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Int J Syst Evol Microbiol 53 (2003), 1495-1501; DOI  10.1099/ijs.0.02658-0
© 2003 International Union of Microbiological Societies

Vibrio fortis sp. nov. and Vibrio hepatarius sp. nov., isolated from aquatic animals and the marine environment

F. L. Thompson1,2, C. C. Thompson1,2, B. Hoste2, K. Vandemeulebroecke2, M. Gullian3 and J. Swings1,2

1 Laboratory for Microbiology, Ghent University, K. L. Ledeganckstraat 35, Ghent 9000, Belgium
2 BCCM/LMG Bacteria Collection, Ghent University, K. L. Ledeganckstraat 35, Ghent 9000, Belgium
3 National Center for Marine and Aquaculture Research, Guayaquil, Ecuador

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


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
In this study, the taxonomic positions of 19 Vibrio isolates disclosed in a previous study were evaluated. Phylogenetic analysis based on 16S rDNA sequences partitioned these isolates into groups that were closely related (98·8–99·1 % similarity) to Vibrio pelagius and Vibrio xuii, respectively. DNA–DNA hybridization experiments further showed that these groups had <70 % similarity to other Vibrio species. Two novel Vibrio species are proposed to accommodate these groups: Vibrio fortis sp. nov. (type strain, LMG 21557T=CAIM 629T) and Vibrio hepatarius sp. nov. (type strain, LMG 20362T=CAIM 693T). The DNA G+C content of both novel species is 45·6 mol%. Useful phenotypic features for discriminating V. fortis and V. hepatarius from other Vibrio species include production of indole and acetoin, utilization of cellobiose, fermentation of amygdalin, melibiose and mannitol, {beta}-galactosidase and tryptophan deaminase activities and fatty acid composition.

Abbreviations: FAFLP, fluorescent amplified fragment length polymorphism; FAME, fatty acid methyl ester

Published online ahead of print on 28 February 2003 as DOI 10.1099/ijs.0.02658-0.

The GenBank/EMBL/DDBJ accession numbers for the 16S rDNA sequences of strains LMG 21557T and LMG 20362T are AJ514916 and AJ345063, respectively.

Tables of variable features among strains of V. fortis and V. hepatarius are available as supplementary material in IJSEM Online.


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
Vibrios are among the most abundant culturable microbes in aquatic environments (Heidelberg et al., 2002aGo). A recent study of the bacterioplankton of Chesapeake Bay showed that Vibrio and Photobacterium species comprised up to 4 % (2x108 cells l-1) of total bacteria (Heidelberg et al., 2002aGo). High Vibrio and Photobacterium numbers (4·3x106 mm-2) were also reported to be attached to the external surface of zooplankton. It was concluded that a close partnership exists between these bacteria and zooplankton (Heidelberg et al., 2002bGo; Lipp et al., 2002Go). Vibrios also belong to the normal microflora of the shrimp Litopenaeus vannamei (Vandenberghe et al., 1999Go). Moss et al. (2000)Go reported that Vibrio and Aeromonas species comprised up to 85 % [about 109 c.f.u. (g gut tissue)-1] of bacterial flora in the gut of this shrimp, whereas Gomez-Gil et al. (1998)Go found a high abundance of vibrios (105 c.f.u. g-1 and 104 c.f.u. ml-1, respectively) in the hepatopancreas and haemolymph of healthy L. vannamei. Certain Vibrio strains have been reported to be potential probiotics for this shrimp (Gomez-Gil et al., 1998Go, 2000Go, 2002Go). Use of probiotics, i.e. live micro-organisms that, when administered in adequate amounts, confer a health benefit on the host, has been reported to reduce the need for medication (e.g. antibiotics and pesticides) and water exchange, which are used massively in intensive shrimp-rearing (Verschuere et al., 2000Go).

