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Microbe Division/Japan Collection of Microorganisms, RIKEN BioResource Center, Wako, Saitama 351-0198, Japan
Correspondence
Mitsuo Sakamoto
sakamoto{at}jcm.riken.jp
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ABSTRACT |
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 TOP ABSTRACT MAIN TEXTDescription of Parabacteroides...Description of Parabacteroides...Description of Parabacteroides...Description of Parabacteroides...REFERENCES |
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The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA gene sequences of P. distasonis strains JCM 5825T, JCM 13400, JCM 13401, JCM 13402, JCM 13403 and JCM 13404 and P. merdae strains JCM 9497T and JCM 13405 are AB238922–AB238929, respectively.
The cellular fatty acid content and biochemical characteristics of Parabacteroides distasonis gen. nov., comb. nov. and Parabacteroides merdae comb. nov. and a phylogenetic tree based on sequences of 16S–23S rRNA gene ITS regions are available as supplementary material in IJSEM Online.
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MAIN TEXT |
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TOPABSTRACTMAIN TEXTDescription of Parabacteroides...Description of Parabacteroides...Description of Parabacteroides...Description of Parabacteroides...REFERENCES |
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) and the Approved Lists of Bacterial Names (Moore et al., 1985). Later, Shah & Collins (1989) formally proposed that the genus Bacteroides should be restricted to Bacteroides fragilis and related taxa and the description of the genus was emended accordingly. Consequently, several novel genera, such as Alistipes (Rautio et al., 2003), Dialister (Moore & Moore, 1994), Dichelobacter (Dewhirst et al., 1990) and Tannerella (Sakamoto et al., 2002), have been proposed for ‘outmembers' of the genus Bacteroides. However, the taxonomic status of Bacteroides distasonis and Bacteroides merdae is still uncertain. 16S rRNA gene sequence analysis (Paster et al., 1994; Sakamoto et al., 2002) led to the suggestion that B. distasonis and B. merdae were not species within the genus Bacteroides. B. distasonis and B. merdae were related to members of the first subcluster of the Porphyromonas cluster, with a mean 16S rRNA gene sequence similarity of about 84 %. In addition, the two species were related to Tannerella forsythensis (Sakamoto et al., 2002) with about 90 % similarity. More recently, Song et al. (2005) proposed a novel species of the genus Bacteroides, Bacteroides goldsteinii. This species was related to B. distasonis and B. merdae, with a mean 16S rRNA gene sequence similarity of about 93 %. Furthermore, B. goldsteinii was related to T. forsythensis, with about 90 % similarity. B. goldsteinii was classified as a novel Bacteroides species as, using current phenotypic tests, the bacterium could not be separated from Bacteroides sensu stricto. In this study, we attempted to determine the taxonomic status of B. distasonis, B. goldsteinii and B. merdae. Based on the results presented, a novel genus is proposed to accommodate B. distasonis, B. goldsteinii and B. merdae.
The strains used in this study were maintained on Eggerth Gagnon (EG) agar (Merck), supplemented with 5 % (v/v) horse blood, for 2 days at 37 °C in an atmosphere of 100 % CO2. Strains JCM 13400, JCM 13401, JCM 13402, JCM 13403, JCM 13404 and JCM 13405 were isolated from human faeces. Bacteroides bile aesculin agar (Shah, 1992) was used to check whether the growth of the isolates was inhibited on this medium. A multiplex-PCR technique using species-specific primers (Liu et al., 2003) was used to identify B. distasonis and B. merdae. Physiological reactions were determined in duplicate with an API 20A anaerobe test kit, as recommended by the manufacturer (bioMérieux). Fatty acid methyl esters (FAMEs) were obtained from about 40 mg wet cells by saponification, methylation and extraction, using minor modifications (Kuykendall et al., 1988) of the method of Miller (1982). Cellular fatty acid profiles were determined by using the MIDI microbial identification system (Microbial ID). Isoprenoid quinones were extracted as described by Komagata & Suzuki (1987) and were analysed as described previously (Sakamoto et al., 2002). Biochemical reactions were determined in duplicate with a Rapid ID 32A anaerobe identification kit, as recommended by the manufacturer (bioMérieux). The 16S rRNA gene was analysed as described previously (Sakamoto et al., 2002). Related sequences were aligned using the CLUSTAL W program (Thompson et al., 1994) and corrected by manual inspection. Nucleotide substitution rates (Knuc values) were calculated (Kimura, 1980) after gaps and unknown bases had been eliminated. A phylogenetic tree was constructed by using the neighbour-joining method (Saitou & Nei, 1987). Bootstrap resampling analysis (Felsenstein, 1985) was performed to estimate the confidence of tree topologies.
