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1 Laboratory of Microbiology, Faculty of Fisheries Sciences, Hokkaido University, 3-1-1 Minato-cho, Hakodate 041, Japan
2 National Research Institute of Fisheries Science, 6-31-1 Nagai, Yokosuka, Kanagawa 238-0316, Japan
Correspondence
Tomoo Sawabe
sawabe{at}fish.hokudai.ac.jp
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ABSTRACT |
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The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA gene sequences of six V. comitans strains, two V. inusitatus strains and V. rarus RW22T are respectively DQ922914–DQ922919, DQ922920–DQ922921 and DQ914239. Those of the gapA gene sequences of five V. comitans strains, V. inusitatus RW14T and V. rarus RW22T are respectively DQ922906–DQ922910, DQ922911 and DQ922913.
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MAIN TEXT |
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TOPABSTRACTMAIN TEXTREFERENCES |
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; Sawabe et al., 1998, 2004a, b; Sawabe, 2006). The unique characteristics of the V. halioticoli-related species are that they are alginolytic, non-motile, fermentative marine bacteria. In addition, these bacteria shared similar ecological niches in the gut of Haliotis abalones all over the world. V. halioticoli, V. neonatus and V. ezurae are abundant in Japanese (Sawabe et al., 1995, 2002, 2003, 2004b) and South African (Sawabe et al., 2003) abalone, whereas V. gallicus and V. superstes are found in French (Sawabe et al., 2004a) and Australian (Hayashi et al., 2003) abalone. High genetic diversity of V. halioticoli was observed in several abalone species (Sawabe et al., 2002; Sawabe, 2006). These bacteria are thought to be involved in digestion of the polysaccharide of kelps ingested by the abalone. These bacteria are also active in making volatile, short-chain fatty acids, mainly acetic acid and formic acid, via fermentation (Sawabe et al., 2003).
The observed genetic diversity of V. halioticoli-related species is attributed to the ‘co-evolution concept’, in which a long symbiotic relationship has been established between the V. halioticoli-related species and the host abalones (Sawabe, 2006). To understand the driving force of the genetic diversity and speciation of V. halioticoli-related species, it is important to attempt to isolate novel V. halioticoli-related species. In this study, we isolated nine strains that were phylogenetically most similar to V. superstes from the gut of warm-water-adapted wild Japanese abalones (Haliotis discus discus, H. gigantea and H. madaka) and the Californian red abalone (Haliotis rufescens). DNA–DNA hybridization experiments, phenotypic characterizations and phylogenetic and genetic analyses demonstrated that these strains represent three as-yet unknown species of Vibrio.
Six strains, GHD1-9 (=LMG 23413=NBRC 102078), GHG2-1T (=LMG 23416T=NBRC 102076T), GHG2-4 (=LMG 23417=NBRC 102077), NHG1-3 (=LMG 23421=NBRC 102080), NHG1-11 (=LMG 23422=NBRC 102079) and NHM1-4 (=LMG 23425=NBRC 102081), were isolated from the guts of wild-caught Japanese abalones H. discus discus, H. gigantea and H. madaka. These animals were collected on the coast of Goto Island (Nagasaki Prefecture, Japan) and Nagai (Kanagawa Prefecture, Japan) by scuba-diving in May and July 2005, respectively, with the permission of the local fishery management. From two, three and three individual animals, heterotrophic bacteria were grown on ZoBell 2216E agar containing 0.5 % sodium alginate at 20 °C according to Sawabe et al. (1995). Among 30 randomly selected bacterial colonies from each animal sample, V. halioticoli-like strains showing facultatively anaerobic, non-motile, alginolytic and Gram-negative rods (Sawabe et al., 1998) were retained for this experiment. Except for strain pairs GHG2-1T and GHG2-4 and NHG1-3 and NHG1-11, strains were not from same individual.
Strains RW22T (=LMG 23674T=NBRC 102084T), RW14T (=LMG 23434T=NBRC 102082T) and RW21 (=LMG 23673=NBRC 102083) were isolated and selected from the gut of one individual of the Californian red abalone, H. rufescens. This animal was purchased from The Abalone Farm (Cayucos, CA, USA) in July 2005. Strains were cultured on ZoBell 2216E agar containing 0.5 % alginate (Oppenheimer & ZoBell, 1952) and stored at –80 °C in 10 % glycerol.
