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Int J Syst Evol Microbiol 53 (2003), 1615-1617; DOI  10.1099/ijs.0.02660-0
© 2003 International Union of Microbiological Societies

Reclassification of Vibrio hollisae as Grimontia hollisae gen. nov., comb. nov.

Fabiano L. Thompson1,2, Bart Hoste2, Katrien Vandemeulebroecke2 and Jean Swings1,2

1 Laboratory for Microbiology, Ghent University, K. L. Ledeganckstraat 35, Ghent 9000, Belgium
2 BCCMTM/LMG Bacteria Collection, Laboratory for Microbiology, Ghent University, K. L. Ledeganckstraat 35, Ghent 9000, Belgium

Correspondence
Fabiano L. Thompson
Fabiano.Thompson{at}ugent.be


   ABSTRACT
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The taxonomic positions of three representative strains of Vibrio hollisae (LMG 17719T, LMG 21416 and LMG 21538) were investigated by means of 16S rDNA sequences and phenotypic data. V. hollisae strains (GenBank/EMBL accession nos AJ514909–AJ514911) shared 99·5 % 16S rDNA sequence similarity, but had only 94·6 % similarity to their closest phylogenetic neighbour, Enterovibrio norvegicus. 16S rDNA sequence similarity of V. hollisae and Vibrio cholerae was only 91 %. These results suggest that V. hollisae should be placed into a novel genus, for which the name Grimontia gen. nov. is proposed.

Abbreviations: FAFLP, fluorescent amplified fragment length polymorphism

Published online ahead of print on 11 April 2003 as DOI 10.1099/ijs.0.02660-0.

The GenBank/EMBL/DDBJ accession numbers for the 16S rDNA sequences of strains LMG 17719T, LMG 21416 and LMG 21538 are AJ514909–AJ514911.


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Vibrio hollisae was first described by Hickman et al. (1982)Go. This organism produces a number of toxins and also invades host epithelial cells (Miliotis et al., 1995Go), causing both gastroenteritis and septicaemia (Abbott & Janda, 1994Go). Phenotypically, V. hollisae strains are atypical of the genus Vibrio, as they are arginine dihydrolase-, lysine and ornithine decarboxylase-negative and cannot grow on thiosulphate/citrate/bile salts/sucrose (TCBS) agar. FAFLP (fluorescent amplified fragment length polymorphism) fingerprinting revealed that V. hollisae is quite different from other vibrios, as it remained unclustered when 506 Vibrio strains were grouped by FAFLP pattern similarity (Thompson et al., 2001Go). Dorsch et al. (1992)Go analysed the phylogenetic positions of several Vibrio species by means of 16S rRNA gene sequences and concluded that V. hollisae should be considered as a novel genus, although these authors highlighted the need for more representative 16S rRNA gene sequences of diverse Vibrio branches to determine whether V. hollisae is actually a novel genus. In a comprehensive phylogenetic study of the families Vibrionaceae, Aeromonadaceae and Plesiomonadaceae based on 16S rRNA gene sequences, Ruimy et al. (1994)Go showed that V. hollisae in fact lies at the outskirts of the genus Vibrio, being as closely related to this genus as to the genera Photobacterium and Salinivibrio. Analyses of toxR and gyrB gene sequences have pointed out the very low similarity between V. hollisae and other Vibrio species (Osorio & Klose, 2000Go; Vuddhakul et al., 2000Go). More recently, on the basis of 16S rDNA sequence analysis, we found that V. hollisae branched between Photobacterium species and a newly described genus, Enterovibrio, rather than with other vibrios (Thompson et al., 2002Go).

In this study, we further analysed the phylogenetic positions of three representative strains of V. hollisae (LMG 17719T, LMG 21416 and LMG 21538) that were associated with cases of gastroenteritis in the USA. Strains LMG 17719T (=ATCC 33564T) and LMG 21416 (=ATCC 33565=JCM 1284) were analysed in detail in the original description of V. hollisae (Hickman et al., 1982Go), while strain LMG 21538 (=CIP 104354) was isolated and studied by Carnahan et al. (1994)Go. 16S rDNA sequence analysis was performed as described previously (Thompson et al., 2001Go). Fatty acid methyl ester analysis was carried out as described by Huys et al. (1994)Go. Isolates were grown on trypticase soy broth (Becton Dickinson) supplemented with 1·5 % (w/v) Bacto agar (Becton Dickinson) and 1·5 % (w/v) NaCl at 28 °C for 24 h. Cells (approx. 50 mg) were harvested and fatty acids were isolated, following the recommendations of the manufacturer, by using the Microbial Identification system and software package, version 3.9 (MIDI).

