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1 Institute of Biotechnology, Vietnamese Academy of Science and Technology, Hanoi, Vietnam
2 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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99.6 % similarity with each other. Strain BL78T exhibited 90.5 % similarity to B. plebeius JCM 12973T and 89.8 % similarity to B. coprocola JCM 12979T and differed from the above group of five strains at 10 % sequence divergence. Strains C35T and C43 were related most closely to Bacteroides eggerthii JCM 12986T, with 95.1 % sequence similarity, to Bacteroides stercoris JCM 9496T, with 94.6 % similarity, and to Bacteroides uniformis JCM 5828T, with 94.4 % similarity, and shared 100 % similarity with each other. From results of phenotypic examination, cellular fatty acid composition analysis, menaquinone composition analysis and DNA G+C contents, the group of five strains as well as strain BL78T were shown to differ from the type strains of B. coprocola and B. plebeius. Strain BL78T differed from the others based on its menaquinone composition, which included MK-11 and MK-12. Strains C35T and C43 could also be differentiated from the type strains of B. eggerthii, B. stercoris and B. uniformis. The group of five strains, strain BL78T, B. coprocola JCM 12979T and B. plebeius JCM 12973T showed low levels of DNA–DNA relatedness (<35 %) with each other. High levels of DNA–DNA relatedness were obtained within the group of five strains (>75 %). Strains C35T and C43 exhibited a high level of DNA–DNA relatedness (>88 %) with each other, but low levels with B. eggerthii JCM 12986T (<40 %), B. stercoris JCM 9496T (<37 %) and B. uniformis JCM 5828T (<16 %). On the basis of these data, three novel Bacteroides species are proposed: Bacteroides barnesiae sp. nov. (type strain BL2T=JCM 13652T=DSM 18169T), Bacteroides salanitronis sp. nov. (type strain BL78T=JCM 13657T=DSM 18170T) and Bacteroides gallinarum sp. nov. (type strain C35T=JCM 13658T=DSM 18171T).
Tables giving the phenotypic characteristics, cellular fatty acid compositions and menaquinone compositions of the novel strains and related Bacteroides species are available as supplementary material in IJSEM Online.
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; Salanitro et al., 1974a, b). However, relatively few Bacteroides species have been isolated from chicken intestine. Bacteroides species are thought to play a fundamental role in the breakdown of complex molecules (such as polysaccharides) into simpler compounds that are used by the animal host as well as the micro-organisms themselves (Reeves et al., 1997; Degnan et al., 1997), in the utilization of nitrogenous substances and in the biotransformation of bile acids and other steroids (Hentges, 1989). Aside from their metabolic activities, Bacteroides species and other anaerobic bacteria provide an additional benefit to their host by preventing colonization of the intestine by pathogenic micro-organisms (van der Waaij et al., 1971; Hentges, 1983). Thus, these organisms generally have a beneficial relationship with their host as long as they are retained in the gut. During a study of the composition and functional role of Bacteroides species from chicken intestine, we identified a cluster of organisms separated from recognized Bacteroides species, and which includes eight Bacteroides-like strains, designated BL2T, BL66, EG3, EG6, M27, BL78T, C35T and C43. Here we describe the taxonomic characteristics of these strains and propose the creation of three novel Bacteroides species.
Eight strains (BL2T, BL66, EG3, EG6, M27, BL78T, C35T and C43) were isolated from the caecum of a healthy chicken. Isolation of strictly anaerobic bacteria was performed according to a standard anaerobic technique in our laboratory (Mitsuoka et al., 1969; Lan et al., 2002). The isolated strains were maintained on Eggerth Gagnon (EG) agar (Merck) supplemented with 5 % (v/v) horse blood for 2 days at 37 °C in an anaerobic jar (Hirayama Manufacturing Corp.) filled with 100 % CO2. Strains BL2T, BL66 and BL78T were isolated on BL agar (Nissui Pharmaceutical Co., Ltd). Strains EG3 and EG6 were isolated on EG agar. Strains M27, C35T and C43 were isolated on medium 10 (Caldwell & Bryant, 1966) by using the ‘plate-in-bottle’ procedure (Mitsuoka et al., 1969).
