ND
ND
ND
-
G+C 'Ontent
(mol%)
46-54
34
37
40-48
ND
28-30
60-61
28
F, Fermentative; NF, nonfermentative.
Abbreviations: A, acetic acid; B, butyric acid; L, lactic acid; P, propionic acid; iV, isovaleric acid; S, succinic acid; PA, phenylacetic acid. Data from
reference 11.
Abbreviations: GDH, glutamate dehydrogenase; G6PDH, glucose-6-phosphate dehydrogenase; 6PGDH, 6-phosphogluconate dehydrogenase.
Production of acetic, phenylacetic, isovaleric, and succinic acids varies between species (see Table 2).
ND, Not determined.
a
Gram-negative, obligately anaerobic, nonsporeforming,
nonmotile rods or coccobacilli. Most cells in broth are small,
0.4 to 0.6 by 1.0 to 2.0 pm. Colonies on blood agar plates are
smooth, shiny, convex, entire, and circular and develop dark
brown or black pigmentation between 7 and 14 days. Protoheme is the major pigment, but protoporphyrin is also
present. Most strains produce colonies which adhere
strongly to blood agar plates, and growth in liquid media is
slow. Proteose Peptone, Trypticase, and yeast extract are
good substrates for growth. Casitone and Casamino Acids
are poor growth substrates. The optimum temperature for
growth is 37°C. Major fermentation products are n-butyric
i2nd acetic acids; lower levels of propionic, isobutyric, and
isovaleric acids are also produced. Phenylacetic acid is not
lxoduced. Except for gelatin hydrolysis, proteolytic activity
iis low. a-Fucosidase is not produced. Cells do not agglutinate sheep erythrocytes. Catalase is not produced. Indole
and H,S are produced. Arginine is hydrolyzed; starch and
esculin are not hydrolyzed. Nitrate is not reduced to nitrite.
'Three serotypes are present.
MDH and glutamate dehydrogenase are present; glucose(5-phosphate dehydrogenase and 6-phosphogluconate dehydrogenase are absent. Cell wall peptidoglycan is based on
liysine. Both nonhydroxylated and 3-hydroxylated fatty acids
are present. The nonhydroxylated fatty acids are composed
of predominantly iso-methyl branched types, with iso-C,,,,
acid predominating.
The DNA base compositions range between 49 and 51
mol% G+C.
The type strain is strain ATCC 35406.
Biochemical and chemical characteristics useful in distinguishing the genus Porphyromonas from the B. fragilis group
TABLE 2. Distinguishing characteristics of species of
the genus Porphyromonas
Species
P. asaccharolytica
P. endodontalis
,F. gingivalis
Major acid
end
products"
A,B,S
A,B
B,iV,pA
aFucosidase
Trypsin
+-
-
-
+
MDH
G+C
content
(mol%)
M
F
S
52-54
49-5 1
4648
a Abbreviations: A, acetate, B, butyrate; iV, isovalerate; PA, phenylacelate; S, succinate.
Electrophoretic mobility compared with Bacteriodes intermedius T588
IMDH (28). F, Fast; M, medium; S, slow.
and some other nonfermentative or weakly fermentative
taxa are shown in Table 1. The major distinguishing characteristics of the three species of the genus Porphyromonas are
given in Table 2.
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