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1 Laboratory for Microbiology, Ghent University, K. L. Ledeganckstraat 35, Ghent 9000, Belgium
2 BCCMTM/LMG Bacteria Collection, Ghent University, K. L. Ledeganckstraat 35, Ghent 9000, Belgium
Correspondence
F. L. Thompson
fabiano.thompson{at}ugent.be
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ABSTRACT |
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Details of strains used in the study and the 16S rDNA/recA regression curve are available as supplementary material in IJSEM Online.
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MAIN TEXT |
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TOPABSTRACTMAIN TEXTREFERENCES |
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, b; Suantika et al., 2001; Urakawa et al., 2000). Vibrios are particularly abundant in and/or on marine organisms (Gomez-Gil et al., 1998; Nishiguchi, 2000; Rosenberg & Ben-Haim, 2002). Several Vibrio species are serious pathogens of aquatic animals (Austin & Austin, 1999; Lightner & Redman, 1998). Vibrio anguillarum, Vibrio salmonicida and Vibrio vulnificus are important bacterial pathogens of several fish species, while Vibrio splendidus-related species represent a threat to bivalves, and Vibrio harveyi and Vibrio campbellii to shrimps (Austin & Austin, 1999; Le Roux et al., 2002). Vibrio cholerae, Vibrio parahaemolyticus and V. vulnificus are pathogens of man (Farmer & Hickman-Brenner, 1992; Wachsmuth et al., 1994). V. cholerae, the causative agent of cholera, has killed thousands of people worldwide in the last decade (WHO, 2001, 2002; http://www.who.int/en/). In the last 3 years alone, about 10 000 people have died of cholera, mainly in developing countries (WHO, 2001, 2002).
According to Bergey's Manual of Systematic Bacteriology (2002) (see http://dx.doi.org/10.1007/bergeysoutline200210), there are six genera within the current family Vibrionaceae: Allomonas (one species), Enhydrobacter (one species), Listonella (two species), Photobacterium (six species), Salinivibrio (one species) and Vibrio (44 species). The genera Allomonas (Kalina et al., 1984) and Enhydrobacter (Staley et al., 1987) were tentatively allocated to the family Vibrionaceae based on phenotypic characteristics, but it is now known that Allomonas belongs to Vibrio and Enhydrobacter to Moraxella (Thompson et al., 2003a). Several novel Vibrio species isolated mainly from the aquatic environment and marine organisms have been described in the last few years, including species related to Vibrio tubiashii, i.e. Vibrio brasiliensis, Vibrio coralliilyticus, Vibrio neptunius, and Vibrio xuii (Ben-Haim et al., 2003; Thompson et al., 2003b); species related to Vibrio splendidus, i.e. Vibrio tasmaniensis, Vibrio kanaloae, Vibrio pomeroyi and Vibrio chagasii (Thompson et al., 2003c, d); species related to Vibrio halioticoli, i.e. ‘Vibrio ezurae’, ‘Vibrio gallicus’ and Vibrio superstes (Hayashi et al., 2003; Sawabe et al., 2003); species related to V. harveyi, i.e. Vibrio rotiferianus (Gomez-Gil et al., 2003a) and species related to Vibrio furnissii, i.e. Vibrio pacinii (Gomez-Gil et al., 2003b). The identification of Vibrio species requires the application of genomic analyses, including AFLP, rep-PCR, DNA–DNA hybridization and 16S rDNA gene sequencing (Thompson et al., 2001a).
In order to find new identification markers and improve our knowledge of the phylogenetic structure of vibrios, it is essential to analyse other genes apart from 16S rDNA. recA has been suggested as a potential marker to unravel phylogenetic relationships among higher taxonomic ranks such as families, classes and phyla because of its ubiquity and house-keeping function in bacteria (Eisen, 1995; Ludwig & Klenk, 2001; Zeigler, 2003). recA is a multifunctional protein contributing to homologous recombination, DNA repair and the SOS response, and specifically binds stretches of single-stranded DNA, unwinds duplex DNA, and finds regions of homology between chromosomes in homologous recombination (Cox, 2003; Lloyd & Sharp, 1993). To date, recA gene sequences have been used only to analyse V. cholerae strains (Byun et al., 1999; Stine et al., 2000), and their value in discriminating closely related species within the family Vibrionaceae is not known. Our aim in the present study was to analyse the usefulness of recA gene sequences as an alternative phylogenetic and identification marker for vibrios.
