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Int J Syst Evol Microbiol 53 (2003), 1813-1817; DOI  10.1099/ijs.0.02625-0
© 2003 International Union of Microbiological Societies

Vibrio superstes sp. nov., isolated from the gut of Australian abalones Haliotis laevigata and Haliotis rubra

Karin Hayashi1, Jun Moriwaki1, Tomoo Sawabe1, Fabiano L. Thompson2, Jean Swings2, Nicholas Gudkovs3, Richard Christen4 and Yoshio Ezura1

1 Laboratory of Microbiology, Graduate School of Fisheries Sciences, Hokkaido University, 3-1-1 Minato-cho, Hakodate 041, Japan
2 Laboratory of Microbiology, University of Ghent, Ledeganckstraat 35, B-9000 Ghent, Belgium
3 CSIRO – Livestock Industries, Australian Animal Health Laboratory, 5 Portarlington Road, Private Mail Bag 24, Geelong, Victoria 3220, Australia
4 Centre National de la Recherche Scientifique and Université de Nice Sophia-Antipolis, Laboratoire Jean Maetz, Villefranche-sur-Mer F06230, France

Correspondence
Tomoo Sawabe
sawabe{at}fish.hokudai.ac.jp


   ABSTRACT
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Five alginolytic, facultatively anaerobic, non-motile bacteria were isolated from the gut of abalones Haliotis laevigata and Haliotis rubra. Phylogenetic analyses based on 16S rDNA data indicated that these strains are related closely to Vibrio halioticoli (98 % 16S rDNA sequence similarity). DNA–DNA hybridization and fluorescent amplified fragment length polymorphism fingerprinting demonstrated that the five strains constituted a single species that was different from all currently known vibrios. The name Vibrio superstes sp. nov. (type strain, LMG 21323T=IAM 15009T=G3-29T; DNA G+C content, 48·0–48·9 mol%) is proposed to encompass this novel taxon. Several phenotypic features were disclosed that discriminate V. superstes from other Vibrio species: V. superstes sp. nov. and V. halioticoli can be differentiated on the basis of 17 traits (indole production, {beta}-galactosidase test and assimilation of 15 carbon compounds).

Abbreviations: FAFLP, fluorescent amplified fragment length polymorphism; ML, maximum-likelihood; MP, maximum-parsimony; NJ, neighbour-joining

The GenBank/EMBL/DDBJ accession numbers for the 16S rDNA sequences of Vibrio superstes are AF519806 (LMG 21319=B1-5), AY155582 (LMG 21320=B2-3), AY155583 (LMG 21321=G3-11), AY155584 (LMG 21322=G3-15) and AY155585 (LMG 21323T=G3-29T).

Figures showing a full phylogenetic tree and a transmission electron micrograph of Vibrio superstes LMG 21323T are available as supplementary material in IJSEM Online.


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Vibrio halioticoli and genetically related species, which are alginolytic, non-motile, fermentative marine bacteria, are abundant in the gut of Haliotis abalones in Japan and South Africa (Sawabe et al., 1995Go, 2002Go). Hypothesized roles of V. halioticoli include its contribution to the digestion of alginate, which is a major polysaccharide in Japanese kelps ingested by these animals, and its conversion into volatile short-chained fatty acids via fermentation (Sawabe et al., 2003Go). Nearly 80 species of abalone are known; they appear in offshore areas worldwide, but little is known about the presence of V. halioticoli-like bacteria in the gut of these molluscs. We recently isolated a set of five strains that were most similar phenotypically to V. halioticoli from the gut of Australian abalones (Haliotis laevigata and Haliotis rubra). DNA–DNA hybridization experiments, phenotypic characterization and phylogenetic and genetic analyses demonstrated that these strains represent a so far unknown species of the genus Vibrio.

Five strains of V. superstes sp. nov. [LMG 21319 (=IAM 15007=B1-5), LMG 21320 (=IAM 15008=B2-3), LMG 21321 (=G3-11), LMG 21322 (=G3-15) and LMG 21323T (=IAM 15009T=G3-29T)] were isolated from the gut of the Australian abalones H. laevigata and H. rubra. These were collected at the coastal area of Clifton Springs, Victoria, Australia, by scuba-diving in December 2000. Strains were cultured on ZoBell 2216E agar (Oppenheimer & ZoBell, 1952Go) and stored at -80 °C in 10 % glycerol.