Cells of strains JCM 13400–13405 were obligately anaerobic, non-spore-forming, non-motile, Gram-negative rods. Strains JCM 13400–13404 were identified as representing B. distasonis by using a multiplex-PCR assay; likewise, strain JCM 13405 was identified as representing B. merdae. The growth of these six clinical isolates and B. distasonis JCM 5825T, B. goldsteinii JCM 13446T and B. merdae JCM 9497T was not inhibited on medium containing 20 % bile. Cells on EG agar were 0.8–1.6x1.2–12 µm in size and occurred singly. Colonies on EG agar plates were 1–2 mm in diameter, grey to off-white–grey, circular, entire, slightly convex and smooth. Phenotypic characteristics are given in the species descriptions.
The cellular fatty acid composition of Bacteroides species has been determined (Mayberry et al., 1982; Miyagawa et al., 1979; Shah & Collins, 1980) and reviewed for the classification of the genus Bacteroides (Shah & Collins, 1983). In this study, the cellular fatty acid compositions of the clinical isolates and B. distasonis JCM 5825T and B. merdae JCM 9497T were almost the same. The major cellular fatty acids of the above strains were anteiso-C15 : 0 and iso 3-OH-C17 : 0 (25–32 and 23–26 %, respectively). A significant amount of C18 : 1
9c (14–16 %) was also present (Supplementary Table S1 in IJSEM Online). These findings are in agreement with that reported for B. goldsteinii, except for anteiso 3-OH-C17 : 0 (Song et al., 2005). Song et al. (2005) reported that the ratio iso 3-OH-C17 : 0/anteiso 3-OH-C17 : 0 in whole-cell methanolysates of B. goldsteinii was lower than that for B. merdae (ratio ranging from 1.4 to 2.2 for B. goldsteinii and 6.1 to 8.3 for B. merdae). In this study, the ratio iso 3-OH-C17 : 0/anteiso 3-OH-C17 : 0 in whole-cell methanolysates of B. distasonis and B. merdae was 5.7–9.4 and 5.2–7.6, respectively.
The major menaquinones of the clinical isolates and B. distasonis JCM 5825T, B. goldsteinii JCM 13446T and B. merdae JCM 9497T were MK-9 and MK-10 (Table 1). The menaquinone compositions of B. distasonis JCM 5825T and B. goldsteinii JCM 13446T were almost the same. On the other hand, the major menaquinones of other Bacteroides species were MK-10 and MK-11, except for Bacteroides vulgatus JCM 5826T, which contained a small amount of MK-11 (Sakamoto et al., 2002).
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; Slots, 1981; Tanner et al., 1985). In addition, the RapID-ANA system (Innovative Diagnostics Systems) has been reported to be helpful in the identification of some phenotypically similar bile-inhibited Bacteroides species (Dellinger & Moore, 1986). The biochemical characteristics of the clinical isolates and B. distasonis JCM 5825T and B. merdae JCM 9497T are available in Supplementary Table S2 in IJSEM Online. In this study, all strains were tested using Rapid ID 32A. The biochemical characteristics of strains JCM 13400–13404 were similar to those of B. distasonis JCM 5825T. Furthermore, the biochemical characteristics of strain JCM 13405 and B. merdae JCM 9497T resembled each other.
Approximately 1500 bases of the 16S rRNA gene sequence were determined for the clinical isolates and B. distasonis JCM 5825T and B. merdae JCM 9497T. Strains JCM 13400–13404 were closely related to B. distasonis JCM 5825T, with about 99 % similarity (>98.7 %). In addition, strain JCM 13405 was closely related to B. merdae JCM 9497T, with 99.9 % similarity. For the phylogenetic analysis, 1340 bp (positions 61–1375; Escherichia coli numbering system) sequences of each strain were used. 16S rRNA gene sequence analysis showed that B. distasonis JCM 5825T, B. goldsteinii JCM 13446T and B. merdae JCM 9497T were not species within the genus Bacteroides (Fig. 1). These three species were phylogenetically closely related to each other (>92.3 %) and were related to T. forsythensis with about 90 % similarity. Other remotely related taxa included the genera Bacteroides (83.5–88.8 % sequence similarity), Dysgonomonas (85.9–89.4 %), Paludibacter (86.9–88.5 %; Ueki et al., 2006), Porphyromonas (82.2–86.9 %), Prevotella (77.2–81.9 %) and Proteiniphilum (85.9–87.3 %; Chen & Dong, 2005). In addition, a preliminary analysis of the 16S–23S rRNA gene internal transcribed spacer (ITS) regions also showed that B. distasonis and B. merdae were phylogenetically distinct from species of the genus Bacteroides and were related to T. forsythensis (Supplementary Fig. S1 in IJSEM Online). The ITS regions have been used as an important tool for classification and differentiation of bacterial species (Conrads et al., 2005).