16S rRNA gene sequences (1400 bp) of the nine strains were determined according to Sawabe et al. (1998) using four sequencing primers (24F, 1100F, 920R and 1540R) by means of a RISA384 DNA sequencer (Shimadzu). The 16S rRNA gene sequences of the novel strains were subjected to a BLAST search against the latest release of GenBank and related sequences were retained. Finally, 16S rRNA gene sequences of V. superstes G3-29T, V. halioticoli IAM 14596T, V. neonatus HDD3-1T, V. ezurae HDS1-1T, V. gallicus CIP 107863T, Vibrio agarivorans 289T, Vibrio wodanis NVI 88/441T, Vibrio logei ATCC 15832T and Vibrio salmonicida NCMB 2262T were included in the phylogenetic analysis as related sequences (Fig. 1a). Phylogenetic trees were constructed using three different methods [neighbour joining (NJ), maximum likelihood (ML) and maximum parsimony (MP)] according to Sawabe et al. (2004b) (details of the phylogenetic analysis are available at http://bioinfo.unice.fr/). For the NJ analysis, distance matrices were calculated using Kimura's two-parameter correction in MEGA version 3.0 (Kumar et al., 2004). ML and MP analysis were conducted by using PHYLIP version 3.573c (Felsenstein, 1993). Because of the close relationships, almost the entire sequence corresponding to positions 4–1474 of strain GHG2-1T was used for the analysis (a short insertion in the sequences of the novel strains between positions 27–31 and 42–48 of strain GHG2-1T was excluded from the analysis). The trees in Fig. 1 correspond to subsets of the final trees obtained using 100 bootstrap replications and the NJ method. Nodes supported by ML and MP analysis are also displayed in Fig. 1.
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). The gapA genes of the nine strains were sequenced according to Sawabe et al. (2004b). A phylogenetic tree was constructed in the same way as the 16S rRNA gene tree. Positions 9–703 of the gapA gene of strain GHG2-1T were used for the phylogenetic analysis. Sequences of V. halioticoli IAM 14596T, V. neonatus HDD3-1T, V. ezurae HDS1-1T, V. agarivorans LMG 21448 and V. superstes G3-29T were included (Fig. 1b
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The results of our phylogenetic analysis based on the 16S rRNA gene clearly showed that the strains belong to the gamma-3 subgroup of the phylum Proteobacteria (Garrity & Holt, 2001). The closest phylogenetic neighbour of the nine abalone strains is V. superstes G3-29T (Fig. 1a). Strains GHG1-9, GHG2-1T, GHG2-4, NHG1-3, NHG1-11 and NHM1-4 (Vibrio comitans sp. nov.) had high levels of 16S rRNA gene sequence similarity to each other, above 99.9 %, and 99.3–99.5 % similarity towards V. superstes G3-29T. Strain RW22T (Vibrio rarus sp. nov.) had 99.6–99.7 % similarity towards the six strains of the first group, 98.9–99.0 % similarity to strains RW14T and RW21 and 98.6 % similarity to V. superstes G3-29T. Finally, strains RW14T and RW21 (Vibrio inusitatus sp. nov.) shared over 99.9 % similarity and showed 99.0 % similarity towards the six strains of the first group and 98.7 % similarity to V. superstes G3-29T. Similarity levels below 98.5 % were found with other Vibrio species.
Phylogenetic analysis of the gapA gene revealed robust clades of the six strains of V. comitans sp. nov. and the two strains of V. inusitatus sp. nov. (Fig. 1b). Both clades were supported by all three phylogenetic analysis methods with 100 % bootstrap values in NJ. The closest phylogenetic neighbour of the two clades was V. superstes G3-29T. V. rarus sp. nov. was clustered with V. halioticoli, V. neonatus and V. ezurae (Fig. 1b). The six strains of V. comitans sp. nov. had 99.4–99.9 % intraspecies gapA gene sequence similarity and 94.6–94.8 % similarity towards the strains of V. inusitatus sp. nov. V. rarus RW22T had 93.3 % similarity towards V. neonatus HDD3-1T and V. ezurae HDS1-1T and 93.4 % similarity towards V. halioticoli IAM 14596T. Similarity levels below 93 % were found with other Vibrio species.
DNAs of bacterial strains were prepared by the procedures of Marmur (1961) with minor modifications. G+C content of the DNA was determined by HPLC (Tamaoka & Komagata, 1984). DNA–DNA hybridization experiments were performed in microdilution wells using a fluorometric direct-binding method described previously by Ezaki et al. (1988, 1989). DNA–DNA relatedness data are shown as mean values of triplicate experiments.
Mutual DNA–DNA hybridization experiments showed that three representative strains of V. comitans sp. nov., GHG2-1T, NHG1-11 and NHM1-4, were conspecific strains clearly apart from the strains of V. inusitatus sp. nov. and V. rarus sp. nov., V. superstes and the other phylogenetic neighbours (Table 1). Strain RW22T and the two strains RW14T and RW21 also represented distinct species separate from V. superstes and V. halioticoli (Table 1).