We have demonstrated that the genus Vibrio harbours a wealth of diverse genomes and represents cosmopolitan and endemic species that are yet to be described (Thompson et al., 2001Go). The exact ecological role of several of these groups is unknown at present. In this study, we report the taxonomic characterization of FAFLP (fluorescent amplified fragment length polymorphism) clusters A9, A26 and A60 that were disclosed in a former study (Thompson et al., 2001Go). Group A9 (n=8) was found to be ubiquitous in the marine environment and was associated with both diseased and healthy aquatic animals. Group A26 consisted of three isolates that originated from the hepatopancreas of wild healthy adults of L. vannamei from Ecuador. Recent results suggest that these isolates may have probiotic properties for L. vannamei under culture conditions (M. Gullian & J. Rodriguez, unpublished data). A representative Vibrio strain, LMG 20362T, showed high levels of colonization in the hepatopancreas of L. vannamei and out-competed and excluded the shrimp pathogen Vibrio harveyi. Additionally, this strain seems to enhance the health and weight of shrimps (M. Gullian & J. Rodriguez, unpublished data). Group A60 (n=8) was restricted to cultures of bivalve larvae (Nodipecten nodosus) in south Brazil. We propose to accommodate isolates of groups A9 and A60 in a novel Vibrio species, Vibrio fortis sp. nov., and isolates of group A26 in another novel species, Vibrio hepatarius sp. nov.


   METHODS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
RESULTS AND DISCUSSION
 REFERENCES
 
Bacterial strains, growth conditions and DNA isolation.
Strains characterized in this study are listed in Table 1Go. Strains were grown aerobically on tryptone soy agar (TSA; Oxoid) supplemented with 2 % (w/v) NaCl for 24 h at 28 °C. DNA was extracted by following the methodology described by Pitcher et al. (1989)Go. All strains included in this study have been deposited in the BCCM/LMG Bacteria Collection at Ghent University, Belgium, and in the CAIM collection of the Centre for Research on Nutrition and Development (CIAD) in Mazatlán, Mexico.


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  		Table 1. List of strains used in this study

 
Genotypic analyses.
Determination of almost-complete 16S rDNA sequences was accomplished essentially as described previously (Thompson et al., 2001Go). Alignment of 16S rDNA sequences, distance estimations (Jukes & Cantor, 1969Go), clustering by the neighbour-joining (Saitou & Nei, 1987Go), maximum-likelihood and maximum-parsimony methods and calculation of cluster stability (bootstrap analysis with 1000 replicates) were performed with BioNumerics 2.5 software (Applied Maths). DNA–DNA hybridization experiments with photobiotin-labelled DNA were run under stringent conditions (39 °C) following the methodology described by Willems et al. (2001)Go. Hybridizations were performed in four replicates. DNA binding values are means of reciprocal and non-reciprocal reactions. The DNA G+C content (mol%) was determined by HPLC (Mesbah et al., 1989Go).

Phenotypic analyses.
Phenotypic characterization of the isolates was performed by using API 20E and API ZYM kits (bioMérieux) and Biolog GN metabolic fingerprinting, following the instructions of the manufacturers with slight modifications (Thompson et al., 2002Go). Classical phenotypic tests were performed as described previously (Baumann et al., 1984Go; Farmer & Hickman-Brenner, 1992Go; Vandamme et al., 1998Go; Thompson et al., 2002Go). Antibiograms were determined by using the disc-diffusion method (Acar & Goldstein, 1996Go) with commercial discs (Oxoid). The inhibition zone of each antibiotic was measured with strains grown on Iso-Sensitest agar (Oxoid) supplemented with 1·5 % (w/v) NaCl for 24 h at 28 °C. Fatty acid methyl ester (FAME) analysis was carried out as described by Huys et al. (2001). 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.