The strains used in this study are listed in Supplementary Table A in IJSEM Online. Strains were grown aerobically on marine agar 2216E (Difco) at 27 °C for 24 h. All strains included in this study are deposited in the BCCMTM/LMG Bacteria Collection or in the research Collection at Ghent University (Ghent, Belgium). Bacterial genomic DNA was extracted following the methodology described by Pitcher et al. (1989).
PCR mixtures were composed of 33·5 µl sterile MilliQ water, 5·0 µl 10x PCR buffer, 5·0 µl dNTPs, 0·5 µl forward primer (10 µM; 5'-TGGACGAGAATAAACAGAAGGC-3'; Byun et al., 1999), 0·5 µl reverse primer (10 µM; 5'-CCGTTATAGCTGTACCAAGCGCCC-3'; Stine et al., 2000), 0·5 µl AmpliTaq DNA polymerase and 5·0 µl template DNA (0·01µg µl–1). PCR was performed using a GeneAmp PCR System 9600 thermocycler (Applied Biosystems). The thermal program consisted of 5 min at 95 °C, 3 cycles of 45 s at 95 °C, 2 min at 55 °C and 1 min at 72 °C, 30 cycles of 20 s at 95 °C, 1 min at 55 °C and 1 min at 72 °C and a final extension of 7 min. at 72 °C. Positive PCRs, giving a product with the expected size and intensity, were purified using the Nucleofast 96 PCR clean up membrane system (Macherey-Nagel), which is based on ultrafiltration membranes. Purified PCR products were eluted in sterile MilliQ water. Subsequently, 3·0 µl purified PCR product was mixed with 1·0 µl ABI Prism Big Dye Terminator ready reaction mix, 3·0 µl forward and/or reverse primer (4 µM), 1·5 µl 5x buffer and 1·5 µl MilliQ water. The thermal program consisted of 30 cycles of 15 s at 96 °C, 1 s at 35 °C and 4 min at 60 °C. Sequencing products were purified using the Montage SEQ96 sequencing reaction cleanup kit (Genomics), which removes contaminating salts and unincorporated dye terminators from DNA sequencing reactions. Purified sequencing products were then dried in an Eppendorf Concentrator 5301 at room temperature for 40 min. Purified sequencing reactions were mixed with 20 µl deionized formamide and heated at 95 °C for 2 min. Subsequently, the mixture was chilled on ice for 2–3 min. Separation of the DNA fragments was carried out in an ABI PRISM 3100 Genetic Analyzer (Applied Biosystems). Time and voltage of sample injection were 22 s at 1 kV. Each run was performed at 50 °C, for 6500 s, at 0·1 mA and 12·2 kV. Raw sequence data were transferred to AutoAssembler software (Applied Biosystems), where consensus sequences were determined. Consensus sequences were imported into BioNumerics 2.5 software, where a similarity matrix and phylogenetic trees were created, based on the neighbour-joining method (Saitou & Nei, 1987) and maximum-parsimony. Pearson's product-moment correlation coefficient and a regression curve were calculated between recA and 16S rDNA data, based on 43 strains. The 16S rDNA data were obtained from EMBL. Splits tree decomposition analysis was carried out using software available online (http://www.mlst.net; Huson, 1998) while Sawyer's test was calculated using the software package START obtained from http://pubmlst.org/software/analysis/start/ (Jolley et al., 2001). EMBL accession numbers for the recA sequences are AJ580845–AJ580909.
In this study we sequenced a 739 bp fragment of recA of 62 Vibrionaceae strains, corresponding to approximately 70 % of the coding region of this locus. We compared recA and 16S rDNA pairwise similarities between 43 strains using Pearson's product-moment correlation coefficient. The correlation of recA and 16S rDNA data was found to be relatively good, at 0·58 (see Supplementary Fig. A in IJSEM Online). The data fitted well in a polynomial regression of second degree (r=0·8). Overall, recA gene sequences were much more discriminatory than 16S rDNA. For 16S rDNA similarity values above 98 %, there was a wide range of recA similarities, from 83 to 99 %. The mean (±SD) G+C content of the recA gene sequences was 46·9±2·2 mol%. This value is in agreement with the G+C content of the whole genome of vibrios (Thompson et al., 2003b, c), suggesting that this locus has not been affected by horizontal gene transfer. In addition, splits tree decomposition analysis and Sawyer's test did not indicate any evidence for recombination within the recA sequences in this study.