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; Hidaka & Sakai, 1968; Holt et al., 1994; Leifson, 1963; Ostle & Holt, 1982; West et al., 1977). Carbon assimilation tests were conducted by using basal seawater medium (Baumann et al., 1984) using a method reported previously (Sawabe et al., 1998, 2004b). These phenotypic characterizations were done at 20 °C.
The nine abalone strains have the main phenotypic features of the genus Vibrio (except for the absence of flagella). The strains are non-motile, Gram-negative and fermentative (Sawabe et al., 1998). No flagellated cells were observed. The strains required salt for growth and were oxidase-positive (Table 2). No peritrichous cells were observed when the strains were cultivated on solid media. Other phenotypic features of the novel strains are shown in Table 2. The six abalone isolates of V. comitans sp. nov. and two isolates of V. inusitatus sp. nov. were phenotypically most similar to each other, although the strains differed in four traits (assimilation of D-mannose, D-sorbitol, D-galactose and D-glucuronate) out of 81 tested (Table 2). V. rarus sp. nov. was phenotypically most similar to V. inusitatus sp. nov. V. rarus and V. inusitatus differed in six traits (growth at 4 °C, indole production, growth in 1 % NaCl, requirement for organic growth factors and assimilation of sucrose and D-fructose) (Table 2). Growth at 4 °C, indole production and a combination of carbon sources are required to differentiate the V. halioticoli-related species (Table 2).
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). Phenotypic traits of V. comitans, V. rarus and V. inusitatus are likely to be similar (Table 2).
Recently, the presence of a radula was reported in the soft-bodied mollusc fossil Odontogrophus omalus found in Middle-Cambrian Burgess shale (Caron et al., 2006). It is speculated that scraping feeding behaviour on cyanobacterial encrustations using the radula might have started 500 million years ago (Caron et al., 2006). Scraping feeding behaviour is one of the physiological characteristics of abalone, especially in newly hatched juveniles. It is interesting to trace back the evolution of the gut vibrios of scraping feeding abalone with respect to the ‘co-evolution concept’. Further genetic analysis by multilocus sequence analysis or genome analysis among the abalone gut vibrios might reveal unique evolutionary histories of vibrios associated with these molluscs.
In conclusion, our polyphasic study clearly demonstrated that the nine abalone isolates represent three novel species of the genus Vibrio, for which we propose the names Vibrio comitans sp. nov., Vibrio rarus sp. nov. and Vibrio inusitatus sp. nov. These novel Vibrio species are described from limited resources of abalone from various parts of the world.
Description of Vibrio comitans sp. nov.
Vibrio comitans (co'mi.tans. L. part. adj. comitans accompanying).
Gram-negative, facultatively anaerobic, non-motile and non-flagellated. Cells in ZoBell 2216E broth are rod-shaped, with rounded ends (0.5–1.0x1.2–2.0 µm). No endospores or capsules are formed. Flagellation is not observed when the organism is cultivated on solidified medium or in liquid medium. Colonies on ZoBell 2216E agar are beige, circular, smooth and convex with an entire edge. Sodium ions are essential for growth. Mesophilic and neutrophilic chemo-organotroph that grows at 4–30 °C. No growth above 37 °C. Growth occurs on thiosulfate/citrate/bile salts/sucrose (TCBS) agar (green colonies). Positive for acid production from D-glucose, D-mannitol and maltose, nitrate reduction, hydrolysis of alginate, oxidase, catalase and assimilation of D-gluconate, D-galactose, cellobiose, D-glucuronate, pyruvate, L-glutamate, D-fructose, D-glucose, maltose, D-xylose, D-mannitol, D-glucosamine, N-acetylglucosamine, fumarate and succinate. The following tests are negative: gas production from glucose, acetoin production, lysine decarboxylase, arginine dihydrolase, ornithine decarboxylase, indole production, luminescence, pigmentation, requirement for organic growth factors, 
-galactosidase test, hydrolysis of starch, gelatin, chitin, Tween 80 and agar, acid production from L-arabinose, inositol, L-rhamnose, sucrose and D-sorbitol and assimilation of D-mannose, sucrose, D-sorbitol, 2-oxoglutarate, melibiose, lactose, trehalose, putrescine, acetate, L-tyrosine, propionate, L-proline, meso-erythritol, DL-malate and aconitate. The G+C content of the DNA is 45.0–48.0 mol%.