   RESULTS AND DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS AND DISCUSSION
REFERENCES
 
The phylogenetic positions of five strains representative of V. fortis, LMG 21557T (GenBank/EMBL accession no. AJ514916), LMG 21558 (AJ514913), LMG 20547 (AJ316202), LMG 21566 (AJ514917) and LMG 21562 (AJ514915), from FAFLP groups A9 and A60, were analysed by means of their 16S rDNA sequences. These isolates had nearly identical 16S rDNA sequences (Fig. 1Go) and their closest neighbour was Vibrio pelagius CECT 4202T (AJ293802) with 98·8 % sequence similarity. When the V. pelagius sequence of Ruimi et al. (1994)Go was used, i.e. X74722, similarity between the five novel isolates and V. pelagius dropped to 97·4 %. Macián et al. (2000)Go have already suggested that the latter GenBank/EMBL entry is most probably a sequence of Vibrio natriegens, rather than V. pelagius. Other phylogenetic neighbours of V. fortis, with a maximum of 97·8 % similarity, are shown in Fig. 1Go. Vibrio cholerae, Vibrio mimicus and Vibrio metschnikovii were the most distant phylogenetic relatives of V. fortis within the genus Vibrio, with 92·5–92·9 % similarity. V. hepatarius LMG 20362T was most closely related to the recently described species Vibrio xuii (99·1 % similarity) (Thompson et al., 2003Go) and to Vibrio tubiashii and Vibrio nereis (98·6–99·0 %) (Fig. 1Go). V. hepatarius was also related to Vibrio mytili, Vibrio diabolicus and Vibrio orientalis (98·0–98·2 %) and its most distant relatives within the genus Vibrio were V. mimicus and Vibrio salmonicida (92·9 %).



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  		Fig. 1. Phylogenetic tree showing the positions of V. fortis and V. hepatarius, estimated by using the neighbour-joining method and based on almost-complete 16S rDNA sequences. Bootstrap values (>50 %) after 1000 simulations are shown. Bar, 1 % estimated sequence divergence.

 
Results of DNA–DNA hybridization experiments are summarized in Table 2Go. We chose four representative isolates from cluster A9, as this group was found to be very heterogeneous by FAFLP analysis, and two representative isolates from group A60, which was a very tight FAFLP cluster (Thompson et al., 2001Go). These six V. fortis isolates formed a single novel species with at least 70 % DNA–DNA similarity, and a maximum of 66 % similarity towards V. pelagius. V. hepatarius LMG 20362T had a maximum of 66 % similarity towards V. orientalis. Both novel species had <45 % DNA–DNA similarity to the recently described species Vibrio coralliilyticus (Ben-Haim et al., 2003Go) and to Vibrio neptunius, Vibrio brasiliensis and V. xuii (Thompson et al., 2003Go). These results corroborate those of our previous FAFLP fingerprinting experiments, which suggested that groups A9, A26 and A60 were novel species within the genus Vibrio (Thompson et al., 2001Go).


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  		Table 2. DNA–DNA binding values and DNA G+C contents of Vibrio strains examined

Taxa: 1, V. fortis LMG 21557T; 2, V. fortis LMG 21558; 3, V. fortis LMG 21562; 4, V. fortis LMG 21561; 5, V. fortis LMG 20547; 6, V. fortis LMG 21565; 7, V. pelagius LMG 3897T; 8, V. coralliilyticus LMG 20984T; 9, V. neptunius LMG 20536T; 10, V. brasiliensis LMG 20546T; 11, V. xuii LMG 21346T; 12, V. hepatarius LMG 20362T; 13, V. diabolicus LMG 19805T; 14, V. tubiashii LMG 10936T; 15, V. nereis LMG 3895T; 16, V. orientalis LMG 7897T; 17, V. mytili LMG 19157T.