Physiological and biochemical characteristics were determined by using an API 20A anaerobic test kit and API Rapid ID 32A enzymic tests in duplicate as recommended by the manufacturer (bioMérieux). Bile resistance was tested by growing the bacteria on Bacteroides bile aesculin agar plates (Shah, 1992). Fermentation metabolic end products were prepared as described by Holdeman et al. (1977) and analysed as described previously (Sakamoto et al., 2004, 2005). 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 using the MIDI microbial identification system (Microbial ID). Isoprenoid quinones were extracted as described by Komagata & Suzuki (1987) and analysed as described previously (Sakamoto et al., 2004, 2005). Chromosomal DNA was isolated by using the methods of Marmur (1961) and Saito & Miura (1963), with some modifications. The DNA G+C content was determined by using the HPLC method of Tamaoka & Komagata (1984), again with some modifications. DNA–DNA hybridization experiments were carried out in microplate wells, as described by Ezaki et al. (1989). Hybridization was performed at 44 °C for 16 h. 16S rRNA gene sequences were obtained and analysed as described previously (Lan et al., 2002; Sakamoto et al., 2002). Reference 16S rRNA gene sequences used for comparisons in this study were retrieved from the DDBJ, EMBL and GenBank nucleotide sequence databases. Sequence data 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 based on the neighbour-joining method (Saitou & Nei, 1987). Bootstrap resampling analysis (Felsenstein, 1985) was performed to estimate the confidence of tree topologies.
Cells of the eight isolates investigated were obligately anaerobic, non-spore-forming, non-motile, Gram-negative pleomorphic rods. On EG agar, cells of strains BL2T, BL66, EG3, EG6 and M27 were 0.5–1.4x0.8–10.6 µm, cells of strain BL78T were 0.4–0.7x0.8–5.6 µm and cells of strains C35T and C43 were 0.4–0.6x0.8–6.5 µm. Cells of all eight strains occurred either singly or in pairs. Colonies of all eight strains were white–greyish. Colonies of strains BL2T, BL66, EG3, EG6 and M27 on EG agar were 1.5–3.0 mm in diameter, circular, raised, convex and smooth. Colonies of strain BL78T on EG agar were 2.0–3.0 mm in diameter, rounded and smooth, and colonies of strains C35T and C43 on EG agar were 1.0–1.5 mm in diameter, polished and circular. All eight strains were able to hydrolyse aesculin on Bacteroides bile aesculin agar. The results of phenotypic tests are given in the species descriptions below. Phenotypic characteristics of the test strains and the type strains of related Bacteroides species are given in Supplementary Table S1 available in IJSEM Online. From the API 20A tests, five strains (BL2T, BL66, EG3, EG6 and M27) exhibited identical sugar fermentation patterns; these strains could be differentiated from Bacteroides coprocola JCM 12979T by their inability to ferment L-rhamnose and could be distinguished from bacteroides plebeius jcm 12973t by their ability to ferment salicin and inability to ferment L-arabinose or L-rhamnose. Strain BL78T could be differentiated from B. coprocola JCM 12979T by its ability to ferment L-arabinose and from B. plebeius JCM 12973T by its ability to ferment salicin. Strains C35T and C43 could be differentiated from Bacteroides eggerthii JCM 12986T by their ability to ferment sucrose and D-raffinose, from Bacteroides stercoris JCM 9496T by their ability to ferment L-arabinose and D-cellobiose and from bacteroides uniformis jcm 5828t by their ability to ferment L-rhamnose and inability to ferment salicin. From the API rapid ID 32A tests, the group of five strains differed from B. coprocola JCM 12979T in that they were negative for 
-galactosidase 6-phosphate and glutamic acid decarboxylase. These five strains differed from B. plebeius JCM 12973T based on the absence of activities for -galactosidase 6-phosphate, -glucuronidase, glutamic acid decarboxylase and arginine, phenylalanine, leucine, glycine and histidine arylamidases. The enzymic pattern of strain BL78T differed from that of B. coprocola JCM 12979T in that it was negative for -galactosidase 6-phosphate, N-acetyl--glucosaminidase, glutamic acid decarboxylase and 
-fucosidase. The enzymic pattern of strain BL78T differed distinctively from that of B. plebeius JCM 12973T in that it was negative for -galactosidase 6-phosphate, -glucuronidase, N-acetyl--glucosaminidase, glutamic acid decarboxylase, -fucosidase and arginine, phenylalanine, leucine, glycine and histidine arylamidases. Isolates C35T and C43 could be differentiated from B. eggerthii JCM 12986T by their activity for glutamic acid decarboxylase and raffinose fermentation, from B. stercoris JCM 9496T by activity for -arabinosidase and glutamic acid decarboxylase and lack of activity for -fucosidase and from B. uniformis JCM 5828T by lack of activity for -galactosidase, -galactosidase 6-phosphate and -fucosidase. Differential characteristics between the novel strains and the type strains of related Bacteroides species are summarized in Table 1.
