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1 Japan Collection of Microorganisms, RIKEN, Wako, Saitama 351-0198, Japan
2 Biological Resource Center, Department of Biotechnology, National Institute of Technology and Evaluation, Kisarazu, Chiba 292-0818, Japan
3 Division of Periodontology, Department of Hard Tissue Engineering, Graduate School, Tokyo Medical and Dental University, Bunkyo-ku, Tokyo 113-8549, Japan
Correspondence
Mitsuo Sakamoto
sakamoto{at}jcm.riken.jp
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ABSTRACT |
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9c, C16 : 0 and C16 : 0 3-OH, whereas other Prevotella species, except for P. loescheii JCM 8530T, possess anteiso-C15 : 0, iso-C17 : 0 3-OH and C18 : 19c. The predominant fatty acids in P. loescheii JCM 8530T are anteiso-C15 : 0, C16 : 0 and C18 : 19c. DNA–DNA hybridization experiments revealed a genomic distinction of strains EHS11T and EPSA11T from P. loescheii JCM 8530T and P. oris JCM 8540T. On the basis of these data, two novel Prevotella species are proposed: Prevotella shahii sp. nov. and Prevotella salivae sp. nov. The type strains of P. shahii and P. salivae are EHS11T (=JCM 12083T=DSM 15611T) and EPSA11T (=JCM 12084T=DSM 15606T), respectively.
Published online ahead of print on 12 December 2003 as DOI 10.1099/ijs.0.02876-0.
The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA gene sequences reported in this paper are AB108825 (Prevotella shahii EHS11T) and AB108826 (Prevotella salivae EPSA11T).
Tables of phenotypic characteristics and levels of DNA relatedness, and a phylogenetic tree, are available as supplementary material in IJSEM Online.
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MAIN TEXT |
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TOPABSTRACTMAIN TEXTREFERENCES |
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) and the Approved Lists of Bacterial Names (Moore et al., 1985). Subsequently, Shah & Collins (1989) formally proposed that the genus Bacteroides be restricted to Bacteroides fragilis and related taxa, and the description of the genus Bacteroides was emended accordingly. Two genera, Porphyromonas (Shah & Collins, 1988) for the ‘asaccharolytic pigmented Bacteroides species’, and Prevotella (Shah & Collins, 1990) for the ‘moderately saccharolytic, predominantly oral Bacteroides species’, were thus created. More recently, a novel genus, Tannerella, was proposed for the important periodontal pathogen Bacteroides forsythus (Sakamoto et al., 2002a). During the study of novel oral phylotypes associated with periodontitis (Sakamoto et al., 2002b), we isolated two strains from the human oral cavity that were obligately anaerobic, non-pigmented, non-spore-forming, non-motile, Gram-negative rods. These isolates were related phenotypically to the genus Prevotella. Prevotella species are mainly isolated from the oral cavity and some species are associated with periodontitis. No novel Prevotella species have been proposed since Könönen et al. (1998) described Prevotella pallens. The present study was designed to determine the taxonomic status of these two isolates. On the basis of the results presented here, we propose that these strains should be classified as two novel species of the genus Prevotella, namely Prevotella shahii sp. nov. and Prevotella salivae sp. nov.
The strains used in the present 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 that contained 100 % CO2. Strain EHS11T was isolated on EG agar from the saliva of a periodontally healthy subject. Strain EPSA11T was isolated, also on EG agar, from the saliva of a patient with chronic periodontitis. Bacteroides bile aesculin agar (Shah, 1992) was used to check whether growth of the isolates was inhibited on this medium.