 
Both novel Vibrio species represented by the 19 isolates examined in this study shared the main phenotypic and chemotaxonomic features of the genus Vibrio (Lambert et al., 1983Go; Farmer & Hickman-Brenner, 1992Go; Bertone et al., 1996Go). They were facultatively anaerobic, oxidase-positive and showed prolific growth on thiosulfate/citrate/bile salts/sucrose agar (TCBS). Isolates were slightly curved rods, motile, susceptible to vibriostatic agent O/129 (except for LMG 21568 and LMG 21559) and their growth was stimulated by NaCl. In spite of their similarity to other Vibrio species, the two novel species showed several differentiating phenotypic features (Table 3Go). We therefore propose to accommodate A9 and A60 isolates in a novel species, V. fortis sp. nov., and A26 isolates in another, V. hepatarius sp. nov. Because several phylogenetic neighbours of V. fortis and V. hepatarius (i.e. V. neptunius, V. brasiliensis, V. xuii and V. coralliilyticus) were analysed phenotypically and described by using the same methodologies as in this study, we assume that these results are largely comparable. Similar phenotypic methodologies have also been applied to the description of V. diabolicus (Raguénès et al., 1997Go), V. mytili (Pujalte et al., 1993Go) and the two novel species in this study, suggesting that comparisons may be reliable.


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  		Table 3. Features that diffentiate V. fortis and V. hepatarius from closely related Vibrio species

Taxa: 1, V. fortis (n=16); 2, V. hepatarius (n=3); 3, V. neptunius (Thompson et al., 2003Go); 4, V. brasiliensis (Thompson et al., 2003Go); 5, V. xuii (Thompson et al., 2003)Go; 6, V. pelagius (Alsina & Blanch, 1994Go); 7, V. coralliilyticus (Ben-Haim et al., 2003Go); 8, V. diabolicus (Raguénès et al., 1997Go); 9, V. mytili (Pujalte et al., 1993Go); 10, V. nereis (Alsina & Blanch, 1994Go); 11, V. orientalis (Alsina & Blanch, 1994Go); 12, V. tubiashii (Alsina & Blanch, 1994Go). Fatty acid data are given as mean±SD (%). Abbreviations: +, positive; -, negative; V, variable feature (followed by type strain feature); ND, no data available. Utilization of gentiobiose, fermentation of amygdalin and melibiose, enzyme activities and fatty acid profiles of known Vibrio species are from our own database.

 
Description of Vibrio fortis sp. nov.
Vibrio fortis (for'tis. L. adj. fortis strong).