The sequence of a 1400 bp fragment of the 16S rDNA gene of strains LMG 21319, LMG 21320, LMG21321, LMG 21322 and LMG 21323T was determined according to Sawabe et al. (1998)Go by using six sequencing primers (24F, 530F, 1100F, 520R, 920R and 1540R). The 16S rDNA sequences of V. superstes and related species were selected from a database of more than 60 000 already aligned bacterial 16S rDNA sequences. Selection of sequences was done according to previous phylogenetic analyses of the entire database and BLAST searches against the latest EBI release. Phylogenetic trees were constructed by using three different methods [BIONJ, maximum-likelihood (ML) and maximum-parsimony (MP)]. For neighbour-joining (NJ) analysis, distance matrices were calculated by using the Kimura two-parameter correction. BIONJ was done according to Gascuel (1997)Go, ML and MP were from PHYLIP (Phylogeny Inference Package, version 3.573c; distributed by J. Felsenstein, Department of Genetics, UW, Seattle, WA, USA). Because of close relationships, no evident homoplasy was detected and almost-entire sequences that corresponded to positions 47–1364 of the sequence of the type strain of V. superstes were used for the analysis (a short insertion in the Salinivibrio costicola sequence between positions 159 and 160 of V. superstes was excluded from the analysis). Phylogenetic trees were drawn by using NJPLOT (Perrière & Gouy, 1996Go). The topology shown (Fig. 1Go) is that of the bootstrap tree, as it has been demonstrated that this topology is often better than that of a simple NJ or MP analysis (Berry & Gascuel, 1996Go). There is no distance bar in Fig. 1Go as it would be meaningless because: (i) distances are corrected (see above) and (ii) this is a bootstrap tree.



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  		Fig. 1. Unrooted phylogenetic tree based on 16S rDNA sequence data. This figure combines the results of three analyses, i.e. NJ, MP and ML. The topology shown was obtained by using NJ and 1000 bootstrap replications (shown above branches).

 
Fluorescent amplified fragment length polymorphism (FAFLP) analysis was performed as described previously (Thompson et al., 2001Go; Sawabe et al., 2002Go). Clustering of the patterns was done by using the Dice coefficient (SD) and the Ward algorithm (Sneath & Sokal, 1973Go).

DNA of bacterial strains was prepared by the procedure of Marmur (1961)Go. DNA G+C contents were determined by HPLC (Tamaoka & Komagata, 1984Go). DNA–DNA hybridization experiments were performed in microdilution wells by using a fluorometric direct-binding method described by Ezaki et al. (1988Go, 1989)Go.

In total, 78 phenotypic characteristics, including alginase activity, were determined by standard methods (Leifson, 1963Go; Hidaka & Sakai, 1968Go; West et al., 1977Go; Ostle & Holt, 1982Go; Baumann & Schubert, 1984Go; Holt et al., 1994Go). These phenotypic characterizations were done at 20 °C.

The results of our phylogenetic analysis showed clearly that the strains belonged to the {gamma}3 subgroup, phylum Proteobacteria (Garrity & Holt, 2001Go) (see Supplementary Fig. A in IJSEM Online). The closest phylogenetic neighbour of the five Australian abalone strains is V. halioticoli (Fig. 1Go). The five strains of V. superstes had high levels of 16S rDNA sequence similarity to each other, i.e. 99·7–99·9 %, and 98·3 % similarity to V. halioticoli IAM 14596T. Similarity levels of <97·3 % were found with other Vibrio species.

The five strains had FAFLP patterns that consisted of 90±10 fragments (minimum, 80; maximum, 108) and mutual similarity of at least 64·6 % (Fig. 2Go). V. superstes showed pattern similarities of <50 % to other Vibrio species, which shows clearly that this novel species is different from other vibrios (Thompson et al., 2001Go). The FAFLP results are supported by our DNA–DNA hybridization experiments, which showed that the five strains of V. superstes (LMG 21319, LMG 21320, LMG 21321, LMG 21322 and LMG 21323T) were conspecific strains that were clearly separated from V. halioticoli (Table 1Go).



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  		Fig. 2. Dendrogram of FAFLP patterns of the five novel Vibrio isolates from Australian abalone. V. halioticoli, Vibrio tapetis and Vibrio penaeicida were included as outgroups.

 

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  		Table 1. DNA relatedness between Vibrio superstes and Vibrio halioticoli

 
The five Australian 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., 1998Go). No flagellated cells were observed by transmission electron microsscopy, but short tubular projections were observed in V. superstes cells, similar to those around Vibrio campbellii cells [as reported by Allen & Baumann (1971)Go] (see Supplementary Fig. B in IJSEM Online). The function of these tubular projections has never been clarified (Allen & Baumann, 1971Go). These strains required salt for growth, did not accumulate poly-{beta}-hydroxybutyrate and were oxidase-positive (Table 2Go). No peritrichous cells were observed when the strains were cultivated on solid media. Other phenotypic features of V. superstes are shown in Table 2Go. The five abalone isolates were most similar phenotypically to V. halioticoli IAM 14596T, although the strains differed by 17 out of 78 traits tested (Table 2Go).