Physiological reactions were determined with an API 20A anaerobic test kit in duplicate, as recommended by the manufacturer (bioMérieux). Metabolic end-products were prepared as described previously (Holdeman et al., 1977) and were analysed by GLC (GC-7A; Shimadzu), using a 2·1 m glass column (2·8 mm, FAL-M 25 %, Chrommosorb W, 80/100 mesh, AW-DMCS H3PO4; Shimadzu). Fatty acid methyl esters 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 the MIDI microbial identification system (Microbial ID). Isoprenoid quinones were extracted as described by Komagata & Suzuki (1987) and were analysed by HPLC with a Cosmosil 5C18 column (4·6x150 mm; Nacalai Tesque). Glucose-6-phosphate dehydrogenase (G6PDH), 6-phosphogluconate dehydrogenase (6PGDH), malate dehydrogenase (MDH) and glutamate dehydrogenase (GDH) activities were determined spectrophotometrically as described previously (Gharbia & Shah, 1991; Bailey & Love, 1995). API ZYM and API An-Ident enzymic substrate tests were performed in duplicate, as recommended by the manufacturer (bioMérieux). Chromosomal DNA was isolated by using previously described methods (Marmur, 1961; Saito & Miura, 1963), with some modifications. The DNA G+C content was determined by the HPLC method of Tamaoka & Komagata (1984), with some modifications. The DNA homology experiment was carried out in microplate wells as described by Ezaki et al. (1989). Hybridization was performed at 44 °C for 16 h. The 16S rRNA gene was analysed as described previously (Sakamoto et al., 2002a). Previously determined 16S rRNA gene sequences used for comparison in this study were retrieved from GenBank/EMBL. Sequence data were aligned with 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. The 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.
Strain EHS11T comprised obligately anaerobic, non-spore-forming, non-motile, Gram-negative rods. Cells on EG agar were 0·5–0·8x8·3–10·0 µm in size and occurred singly. Colonies were 1–2 mm in diameter, tan to light brown, circular, entire, slightly convex and smooth on EG agar plates. Strain EPSA11T comprised obligately anaerobic, non-spore-forming, non-motile, Gram-negative rods. Cells on EG agar were 0·5–0·8x0·8–1·7 µm in size and occurred singly. Colonies were 1–2 mm in diameter, grey to light brown, circular, entire, slightly convex and smooth on EG agar plates. Strain EPSA11T hydrolysed aesculin on Bacteroides bile aesculin agar, whereas strain EHS11T did not. In addition, Prevotella loescheii JCM 8530T, Prevotella oralis JCM 6330, Prevotella oris JCM 8540T and Prevotella veroralis JCM 6290T hydrolysed aesculin on the same agar plates. Growth of the isolates and other Prevotella species was inhibited on Bacteroides bile aesculin agar. Results of phenotypic tests are given in the species description. In addition, phenotypic characteristics of other Prevotella species are available as supplementary material in IJSEM Online. The phenotypic characteristics of strain EHS11T were similar to those of P. loescheii JCM 8530T and Prevotella melaninogenica JCM 6325T. Strain EHS11T could not be differentiated from P. melaninogenica JCM 6325T by API 20A tests. On the other hand, strain EHS11T could be differentiated from P. loescheii JCM 8530T by aesculin hydrolysis. Testing for hydrolysis of aesculin has been reported to be helpful in differentiating P. loescheii (formerly Bacteroides loescheii) from other related species, such as P. melaninogenica (formerly Bacteroides melaninogenicus) (Holdeman & Johnson, 1982). Phenotypic characteristics of strain EPSA11T were similar to those of P. oris JCM 8540T. Strain EPSA11T could be differentiated from P. oris JCM 8540T by gelatin digestion and D-rhamnose fermentation. However, Holdeman et al. (1982) reported that digestion of gelatin and fermentation of D-rhamnose varied between the type strain and 17 other strains of P. oris (formerly Bacteroides oris).