The type strain is GHG2-1T (=LMG 23416T=NBRC 102076T). The type strain and five reference strains [GHD1-9 (=LMG 23413=NBRC 102078), GHG2-4 (=LMG 23417=NBRC 102077), NHG1-3 (=LMG 23421=NBRC 102080), NHG1-11 (=LMG 23422=NBRC 102079) and NHM1-4 (=LMG 23425=NBRC 102081)] were isolated from the guts of wild-caught abalone (H. discus discus, H. gigantea and H. madaka).
Description of Vibrio rarus sp. nov.
Vibrio rarus (ra'rus. L. masc. adj. rarus few, scarce, rare).
Gram-negative, facultatively anaerobic, non-motile and non-flagellated. Cells in ZoBell 2216E broth are rod-shaped, with rounded ends (0.5–1.0x1.0–2.0 µm). No endospores or capsules are formed. Flagellation is not observed when the organism is cultivated on solidified medium or in liquid medium. Colonies on ZoBell 2216E agar are beige, circular, smooth and convex with an entire edge. Sodium ions are essential for growth. Mesophilic and neutrophilic chemo-organotroph that grows at 15–30 °C. No growth above 37 °C. Growth occurs on TCBS agar (green colonies). Positive for acid production from D-glucose, D-mannitol and maltose, nitrate reduction, indole production, hydrolysis of alginate, oxidase, catalase, requirement for organic growth factors and assimilation of D-mannose, sucrose, D-gluconate, cellobiose, D-sorbitol, acetate, pyruvate, L-glutamate, L-proline, D-glucose, maltose, D-xylose, D-mannitol, D-glucosamine, N-acetylglucosamine, fumarate and succinate. The following tests are negative: gas production from glucose, acetoin production, lysine decarboxylase, arginine dihydrolase, ornithine decarboxylase, luminescence, pigmentation, -galactosidase test, hydrolysis of starch, gelatin, chitin, Tween 80, agar and DNA, acid production from L-arabinose, inositol, L-rhamnose, sucrose and L-sorbitol and assimilation of glycerol, 2-oxoglutarate, D-galactose, melibiose, lactose, D-glucuronate, trehalose, putrescine, 
-aminobutyrate, L-tyrosine, propionate, D-fructose, citrate, meso-erythritol, DL-malate and aconitate. The G+C content of the DNA is 43.8 mol%.
The type strain RW22T (=LMG 23674T=NBRC 102084T) was isolated from the gut of the Californian red abalone, H. rufescens.
Description of Vibrio inusitatus sp. nov.
Vibrio inusitatus (i.nu.si.ta'tus. L. masc. adj. inusitatus unusual, uncommon).
Gram-negative, facultatively anaerobic, non-motile and non-flagellated. Cells in ZoBell 2216E broth are rod-shaped, with rounded ends (0.5–1.0x1.0–2.0 µm). No endospores or capsules are formed. Flagellation is not observed when the organism is cultivated on solidified medium or in liquid medium. Colonies on ZoBell 2216E agar are beige, circular, smooth and convex with an entire edge. Sodium ions are essential for growth. Mesophilic and neutrophilic chemo-organotroph that grows at 4–30 °C. No growth above 37 °C. Growth occurs on TCBS agar (green colonies). Positive for acid production from D-glucose, D-mannitol and maltose, nitrate reduction, hydrolysis of alginate, oxidase, catalase and assimilation of D-mannose, cellobiose, D-fructose, D-glucose, maltose, D-mannitol, N-acetylglucosamine, fumarate, succinate, D-xylose and L-glutamate. The following tests are negative: gas production from glucose, acetoin production, lysine decarboxylase, arginine dihydrolase, ornithine decarboxylase, indole production, luminescence, pigmentation, requirement for organic growth factors, -galactosidase test, hydrolysis of starch, gelatin, chitin, Tween 80 and agar, acid production from L-arabinose, inositol, L-rhamnose, sucrose and D-sorbitol and assimilation of sucrose, D-sorbitol, glycerol, 2-oxoglutarate, D-galactose, melibiose, lactose, D-glucuronate, trehalose, putrescine, acetate, L-tyrosine, L-proline, propionate, meso-erythritol, citrate, DL-malate and aconitate. The G+C content of the DNA is 43.1–43.7 mol%.
The type strain RW14T (=LMG 23434T=NBRC 102082T) and reference strain RW21 (=LMG 23673=NBRC 102083) were isolated from the gut of the Californian red abalone, H. rufescens.
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ACKNOWLEDGEMENTS |
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REFERENCES |
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TOPABSTRACTMAIN TEXTREFERENCES |
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