Cells are slightly curved, 1 µm in width and 3 µm in length. They form translucent to opaque, low convex, non-swarming, smooth-rounded colonies with entire margins that are beige in colour and about 4 mm in diameter on TSA after 48 h incubation at 28 °C. Strains form yellow and/or green, translucent, smooth-rounded colonies of 4–5 mm diameter on TCBS. All strains have a facultatively anaerobic metabolism and ferment glucose and mannitol, but not inositol, sorbitol or rhamnose. Growth occurs at 4–35 °C and in media that contain 1–8 % (w/v) NaCl. Prolific growth occurs at 28 °C in media that contain 2·5 % (w/v) NaCl. The following features are positive for all strains: oxidase, catalase, {beta}-galactosidase and tryptophan deaminase activities and indole production. All strains utilize dextrin, glycogen, Tween 40, Tween 80, N-acetyl-D-glucosamine, N-acetyl-D-galactosamine, cellobiose, D-fructose, D-galactose, gentiobiose, {alpha}-D-glucose, maltose, D-mannitol, D-mannose, psicose, D-sorbitol, sucrose, D-trehalose, methyl pyruvate, monomethyl succinate, D-gluconic acid, DL-lactic acid, succinic acid, L-alanine, L-alanylglycine, L-asparagine, L-aspartic acid, L-glutamic acid, glycyl L-aspartic acid, glycyl L-glutamic acid, L-proline, L-serine, L-threonine, inosine, thymidine and glycerol as sole carbon sources. None of the strains can utilize adonitol, D-arabitol, i-erythritol, L-fucose, m-inositol, L-rhamnose, xylitol, citric acid, formic acid, D-galactonic acidolactone, D-glucuronic acid, {alpha}-hydroxybutyric acid, p-hydroxyphenylacetic acid, itaconic acid, {alpha}-ketobutyric acid, malonic acid, D-saccharic acid, sebacic acid, succinamic acid, glucuronamide, alaninamide, hydroxy L-proline, L-phenylalanine, L-pyroglutamic acid, DL-carnitine, urocanic acid, phenylethylamine, 2-aminoethanol, 2,3-butanediol or glucose 1-phosphate as sole carbon sources. The following tests are negative for all strains: arginine dihydrolase, lysine and ornithine decarboxylase activities, H2S production and urease activity. The most abundant fatty acids are summed feature 3 (37·5±2·9 %; comprises C16 : 1{omega}7c and/or iso-C15 : 0 2-OH), C16 : 0 (18·0±7·0 %), C18 : 1{omega}7c (11·9±2·9 %), iso-C16 : 0 (8·4±4·3 %), C14 : 0 (5·3±1·4 %), C12 : 0 (3·6±1·2 %), iso-C14 : 0 (2·7±1·5 %), summed feature 2 (2·4±0·4 %; comprises 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), C12 : 0 3-OH (1·5±0·4 %), C18 : 0 (1·2±0·6 %), iso-C14 : 0 3-OH (1·1±0·6 %), C17 : 1{omega}8c (0·7±1·9 %), unknown 12·484 (0·6±0·2 %), iso-C18 : 0 (0·6±0·3 %), C15 : 0 (0·6±1·2 %), C17 : 0 (0·5±0·9 %), iso-C12 : 0 (0·4±0·2 %), summed feature 7 (0·4±0·2 %; comprises C19 : 1{omega}6c and/or unidentified fatty acid with equivalent chain-length value of 18·846), iso-C12 : 0 3-OH (0·3±0·2 %), C15 : 1{omega}8c (0·3±0·9 %), C20 : 1{omega}7c (0·2±0·1 %), C16 : 1{omega}5c (0·2±0·1 %), C16 : 1{omega}7c alcohol (0·2±0·1 %), unknown 11·799 (0·2±0·1 %), C18 : 1{omega}5c (0·1±0·1 %), C11 : 0 3-OH (0·1±0·5 %), C10 : 0 3-OH (0·1±0·4 %), C12 : 0 2-OH (0·1±0·0 %), C16 : 0 3-OH (0·1±0·3 %), 11-methyl C18 : 1{omega}7c (0·1±0·1 %), anteiso-C17 : 0 (0·1±0·3 %), C13 : 0 (0·1±0·2 %) and C17 : 1{omega}6c (0·1±0·1 %). All strains are susceptible to tetracycline (30 µg) and chloramphenicol (30 µg), but are moderately resistant to polymyxin (300 U). Additional phenotypic features are listed in Supplementary Table A in IJSEM Online. 16S rDNA sequences of strains LMG 21557T, LMG 21558, LMG 20547, LMG 21566 and LMG 21562 are deposited in GenBank/EMBL under accession numbers AJ514916, AJ514913, AJ316202, AJ514917 and AJ514915, respectively. DNA G+C content of the type strain is 45·6 mol%.

The type strain of this species, LMG 21557T (=CAIM 629T), was isolated from the white shrimp Litopenaeus vannamei in Ecuador.

Description of Vibrio hepatarius sp. nov.
Vibrio hepatarius (he.pa.ta'ri.us. L. masc. adj. hepatarius of or belonging to the liver).