The cellular fatty acid composition of Bacteroides species has been determined (Miyagawa et al., 1979; Shah & Collins, 1980; Mayberry et al., 1982) and reviewed for classification of the genus Bacteroides (Shah & Collins, 1983). In this study, the cellular fatty acid composition of strain EPSA11T was very similar to that of P. oris JCM 8540T (Table 1). Among the strains tested, only these two strains contain C17 : 0 3-OH (3·4 %). On the other hand, the cellular fatty acid composition of strain EHS11T was significantly different from those of other Prevotella species. In strain EHS11T, the predominant cellular fatty acids are C18 : 19c, C16 : 0 and C16 : 0 3-OH, whereas other Prevotella species, except for P. loescheii JCM 8530T, possess anteiso-C15 : 0, iso-C17 : 0 3-OH and C18 : 19c. Predominant cellular fatty acids in P. loescheii JCM 8530T are anteiso-C15 : 0, C16 : 0 and C18 : 19c. P. loescheii has been reported to possess greater relative amounts of C16 : 0 (Wu et al., 1992). It has been reported that anteiso-C15 : 0, iso-C15 : 0, iso-C17 : 0 3-OH and C16 : 0 are the major cellular fatty acids in the genus Prevotella (Moore et al., 1994). According to this report, strain EHS11T might not be a member of the genus Prevotella. However, the predominant cellular fatty acids in Prevotella dentalis are C16 : 0 3-OH, C16 : 0 and iso-C14 : 0 (Willems & Collins, 1995), which differ from those of other Prevotella species, such as strain EHS11T.
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, 1983). In our study, the menaquinone composition of strain EPSA11T was very similar to that of P. oris JCM 8540T. On the other hand, the menaquinone composition of strain EHS11T was significantly different from that of P. loescheii JCM 8530T or P. melaninogenica JCM 6325T, which are related phenotypically to strain EHS11T (see supplementary material in IJSEM Online).
The dehydrogenase enzyme pattern is an important criterion that differentiates the genus Bacteroides sensu stricto from other Gram-negative, anaerobic, non-spore-forming rods (Shah & Collins, 1989; Shah, 1992). B. fragilis and related species possess enzymes of the hexose monophosphate shunt–pentose phosphate pathway, such as G6PDH, 6PGDH, MDH and GDH. Shah & Collins (1988, 1990) have proposed the novel genera Porphyromonas and Prevotella because of the lack of enzymes (G6PDH and 6PGDH). In the present study, G6PDH and 6PGDH activities were not detected in extracts of clinical isolates (EHS11T and EPSA11T) or other Prevotella species. Bailey & Love (1995) have reported that activity of neither enzyme was detected in extracts of Prevotella bivia, Prevotella corporis, Prevotella intermedia, P. loescheii, P. melaninogenica, P. oralis, P. oris or P. veroralis. Our findings are in good agreement with their report. On the other hand, both MDH and GDH activities were detected in extracts of all strains tested. Among the strains tested, P. oris JCM 8540T and strain EPSA11T exhibited minor amounts of GDH activity. Furthermore, P. bivia JCM 6331T and P. corporis JCM 8529T exhibited minor amounts of MDH activity.
The API ZYM and API An-Ident systems have been reported to be useful in the identification of oral and non-oral, Gram-negative bacteria (Slots, 1981; Laughon et al., 1982; 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). Biochemical characteristics of clinical isolates and other Prevotella species are shown in Table 2. All strains were tested by using API ZYM and API An-Ident. Biochemical characteristics of strain EHS11T were similar to those of P. loescheii JCM 8530T, P. melaninogenica JCM 6325T and P. veroralis JCM 6290T. However, strain EHS11T could be differentiated from P. loescheii JCM 8530T, P. melaninogenica JCM 6325T and P. veroralis JCM 6290T by API An-Ident tests. 
-Glucosidase, arginine and histidine aminopeptidase activities were helpful in the differentiation of these species. Biochemical characteristics of strain EPSA11T were similar to those of P. oris JCM 8540T. However, strain EPSA11T could be differentiated from P. oris JCM 8540T by 
-fucosidase (API ZYM), -glucosidase (API An-Ident) and -galactosidase (API An-Ident) activities.
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). The relatively low levels of DNA relatedness observed demonstrate the genomic distinction of strains EHS11T and EPSA11T from P. loescheii JCM 8530T, P. melaninogenica JCM 6325T and P. oris JCM 8540T (
21 %, see supplementary material in IJSEM Online).
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). Strain EHS11T was related to P. loescheii with about 95 % sequence similarity, whereas strain EPSA11T was related to P. oris, with about 94 % similarity. In addition, strain EHS11T was related to ‘Prevotella sp. B31FD’ (Paster et al., 2001), which was isolated from subgingival dental plaque, with about 98 % similarity, whereas strain EPSA11T was related to ‘Prevotella sp. oral clone DO033’ (Kazor et al., 2003), with about 99 % similarity.