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; Miyagawa et al., 1979; Shah & Collins, 1980) and was reviewed for the classification of the genus Bacteroides by Shah & Collins (1983). In the present study, the major cellular fatty acids of five strains (BL2T, BL66, EG3, EG6 and M27) included anteiso-C15 : 0, iso-C15 : 0, C16 : 0 3-OH and C16 : 0. The major cellular fatty acids of strain BL78T were anteiso-C15 : 0, iso-C15 : 0, C16 : 0 3-OH and iso-C17 : 0 3-OH. The major cellular fatty acids of strains C35T and C43 were anteiso-C15 : 0, iso-C15 : 0 and iso-C17 : 0 3-OH. Strains C35T and C43 showed slightly higher levels of anteiso-C15 : 0 (37.1 and 38.4 %, respectively) than B. eggerthii JCM 12986T (33 %), B. stercoris JCM 9496T (30 %) and B. uniformis JCM 5828T (33 %). The cellular fatty acid compositions of the novel strains and of the type strains of related Bacteroides species are given in Supplementary Table S2 in IJSEM Online.
Isoprenoid quinones (principally menaquinones and ubiquinones) are important in the functioning of respiratory electron transport systems. The usefulness of quinone analysis for bacterial classification and identification has been reviewed by Collins & Jones (1981). The major menaquinones of members of the genus Bacteroides are MK-10 and MK-11 (Shah, 1992). Indeed, five of the studied strains (BL2T, BL66, EG3, EG6 and M27) and two related Bacteroides species (B. coprocola JCM 12979T and B. plebeius JCM 12973T) possess a high level of MK-10 (58–67 %) and MK-11 (25–34 %). However, strain BL78T exhibited MK-11 (43 %) and MK-12 (43 %) as the main components (see Supplementary Table S3 in IJSEM Online). Strains C35T and C43 and three reference type strains (B. eggerthii JCM 12986T, B. stercoris JCM 9496T and B. uniformis JCM 5828T) also possess MK-10 and MK-11 as the major menaquinones.
Approximately 1500 bases of the 16S rRNA gene sequence were determined for each of the eight new isolates. For the phylogenetic analysis, 1338 bp sequences (positions 61–1375 of the Escherichia coli numbering system) of each organism were used. Five strains (BL2T, BL66, EG3, EG6 and M27) were found to be genetically closely related to each other, with 99.6 % 16S rRNA gene sequence similarity, and created a separate branch; these five strains differed from strain BL78T with 10 % sequence divergence. Strain BL78T and the group of five strains comprised a new subcluster, which displayed the closest phylogenetic relationship with the subcluster of B. plebeius JCM 12973T and B. coprocola JCM 12979T. Tree-making analysis clearly showed that these six strains represent a new subcluster within the genus Bacteroides and that five of the isolates, BL2T, BL66, EG3, EG6 and M27, represented the same species (as supported by the DNA–DNA hybridization data below). Strains C35T and C43 were genetically closely related to each other (100 % sequence similarity) and formed a subline separate from those of related recognized species. They exhibited 95.1 % similarity to B. eggerthii JCM 12986T as the closest related recognized species, 94.6 % to B. stercoris JCM 9496T and 94.4 % to B. uniformis JCM 5828T. Although strains C35T and C43 were most closely related to B. eggerthii, they formed a subcluster with B. stercoris within the cluster with B. eggerthii and B. uniformis. The phylogenetic positions of strains BL2T, BL78T and C35T are shown in Fig. 1.