The results of our phylogenetic analysis are depicted in Fig. 1Go. The three V. hollisae strains shared 99·5 % 16S rDNA sequence similarity, but had only 94·6 % similarity to their closest phylogenetic neighbour, Enterovibrio norvegicus. A maximum-parsimony tree gave a very similar branching pattern to the neighbour-joining tree shown in Fig. 1Go. 16S rDNA sequence similarity of V. hollisae to the genera Photobacterium and Salinivibrio was respectively 93 and 91·2 % whereas similarity between V. hollisae and V. cholerae was only 90·8 %, clearly indicating that V. hollisae belongs to a different genus within the family Vibrionaceae.



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  		Fig. 1. Phylogenetic tree with estimated positions of V. hollisae, Allomonas enterica and Enhydrobacter aerosaccus by using the neighbour-joining method, based on almost-complete 16S rDNA sequences (positions 10–1415). Bootstrap percentages after 1000 simulations are shown. Bar, 2 % estimated sequence divergence.

 
In our phylogenetic analyses we included representative 16S rDNA sequences of all six genera currently assigned to the family Vibrionaceae, i.e. Allomonas, Enhydrobacter, Listonella, Photobacterium, Salinivibrio and Vibrio [see outline of Bergey's Manual of Systematic Bacteriology (2002) at http://dx.doi.org/10·1007/bergeysoutline200210]. We also included representative sequences of the newly described genus Enterovibrio (Thompson et al., 2002Go). 16S rDNA sequences of Allomonas enterica LMG 21754T (GenBank/EMBL accession no. AJ550855, 1468 bp) and Enhydrobacter aerosaccus LMG 21877T (AJ550856, 1484 bp) were determined in the course of this study. The genera Allomonas (Kalina et al., 1984Go) and Enhydrobacter (Staley et al., 1987Go) were allocated tentatively to the family Vibrionaceae based on phenotypic features, but so far there had been no confirmation of their phylogenetic positions based on 16S rDNA sequence data (Farmer, 1986Go; Farmer & Hickman-Brenner, 1992Go). According to our 16S rDNA data, A. enterica and E. aerosaccus are highly related (with almost 100 % 16S rDNA sequence similarity) to Vibrio fluvialis (X74703) and Moraxella osloensis (X74897, AF005191 and AY043376), respectively (Pettersson et al., 1998Go; Coenye et al., 2002Go). Further experiments with a more comprehensive collection of reference strains of Allomonas and Enhydrobacter are needed to clarify the taxonomic affiliations of these genera.

The three 16S rDNA sequences of V. hollisae determined in the present study (GenBank accession nos AJ514909–AJ514911) were highly related (99·3 %) to sequence X74707, determined by Ruimy et al. (1994)Go for the type strain of V. hollisae. The four above-mentioned sequences were ~4 % different from sequence X56583, proposed by Dorsch et al. (1992)Go. Mellado et al. (1996)Go had already highlighted the need for an explanation of such a difference in sequence data. For their comparisons, Mellado et al. (1996)Go used the sequence of Dorsch et al. (1992)Go, although our results show clearly that the most accurate sequence is in fact that of Ruimy et al. (1994)Go or any of the three sequences determined in this study.

V. hollisae can be also differentiated from other members of the family Vibrionaceae by several phenotypic features (Table 1Go). V. hollisae has higher levels of the fatty acids C18 : 1{omega}9c and C16 : 1{omega}9c and does not grow on TCBS, as most vibrios can. V. hollisae is arginine dihydrolase-negative and nitrate reduction-positive, by which it differs from the genera Enterovibrio, Photobacterium and Salinivibrio.


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  		Table 1. Features that differentiate Grimontia gen. nov. from other genera of the family Vibrionaceae

Taxa: 1, Grimontia; 2, Enterovibrio (Thompson et al., 2002Go); 3, Photobacterium (Alsina & Blanch, 1994Go); 4, Salinivibrio (Mellado et al., 1996Go); 5, Vibrio (Alsina & Blanch, 1994Go). Fatty acid data (%) are from our own database. TCBS medium was obtained from Oxoid.

 
On the basis of the phylogenetic and phenotypic data presented here, we propose to accommodate V. hollisae in a novel genus, Grimontia gen. nov. The type species of the novel genus is Grimontia hollisae gen. nov., comb. nov.

Description of Grimontia gen. nov.
Grimontia (Gri.mon'ti.a. N.L. gen. n. Grimontia of Grimont, after the French microbiologist P. A. D. Grimont).