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.
Description of Prevotella shahii sp. nov.
Prevotella shahii (sha'hi.i. N.L. gen. masc. n. shahii of Shah, named after the Trinidadian-born British microbiologist Haroun N. Shah, for his contributions to taxonomy of the genus Bacteroides and related taxa).
Cells are obligately anaerobic, non-spore-forming, non-motile, Gram-negative rods (0·5–0·8x8·3–10·0 µm). Colonies are 1–2 mm in diameter, tan to light brown, circular, entire, slightly convex and smooth on EG agar plates. Growth is inhibited in the presence of 20 % bile. Acid is produced from glucose, lactose, maltose, D-mannose, D-raffinose and sucrose. Acid is not produced from L-arabinose, D-cellobiose, glycerol, D-mannitol, D-melezitose, D-rhamnose, salicin, D-sorbitol, D-trehalose or D-xylose. Aesculin is not hydrolysed. Indole is not produced. Gelatin is digested. Catalase and urease are not produced. Major end products (from 1 % peptone/1 % yeast extract/1 % glucose broth cultures) are succinic and acetic acids. MDH and GDH activities are present, whereas G6PDH and 6PGDH activities are absent. Both non-hydroxylated and 3-hydroxylated long-chain fatty acids are present. Major cellular fatty acids are C18 : 19c, C16 : 0 and C16 : 0 3-OH. Principal respiratory quinones are menaquinones MK-10 (18 %), MK-11 (58 %) and MK-12 (22 %). Minor menaquinones are MK-8 (1 %) and MK-9 (1 %). DNA G+C content of the type strain is 44·3 mol%.
The type strain of P. shahii is EHS11T (=JCM 12083T=DSM 15611T), isolated from the saliva of a periodontally healthy human subject.
Description of Prevotella salivae sp. nov.
Prevotella salivae (sa.li'vae. L. fem. gen. n. salivae from/of slime, referring to the saliva from which the micro-organism was isolated).
Cells are obligately anaerobic, non-spore-forming, non-motile, Gram-negative rods (0·5–0·8x0·8–1·7 µm). Colonies are 1–2 mm in diameter, grey to light brown, circular, entire, slightly convex and smooth on EG agar plates. Growth is inhibited in the presence of 20 % bile. Acid is produced from L-arabinose, D-cellobiose, glucose, lactose, maltose, D-mannose, D-raffinose, salicin, sucrose and D-xylose. Acid is not produced from glycerol, D-mannitol, D-melezitose, D-rhamnose, D-sorbitol or D-trehalose. Aesculin is hydrolysed. Indole is not produced. Gelatin is not digested. Catalase and urease are not produced. Major end products (from 1 % peptone/1 % yeast extract/1 % glucose broth cultures) are succinic and acetic acids; small amounts of isovaleric acid are also produced. MDH is present and GDH is present in minor amounts. G6PDH and 6PGDH activities are absent. Both non-hydroxylated and 3-hydroxylated long-chain fatty acids are present. Major cellular fatty acids are anteiso-C15 : 0, iso-C17 : 0 3-OH and C18 : 19c. Predominant respiratory quinones are menaquinones MK-10 (13 %), MK-11 (67 %) and MK-12 (20 %). DNA G+C content of the type strain is 41·3 mol%.
The type strain of P. salivae is EPSA11T (=JCM 12084T=DSM 15606T), isolated from the saliva of a patient with chronic periodontitis.
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ACKNOWLEDGEMENTS |
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J. Downes, I. Sutcliffe, A. C. R. Tanner, and W. G. Wade Prevotella marshii sp. nov. and Prevotella baroniae sp. nov., isolated from the human oral cavity Int J Syst Evol Microbiol, July 1, 2005; 55(4): 1551 - 1555. [Abstract] [Full Text] [PDF]
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M. Sakamoto, Y. Huang, M. Umeda, I. Ishikawa, and Y. Benno Prevotella multiformis sp. nov., isolated from human subgingival plaque Int J Syst Evol Microbiol, March 1, 2005; 55(2): 815 - 819. [Abstract] [Full Text] [PDF]
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