Cells are slightly curved, 1 µm in width and 2–3 µm in length. They form translucent, convex, non-swarming, smooth-rounded colonies with entire margins that are beige in colour and about 6 mm in diameter on TSA after 48 h incubation at 28 °C. Strains form yellow, translucent, smooth-rounded colonies of 6 mm diameter on TCBS. All strains have a facultatively anaerobic metabolism and ferment glucose, mannitol, sucrose and amygdalin, but not inositol, rhamnose, melibiose or arabinose. Growth occurs at 4–35 °C and in media that contain 0–8 % (w/v) NaCl. Prolific growth occurs at 28 °C in media that contain 2·5 % (w/v) NaCl. The following tests are positive for all strains: oxidase and catalase activities, indole and acetoin production and NO3 reduction. All strains utilize dextrin, N-acetyl-D-glucosamine, cellobiose, D-fructose, {alpha}-D-glucose, maltose, psicose, sucrose, D-trehalose, methyl pyruvate, inosine and glycerol as sole carbon sources. None of the strains can utilize glycogen, Tween 40, N-acetyl-D-galactosamine, adonitol, L-arabinose, D-arabitol, i-erythritol, L-fucose, D-galactose, gentiobiose, m-inositol, {alpha}-lactose, {alpha}-D-lactose lactulose, D-melibiose, D-raffinose, L-rhamnose, turanose, xylitol, monomethyl succinate, acetic acid, cis-aconitic acid, citric acid, formic acid, D-galactonic acidolactone, D-galacturonic acid, D-gluconic acid, D-glucosaminic acid, D-glucuronic acid, {alpha}-hydroxybutyric acid, {gamma}-hydroxybutyric acid, p-hydroxyphenylacetic acid, itaconic acid, {alpha}-ketobutyric acid, {alpha}-ketovaleric acid, malonic acid, propionic acid, quinic acid, D-saccharic acid, sebacic acid, bromosuccinic acid, succinamic acid, glucuronamide, alaninamide, D-alanine, L-aspartic acid, glycyl L-aspartic acid, glycyl L-glutamic acid, L-histidine, hydroxy L-proline, L-leucine, L-ornithine, L-phenylalanine, L-pyroglutamic acid, D-serine, L-threonine, DL-carnitine, {gamma}-aminobutyric acid, urocanic acid, uridine, thymidine, phenylethylamine, putrescine, 2-aminoethanol, 2,3-butanediol, DL-{alpha}-glycerol phosphate, glucose 1-phosphate or glucose 6-phosphate as sole carbon sources. The following tests are negative for all strains: {beta}-galactosidase, lysine and ornithine decarboxylases, H2S production and urease. The most abundant fatty acids are summed feature 3 (28·4±15·2 %; comprises C16 : 1{omega}7c and/or iso-C15 : 0 2-OH), C16 : 0 (14·6±9·6 %), iso-C15 : 0 (13·2±22·1 %), C18 : 1{omega}7c (10·3±9·9 %), C14 : 0 (5·4±1·4 %), iso-C16 : 0 (4·7±2·7 %), iso-C13 : 0 (3·7±5·4 %), iso-C17 : 0 (2·5±3·7 %), C12 : 0 (2·2±1·9 %), summed feature 2 (2·2±0·3 %; comprises 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), iso-C14 : 0 (2·0±1·4 %), anteiso-C15 : 0 (1·9±2·9 %), C12 : 0 3-OH (1·1±1·0 %), iso-C17 : 1{omega}5c (1·1±1·9 %), iso-C17 : 1{omega}10c (0·8±1·4 %), unknown 12·484 (0·5±0·5 %), iso-C14 : 0 3-OH (0·5±0·6 %), anteiso-C17 : 0 (0·5±0·6 %), anteiso-C13 : 0 (0·5±0·8 %), C16 : 1{omega}7c alcohol (0·4±0·6 %), C15 : 0 (0·4±0·4 %), C17 : 0 (0·2±0·2 %) and C17 : 1{omega}8c (0·1±0·2 %). All strains are susceptible to the vibriostatic agent O/129 (10 and 150 µg), polymyxin (300 U), tetracycline (30 µg) and chloramphenicol (30 µg), but are moderately resistant to ampicillin (25 µg). Additional phenotypic features are listed in Supplementary Table B in IJSEM Online. The 16S rDNA sequence of strain LMG 20362T is deposited in GenBank/EMBL under accession number AJ345063. DNA G+C content of the type strain is 45·5 mol%.

The type strain of this species, LMG 20362T (=CAIM 693T), was isolated from the white shrimp Litopenaeus vannamei in Ecuador.


   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 Professor P. Vandamme for helping with the nomenclature of the novel species. The authors also acknowledge the suggestions of the two reviewers.


   REFERENCES
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 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS AND DISCUSSION
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