A neighbour-joining (NJ) tree with the estimated positions of the 71 representative Vibrionaceae strains based on 673 bp is presented in Fig. 1. We also built a maximum-parsimony tree that confirmed the grouping obtained by NJ. Vibrio species appear to be polyphyletic. Photobacterium species had at most 84 % recA sequence similarity towards Vibrio species, but are apparently nested within vibrios. Photobacterium species did not form a homogeneous group, having recA similarity values ranging from 82 to 96 %. Baumann et al. (1983) suggested that Photobacterium and Vibrio are two distinct phylogenetic groups. The recA sequence similarities of Vibrio species were between 74 and 99·6 %. Several Vibrio species formed deep branches e.g. V. gallicus, V. pacinii, Vibrio cincinnatiensis, Vibrio rumoiensis and Vibrio aestuarianus.
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), and were later confirmed by DNA–DNA hybridization to belong to the same species (unpublished data). Vibrio ichthyoenteri and Vibrio scophthalmi shared only 90 % recA sequence similarity, but 99 % similarity for the 16S rDNA (Thompson et al., 2002).
V. coralliilyticus LMG 21350 and LMG 19270 shared 96·8 % recA sequence similarity. These strains appeared within the former AFLP clusters A1 and A3, respectively (Thompson et al., 2001a). V. coralliilyticus and V. neptunius were phylogenetic neighbours, sharing 96 % recA similarity. According to Ben-Haim et al. (2003), V. neptunius, V. tubiashii, V. nereis and Vibrio shilonii were the species most closely related to V. coralliilyticus, having 97 to 98 % 16S rDNA sequence similarity.
V. harveyi-related species, i.e. V. campbellii, Vibrio natriegens, V. parahaemolyticus and V. rotiferianus, had recA sequence similarities between 89 and 98 %. V. parahaemolyticus strains LMG 2850T and 9115 had 96 % recA sequence similarity. Their closest neighbour was V. harveyi (92 % similarity). V. campbellii, V. harveyi and V. rotiferianus had about 97 % recA sequence similarity. These species are highly related on the basis of 16S rDNA sequences (>98 %), DNA–DNA hybridization (>65 %), Biolog and FAME (Gomez-Gil et al., 2003a).
V. nereis and V. xuii had 99 % 16S rDNA sequence similarity, but only 90 % recA gene sequence similarity. Vibrio fortis and Vibrio pelagius were closely related by 16S rDNA (98·8 %) and DNA–DNA hybridization (65 %) (Thompson et al., 2003e), but the recA sequence similarity between these two species was only 94·5 %. V. fortis LMG 20547 was closer to V. pelagius (98 % recA sequence similarity) than to V. fortis LMG 21557T, suggesting that strain LMG 20547 belongs to the species V. pelagius. LMG 20547 and the type strain of V. pelagius had 66 % similarity by DNA–DNA hybridization (Thompson et al., 2003e).
V. chagasii LMG 21353T and LMG 13219 had 97 % recA sequence similarity. These strains were found in the former FAFLP clusters A52 and A53, respectively (Thompson et al., 2001a). The closest neighbours of V. chagasii strains were V. fortis and V. pomeroyi, having at most 91 % recA sequence similarity. V. pomeroyi, V. splendidus and Vibrio cyclitrophicus shared only 92 % recA sequence similarity. V. splendidus had 93·7 and 95 % recA sequence similarity towards V. kanaloae and V. tasmaniensis, respectively. V. tasmaniensis, V. pomeroyi and V. kanaloae shared at most 95·7 % recA sequence similarity. Vibrio lentus LMG 21034T and R-3884 had 99 % recA sequence similarity, but only 97 % towards V. splendidus. V. lentus had 94 and 92 % similarity towards V. tasmaniensis and V. cyclitrophicus, respectively. The V. splendidus-related group is very homogeneous on the basis of 16S rDNA sequences (>98·7 % similarity), DNA–DNA hybridization (>50 %) and phenotype (Macian et al., 2001; Thompson et al., 2003c, d), suggesting that recA sequences are indeed valuable for the discrimination of these species.
The novel species V. neptunius, V. brasiliensis and V. xuii were closely related to V. tubiashii (98–99 % 16S rDNA gene sequence similarity) (Thompson et al., 2003b), but recA sequence similarity among these species was below 90 %. V. mediterranei and V. shilonii were almost identical by both recA and 16S rDNA. These results corroborate the proposal of Thompson et al. (2001b) that V. shilonii should be considered a later synonym of V. mediterranei.