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  		Table 2. Phenotypic characteristics for distinguishing Vibrio superstes from previously described alginolytic Vibrio species

Species/strains: 1, V. superstes LMG 21319–LMG 21323T; 2, V. halioticoli IAM 14596T; 3, Vibrio pelagius biovar 1 ATCC 25916T. +, Positive; -, negative; V+, variable (type strain is positive); V-, variable (type strain is negative). All species are negative for the following characteristics: pigmentation, swarming, poly-{beta}-hydroxybutyrate accumulation, luminescence, growth at 4 and 40 °C, amylase, gelatinase, chitinase, agarase, gas production from D-glucose, acetoin production, lysine decarboxylase, arginine dehydrolase, ornithine decarboxylase, acid from L-arabinose, inositol and L-rhamnose, requirement for organic growth factors, utilization of D-sorbitol, L-tyrosine, meso-erythritol, L-arabinose, citrate, DL-malate, {delta}-aminovalerate and aconitate. All species are positive for the following characteristics: Na+ requirement, growth at 15 and 30 °C, oxidase, catalase, alginase, nitrate reduction, O/129 sensitivity, methyl red test, growth on TCBS (thiosulfate/citrate/bile salts/sucrose) agar, growth in 3 % NaCl, acid from D-glucose, D-mannitol and maltose, utilization of alginate, D-fructose, D-glucose, maltose, D-mannitol, D-glucosamine, N-acetylglucosamine, fumarate and succinate. All species are fermentative in the oxidation–fermentation test.

 
Despite the close phylogenetic relationship between V. superstes and V. halioticoli, V. superstes occurs in rather small populations, the size of which range from 0 to 20 % in the gut of Australian abalones (data not shown). Compared to the abundant populations of V. halioticoli and its speculated symbiotic contribution to the conversion of alginate to acetic acid in the gut of Japanese and South African abalones (Sawabe et al., 2003Go), V. superstes may not be able to form such associations with Australian abalones because the major food of Australian abalones is red algae (Foale & Day, 1992Go). Differences in feeding behaviour of host abalones may affect the microflora of the gut microbial ecosystem and select for biochemical traits of these symbiotic vibrios. Major phenotypic traits of V. superstes differed from those of V. halioticoli in that the former was positive for use of 14 carbon compounds (Table 2Go). V. superstes may have acquired the ability to assimilate multiple carbon compounds to survive in the gut of the Australian abalone.

In conclusion, our polyphasic study demonstrated clearly that the five abalone isolates represent a so far undescribed species of the genus Vibrio, for which we propose the name Vibrio superstes sp. nov. The name V. superstes, which means survivor, has been chosen in this respect. Global whole-genome analyses may clarify the evolutionary history of V. superstes and V. halioticoli. Studies on the ecology of V. superstes are under way in order to better understand its interactions in the gut of marine herbivores, particularly abalones.

Description of Vibrio superstes sp. nov.
Vibrio superstes (su.per'stes. L. masc. adj. superstes remaining alive after another's death, outliving, surviving).

Gram-negative, facultatively anaerobic, non-motile and non-flagellated. Cells in ZoBell 2216E broth are rod-shaped with rounded ends (0·6–0·8x1·2–1·3 µm). No endospores or capsules are formed. Flagellation is not observed when the organism is cultivated on solid and/or in liquid media. Colonies on ZoBell 2216E agar are beige, circular, smooth and convex with entire edges. Sodium ions are essential for growth. Mesophilic and neutrophilic chemo-organotroph: grows between 15 and 30 °C. No growth occurs at 40 °C. Positive for acid production from glucose, nitrate reduction, hydrolysis of alginate, oxidase and catalase and assimilation of D-mannose, sucrose, D-gluconate, D-galactose, cellobiose, melibiose, lactose, D-glucuronate, trehalose, {gamma}-aminobutyrate, acetate, propionate, L-glutamate, D-xylose, D-fructose, maltose, D-glucosamine, N-acetylglucosamine, D-mannitol, fumarate, succinate, D-glucose and alginate. The following tests are negative: gas production from glucose, acetoin production, lysine decarboxylase, arginine dehydrolase, ornithine decarboxylase, indole production, {beta}-galactosidase test, luminescence, pigmentation, requirement for organic growth factors, hydrolysis of starch, gelatin, chitin, Tween 80 and agar, accumulation of poly-{beta}-hydroxybutyrate, assimilation of D-sorbitol, glycerol, citrate, meso-erythritol, DL-malate, 2-oxoglutarate, putrescine, {delta}-aminovalerate, pyruvate, L-tyrosine, aconitate and L-arabinose. DNA G+C content is 48·0–48·9 mol%.

The type strain is LMG 21323T=IAM 15009T. The bacterium was isolated from the gut of the Australian abalones Haliotis rubra and H. laevigata.


   ACKNOWLEDGEMENTS
 
This work was supported by Grants-in-Aid for Scientific Research from the Ministry of Education, Science and Culture of Japan (nos 09460081 and 13760134) and F. L. T. has a PhD scholarship (no. 2008361/98-6) from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Brazil. J. S. acknowledges grants from the Fund for Scientific Research (FWO), Belgium.


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