Cells are Gram-negative, motile by a polar flagellum and oxidase-positive. Strains have a DNA G+C content of 48·5–51·0 mol%. Most abundant fatty acids are summed feature 3 (31±1 %; comprising C16 : 1{omega}7c and/or iso-C15 : 0 2-OH), C18 : 1{omega}7c (23±2 %), C16 : 0 (14±1 %), C12 : 0 (5±1 %), C18 : 1{omega}9c (5±1 %), summed feature 2 (5±2 %; comprising C14 : 0 3-OH and/or iso-C16 : 1 I and/or unidentified fatty acid with equivalent chain-length value of 10·928 and/or C12 : 0 ALDE), C16 : 1{omega}9c (4±0 %), C12 : 0 3-OH (4±2 %), C14 : 0 (3±0 %) and C18 : 0 (2±1 %). Chemoheterotrophic, mesophilic and moderately halophilic. Strains are negative for Voges–Proskauer reaction, arginine dihydrolase, lysine and ornithine decarboxylase, but indole production and nitrate reduction are positive. 16S rDNA sequences of Grimontia strains have typical signatures at positions 970–971 (TC instead of AG) and 1107–1108 (CG instead of AA), which differ from those of other members of the family Vibrionaceae.

The type species is Grimontia hollisae (LMG 17719T; GenBank/EMBL accession no. AJ514909, DNA G+C content is 48·5 mol%). Description of Grimontia hollisae gen. nov., comb. nov. is based on the original description of Hickman et al. (1982)Go.


   ACKNOWLEDGEMENTS
 
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. The authors acknowledge the suggestions of the two reviewers.


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Dorsch, M., Lane, D. & Stackebrandt, E. (1992). Towards a phylogeny of the genus Vibrio based on 16S rRNA sequences. Int J Syst Bacteriol 42, 58–63.[Abstract/Free Full Text]

Farmer, J. J., III (1986). International Committee on Systematic Bacteriology. Subcommittee on the taxonomy of Vibrionaceae. Minutes of the meetings, 8 and 11 September 1986, Manchester, England. Int J Syst Bacteriol 39, 201–212.

Farmer, J. J., III & Hickman-Brenner, F. W. (1992). The genera Vibrio and Photobacterium. In The Prokaryotes. A Handbook on the Biology of Bacteria: Ecophysiology, Isolation, Identification, Applications, 2nd edn, pp. 2952–3011. Edited by A. Balows, H. G. Trüper, M. Dworkin, W. Harder & K. H. Schleifer. New York: Springer-Verlag.

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Huys, G., Vancanneyt, M., Coopman, R., Janssen, P., Falsen, E., Altwegg, M. & Kersters, K. (1994). Cellular fatty acid composition as a chemotaxonomic marker for the differentiation of phenospecies and hybridization groups in the genus Aeromonas. Int J Syst Bacteriol 44, 651–658.[Abstract/Free Full Text]

Kalina, G. P., Antonov, A. S., Turova, T. P. & Grafova, T. I. (1984). Allomonas enterica gen. nov., sp. nov., deoxyribonucleic acid homology between Allomonas and some other members of the Vibrionaceae. Int J Syst Bacteriol 34, 150–154.[Abstract/Free Full Text]

Mellado, E., Moore, E. R. B., Nieto, J. J. & Ventosa, A. (1996). Analysis of 16S rRNA gene sequences of Vibrio costicola strains: description of Salinivibrio costicola gen. nov., comb. nov. Int J Syst Bacteriol 46, 817–821.[Abstract/Free Full Text]

Miliotis, M. D., Tall, B. D. & Gray, R. T. (1995). Adherence to and invasion of tissue culture cells by Vibrio hollisae. Infect Immun 63, 4959–4963.[Abstract]

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Pettersson, B., Kodjo, A., Ronaghi, M., Uhlén, M. & Tønjum, T. (1998). Phylogeny of the family Moraxellaceae by 16S rDNA sequence analysis, with special emphasis on differentiation of Moraxella species. Int J Syst Bacteriol 48, 75–89.[Abstract/Free Full Text]

Ruimy, R., Breittmayer, V., Elbaze, P., Lafay, B., Boussemart, O., Gauthier, M. & Christen, R. (1994). Phylogenetic analysis and assessment of the genera Vibrio, Photobacterium, Aeromonas, and Plesiomonas deduced from small-subunit rRNA sequences. Int J Syst Bacteriol 44, 416–426.[Abstract/Free Full Text]

Staley, J. T., Irgens, R. L. & Brenner, D. J. (1987). Enhydrobacter aerosaccus gen. nov., sp. nov., a gas-vacuolated, facultatively anaerobic, heterotrophic rod. Int J Syst Bacteriol 37, 289–291.[Abstract/Free Full Text]

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