V. vulnificus LMG 13545T, MO6-24S and 5310 had recA sequence similarity between 96 and 99 %. Vibrio fluvialis LMG 7894T, AS555 and AS530 shared more than 99 % sequence similarity, whereas V. fluvialis and V. furnissii had at most 93 % similarity. Strains AS555 and AS530 were identified by Stine et al. (2000) as V. parahaemolyticus, but our results indicate that they may belong to V. fluvialis.
Vibrio mimicus and V. cholerae, the two bona fide members of the genus Vibrio, were separated in two different groups. V. mimicus LMG 7896T, 523-80, 8643, R-20564, R-20565 and R-20568 shared at least 98 % recA sequence similarity, while V. cholerae LMG 21698T, A-5, NRT36-S, R-18244, R-18258, R-18297, R-18303, R-20544, R-20545, R-20546 and R-20548 had at least 94 % recA sequence similarity. In our AFLP analysis, these R- strains were highly related and had 74–98 % pattern similarity (Thompson et al., 2003f). V. cholerae strains included in this study represent well the currently known genomic diversity within this species (Thompson et al., 2003f), suggesting that recA is a valuable marker for the identification of V. cholerae strains. The recA similarity values between V. cholerae and V. mimicus were at most 94 %. Strains NRT36-S and A-5 clustered in between V. cholerae and V. mimicus. These strains appear to be at the outskirts of the species V. cholerae. Strains of different serogroups had very similar (99 %) recA sequences. V. cholerae LMG 21698T and R-18297 clustered together, having 99 % recA similarity. All V. cholerae O139 strains had 100 % similarity. Farfan et al. (2002) have highlighted that V. cholerae strains of different serogroups may have identical sequences. It has been argued that serogroup O139 strains have evolved from O1 strains (Faruque et al., 1998).
Vibrio ordalii and V. anguillarum showed a close relationship, having 98 % recA sequence similarity. V. diazotrophicus LMG 7893T and LMG 11217 had more than 99 % sequence similarity, and their closest neighbour was V. campbellii (86·9 % similarity). Grimontia hollisae was distantly related to Vibrio (66·3 % sequence similarity) and Photobacterium (70·5 % sequence similarity).
Until now, the backbone of bacterial systematics has been derived from the 16S rDNA sequence-based phylogeny (Ludwig & Klenk, 2001). 16S rDNA is indeed the most useful chronometer to allocate strains to different branches of the family Vibrionaceae (Thompson et al., 2002). However, several vibrios have nearly identical 16S rDNA sequences and this makes it difficult to use 16S rDNA sequences to discriminate closely related species. Furthermore, phenotypic features are very similar among vibrios and so AFLP or DNA–DNA hybridization remain the techniques of choice for species identification. The grouping of the Vibrionaceae obtained on the basis of recA gene sequences reflects well the grouping based on 16S rDNA gene sequences (Thompson et al., 2002). This study highlights the usefulness of recA gene sequences as alternative phylogenetic markers for vibrios. Our data suggest that strains of the same species have at least 94 % recA sequence similarity, but additional strains from each recognized species of the Vibrionaceae should be examined in future studies in order to confirm this threshold. We also intend to search for other alternative chronometers (Zeigler, 2003) which, in combination with recA, will provide a rapid and reliable means of identifying vibrios.
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ACKNOWLEDGEMENTS |
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F. L. Thompson, C. C. Thompson, S. Naser, B. Hoste, K. Vandemeulebroecke, C. Munn, D. Bourne, and J. Swings Photobacterium rosenbergii sp. nov. and Enterovibrio coralii sp. nov., vibrios associated with coral bleaching Int J Syst Evol Microbiol, March 1, 2005; 55(2): 913 - 917. [Abstract] [Full Text] [PDF]
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P. V. Dunlap and J. C. Ast Genomic and Phylogenetic Characterization of Luminous Bacteria Symbiotic with the Deep-Sea Fish Chlorophthalmus albatrossis (Aulopiformes: Chlorophthalmidae) Appl. Envir. Microbiol., February 1, 2005; 71(2): 930 - 939. [Abstract] [Full Text] [PDF]
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 F. L. Thompson, T. Iida, and J. Swings Biodiversity of Vibrios Microbiol. Mol. Biol. Rev., September 1, 2004; 68(3): 403 - 431. [Abstract] [Full Text] [PDF]
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