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On the basis of the data presented here we propose the creation of three novel Bacteroides species: Bacteroides barnesiae sp. nov., Bacteroides salanitronis sp. nov. and Bacteroides gallinarum sp. nov. Differential characteristics of these three species and of related Bacteroides species are shown in Table 1
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Description of Bacteroides barnesiae sp. nov.
Bacteroides barnesiae (barne'si.ae. N.L. gen. fem. n. barnesiae of Barnes, named after Ella M. Barnes, a British microbiologist, who has contributed much to our knowledge of intestinal bacteriology and anaerobic bacteriology in general).
Cells are strictly anaerobic, non-spore-forming, non-motile, Gram-negative, pleomorphic rods, 0.5–1.4 µm wide and 0.8–10.6 µm long, which occur singly or in pairs. Surface colonies on EG blood agar plates after 2 days are 1.5–3.0 mm in diameter, white-greyish, circular, raised and convex. Optimum growth temperature is 37 °C. Grows in the presence of bile. Indole is not produced. Catalase- and urease-negative. Nitrate is not reduced to nitrite. Gelatin is not liquefied. Aesculin is hydrolysed. Using the API 20A system, produces acid from glucose, lactose, sucrose, maltose, salicin, D-xylose, D-cellobiose, D-mannose and D-raffinose, but not from D-mannitol, L-arabinose, glycerol, D-melezitose, D-sorbitol, L-rhamnose or D-trehalose. Using the rapid ID 32A system, positive reactions are obtained for -galactosidase, -galactosidase, -glucosidase, -glucosidase, -arabinosidase, N-acetyl--glucosaminidase, -fucosidase, alkaline phosphatase, leucyl glycine arylamidase, alanine arylamidase and glutamyl glutamic acid arylamidase. Negative reactions are obtained for L-arginine dihydrolase, -galactosidase 6-phosphate, -glucuronidase, glutamic acid decarboxylase and arginine, proline, phenylalanine, leucine, pyroglutamic acid, tyrosine, glycine, histidine and serine arylamidases. The major end products [from 1 % (w/v) peptone/1 % (w/v) yeast extract/1 % (w/v) glucose broth culture] are succinic and acetic acids; small amounts of isovaleric acid are also produced. The major cellular fatty acid is anteiso-C15 : 0 (23–32 % of the total). Significant amounts of iso-C15 : 0 (10–15 %), C16 : 0 (10–15 %) and C16 : 0 3-OH (10–14 %) are also present. The principal respiratory quinones are menaquinones MK-10 (58–67 %) and MK-11 (25–34 %). Menaquinone MK-9 (2–3 %) is present as a minor component. The DNA G+C content of the type strain is 46.8 mol%.
The type strain, BL2T (=JCM 13652T=DSM 18169T), was isolated from caecum of a healthy chicken. Four additional strains [BL66 (=JCM 13653), EG3 (=JCM 13654), EG6 (=JCM 13655) and M27 (=JCM 13656)] are included in the description.
Description of Bacteroides salanitronis sp. nov.
Bacteroides salanitronis (sa.la.ni.tro'nis. N.L. gen. masc. n. salanitronis of Salanitro, named after Joseph P. Salanitro, an American microbiologist, who has contributed much to our knowledge of intestinal bacteriology in chicken and anaerobic bacteriology in general).