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). In addition, although the major menaquinones of T. forsythensis were MK-10 and MK-11, the major menaquinones of B. distasonis, B. goldsteinii and B. merdae were MK-9 and MK-10. The three species were phenotypically similar to Bacteroides sensu stricto, but phylogenetically distinct. Furthermore, B. distasonis, B. goldsteinii and B. merdae could be differentiated from Bacteroides sensu stricto (predominant menaquinones: MK-10 and MK-11) by the menaquinone composition. This is an important chemotaxonomic characteristic of these species. These results suggest that a novel genus should be established to accommodate B. distasonis, B. goldsteinii and B. merdae.
Based on the above-mentioned findings and the 16S rRNA gene sequence analysis, we propose a novel genus, Parabacteroides gen. nov. Bacteroides distasonis, Bacteroides goldsteinii and Bacteroides merdae are reclassified as Parabacteroides distasonis gen. nov., comb. nov., Parabacteroides goldsteinii comb. nov. and Parabacteroides merdae comb. nov., respectively. Differential characteristics of Parabacteroides gen. nov. and some related taxa are shown in Table 2.
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Description of Parabacteroides gen. nov. |
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TOPABSTRACTMAIN TEXTDescription of Parabacteroides...Description of Parabacteroides...Description of Parabacteroides...Description of Parabacteroides...REFERENCES |
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Cells are Gram-negative, obligately anaerobic, non-spore-forming, non-motile and rod-shaped, and 0.8–1.6x1.2–12 µm in size. Colonies on EG agar plates are 1–2 mm in diameter, grey to off-white–grey, circular, entire, slightly convex and smooth. Saccharolytic. Major end-products are acetic and succinic acids; lower levels of other acids may be produced. Grow on medium containing 20 % bile. Aesculin is hydrolysed. Indole is not produced. Glucose-6-phosphate dehydrogenase (G6PDH), 6-phosphogluconate dehydrogenase (6PGDH), malate dehydrogenase and glutamate dehydrogenase are present. 
-Fucosidase is negative. The principal respiratory quinones are menaquinones MK-9 and MK-10. Both non-hydroxylated and 3-hydroxylated long-chain fatty acids are present. The non-hydroxylated acids are predominantly of the saturated straight-chain and anteiso-methyl branched-chain types. The G+C content is 43–46 mol%. Member of the Bacteroides subgroup of the phylum Bacteroidetes. The type species is Parabacteroides distasonis.
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Description of Parabacteroides distasonis (Eggerth and Gagnon 1933) comb. nov.
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TOPABSTRACTMAIN TEXTDescription of Parabacteroides...Description of Parabacteroides...Description of Parabacteroides...Description of Parabacteroides...REFERENCES |
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Basonym: Bacteroides distasonis Eggerth and Gagnon 1933.
The description of Parabacteroides distasonis is as those given by Eggerth & Gagnon (1933) and Holdeman et al. (1977, 1984). Urease is not produced. Catalase is produced. Gelatin is not liquefied. Acid is produced from D-cellobiose, glucose, lactose, D-mannose, D-melezitose, D-raffinose, L-rhamnose, salicin, sucrose, D-trehalose and D-xylose, but not from L-arabinose, glycerol, D-mannitol or D-sorbitol. Positive reactions are obtained using Rapid ID 32A for -galactosidase, 
-galactosidase, -glucosidase, -glucosidase, N-acetyl--glucosaminidase, glutamic acid decarboxylase, alkaline phosphatase, arginine arylamidase, leucyl glycine arylamidase, phenylalanine arylamidase, leucine arylamidase, tyrosine arylamidase, alanine arylamidase, glycine arylamidase, histidine arylamidase and glutamyl glutamic acid arylamidase. Variable for -arabinosidase and serine arylamidase. Mannose and raffinose are fermented. All the other tests are negative. Major cellular fatty acids are anteiso-C15 : 0 and iso 3-OH-C17 : 0. A significant amount of C18 : 19c is also present. The G+C content of the type strain is 44 mol%.
The type strain is JCM 5825T (=CCUG 4941T=DSM 20701T=ATCC 8503T), which was isolated from human faeces, where it is one of the most common species. Strains have been isolated occasionally from human clinical specimens.