Cells are strictly anaerobic, non-spore-forming, non-motile, Gram-negative rods, 0.4–0.7 µm wide and 0.8–5.6 µm long, which occur singly or in pairs. Surface colonies on EG blood agar plates after 2 days are 2.0–3.0 mm in diameter, white-greyish, rounded and smooth. Optimum growth temperature is 37 °C. Grows in the presence of bile. Indole is not produced. Catalase- and urease-negative. Nitrate is not reduced to nitrite. Gelatin is not liquefied. Aesculin is hydrolysed. Using the API 20A system, produces acid from glucose, lactose, sucrose, maltose, D-xylose, L-arabinose, D-cellobiose, D-mannose and D-raffinose, but not from D-mannitol, glycerol, D-melezitose, D-sorbitol or D-trehalose. Salicin and L-rhamnose are fermented weakly. Using the rapid ID 32A system, positive reactions are obtained for -galactosidase, -galactosidase, -glucosidase, -glucosidase, -arabinosidase, alkaline phosphatase, leucyl glycine arylamidase, alanine arylamidase and glutamyl glutamic acid arylamidase. Negative reactions are obtained for L-arginine dihydrolase, -galactosidase 6-phosphate, -glucuronidase, N-acetyl--glucosaminidase, glutamic acid decarboxylase, -fucosidase and arginine, proline, phenylalanine, leucine, pyroglutamic acid, tyrosine, glycine, histidine and serine arylamidases. The major end products [from 1 % (w/v) peptone/1 % (w/v) yeast extract/1 % (w/v) glucose broth culture] are succinic and acetic acids; a small amount of isovaleric acid is also produced. The major cellular fatty acid is anteiso-C15 : 0 (32 % of the total). Significant amounts of iso-C15 : 0 (14 %), C16 : 0 3-OH (12 %) and iso-C17 : 0 3-OH (10 %) are also present. The principal respiratory quinones are menaquinones MK-11 (43 %) and MK-12 (43 %). Menaquinones MK-10 (5 %) and MK-13 (7 %) are present as minor components. The DNA G+C content is 46.9 mol%.
The type and only strain, BL78T (=JCM 13657T=DSM 18170T), was isolated from caecum of a healthy chicken.
Description of Bacteroides gallinarum sp. nov.
Bacteroides gallinarum (gal.li.na'rum. L. gen. fem. pl. n. gallinarum from/of chickens or hens).
Cells are strictly anaerobic, non-spore-forming, non-motile, Gram-negative rods, 0.4–0.6 µm wide and 0.8–6.5 µm long, which occur singly or in pairs. Surface colonies on EG blood agar plates after 2 days are 1.0–1.5 mm in diameter, white-greyish, polished and circular. Optimum growth temperature is 37 °C. Grows well in the presence of bile and can produce indole. Catalase- and urease-negative. Nitrate is not reduced to nitrite. Gelatin is not liquefied. Aesculin is hydrolysed. Using the API 20A system, produces acid from glucose, lactose, sucrose, maltose, D-xylose, L-arabinose, D-cellobiose, D-mannose and D-raffinose, but not from D-mannitol, salicin, glycerol, D-melezitose, D-sorbitol or D-trehalose. L-Rhamnose is fermented weakly. Using the rapid ID 32A system, positive reactions are obtained for -galactosidase, -glucosidase, -glucosidase, -arabinosidase, N-acetyl--glucosaminidase, mannose and raffinose fermentation, glutamic acid decarboxylase, alkaline phosphatase, leucyl glycine arylamidase, alanine arylamidase and glutamyl glutamic acid arylamidase. Negative reactions are obtained for L-arginine dihydrolase, -galactosidase, -galactosidase 6-phosphate, -glucuronidase, -fucosidase and arginine, proline, phenylalanine, leucine, pyroglutamic acid, tyrosine, glycine, histidine and serine arylamidases. The major end products [from 1 % (w/v) peptone/1 % (w/v) yeast extract/1 % (w/v) glucose broth culture] are succinic and propionic acids; small amounts of acetic acid and isovaleric acid are also produced. The major cellular fatty acids are anteiso-C15 : 0 (37.1–38.4 % of the total) and iso-C17 : 0 3-OH (20.8–22.3 %). A significant amount of iso-C15 : 0 (10.4–10.7 %) is also present. The principal respiratory quinones are menaquinones MK-10 (37.9–38.1 %) and MK-11 (16.1–19.2 %). The DNA G+C content of the type strain is 47.0 mol%.
The type strain, C35T (=JCM 13658T=DSM 18171T), was isolated from caecum of a healthy chicken. One additional strain (C43=JCM 13659) is included in the description.
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ACKNOWLEDGEMENTS |
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REFERENCES |
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