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Description of Parabacteroides goldsteinii (Song et al. 2006) comb. nov.
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TOPABSTRACTMAIN TEXTDescription of Parabacteroides...Description of Parabacteroides...Description of Parabacteroides...Description of Parabacteroides...REFERENCES |
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Basonym: Bacteroides goldsteinii Song et al. 2006.
The description of Parabacteroides goldsteinii is as that given by Song et al. (2005). Urease is not produced. Nitrate is not reduced. Acid is produced from cellobiose, glucose, rhamnose, sucrose, trehalose and xylose, but not from arabinose or xylan. In peptone yeast broth and peptone yeast glucose broth, major amounts of acetic and succinic acids and minor amounts of isovaleric acid, propionic acid and formic acid are produced. Using API ZYM, Rapid ID 32A and RapID ANA II systems, strains have the same profile. Positive reactions are obtained for -glucosidase, -galactosidase, -galactosidase, N-acetyl--glucosaminidase, naphthol-AS-BI-phosphohydrolase, acid phosphatase, alkaline phosphatase, leucine arylamidase, p-nitrophenylphosphatase, arginine arylamidase, leucyl glycine arylamidase, phenylalanine arylamidase, alanine arylamidase, glycine arylamidase, histidine arylamidase, glutamyl glutamic acid arylamidase, leucyl glycine aminopeptidase, glycine aminopeptidase, phenylalanine aminopeptidase, arginine aminopeptidase and serine aminopeptidase. All the other tests are negative. Mannose and raffinose are fermented (Rapid ID 32A). Using Rosco diagnostic tablets (Rosco), -xylosidase, -glucuronidase, -glucosidase, -glucosidase, -galactosidase, -galactosidase (o-nitrophenol--D-galactopyranoside), N-acetyl--glucosaminidase, alkaline phosphatase and -arabinosidase are present; -arabinosidase is tested as positive only by Rosco tablets. Major cellular fatty acids are anteiso-C15 : 0 and iso 3-OH-C17 : 0 (25–28 and 18–23 %, respectively). Significant amounts of C18 : 19c and anteiso 3-OH-C17 : 0 (11–16 and 9–15 %, respectively) are also present. Susceptible to metronidazole (MIC
2 µg ml–1) and ertapenem (MIC1 µg ml–1). Some resistance is seen with clindamycin (MIC8 µg ml–1). Resistant to penicillin G (MIC
32 µg ml–1), cefotetan (MIC256 µg ml–1) and vancomycin (MIC32 µg ml–1). -Lactamase-positive. The G+C content of the type strain is 43 mol%.
The type strain is JCM 13446T (=CCUG 48944T), which was isolated from human clinical specimens of intestinal origin.
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Description of Parabacteroides merdae (Johnson et al. 1986) comb. nov.
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TOPABSTRACTMAIN TEXTDescription of Parabacteroides...Description of Parabacteroides...Description of Parabacteroides...Description of Parabacteroides...REFERENCES |
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Basonym: Bacteroides merdae Johnson et al. 1986.
The description is the same as that given by Johnson et al. (1986). Urease and catalase are not produced. Gelatin is not liquefied. Acid is produced from glucose, lactose, maltose, D-mannose, D-raffinose, sucrose, D-trehalose and D-xylose, but not from L-arabinose, D-cellobiose, glycerol, D-mannitol, D-melezitose, L-rhamnose, salicin or D-sorbitol. Positive reactions are obtained using Rapid ID 32A for -galactosidase, -galactosidase, -glucuronidase, N-acetyl--glucosaminidase, glutamic acid decarboxylase, alkaline phosphatase, arginine arylamidase, leucyl glycine arylamidase, phenylalanine arylamidase, leucine arylamidase, pyroglutamic acid arylamidase, tyrosine arylamidase, alanine arylamidase, glycine arylamidase, histidine arylamidase and glutamyl glutamic acid arylamidase. Variable for -glucosidase, -arabinosidase and serine arylamidase. Mannose and raffinose are fermented. All the other tests are negative. Major cellular fatty acids are anteiso-C15 : 0 and iso 3-OH-C17 : 0. A significant amount of C18 : 19c is also present. The G+C content of the type strain is 44 mol%.
The type strain is JCM 9497T (=CCUG 38734T=ATCC 43184T), which was isolated from human faeces.
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ACKNOWLEDGEMENTS |
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REFERENCES |
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TOPABSTRACTMAIN TEXTDescription of Parabacteroides...Description of Parabacteroides...Description of Parabacteroides...Description of Parabacteroides...REFERENCES |
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