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A European epidemiological survey of Vibrio splendidus clade shows unexplored diversity and massive exchange of virulence factors

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Abstract

The Vibrio splendidus clade has previously been associated with epidemic outbreaks of various aquatic animals, as in the case of the cupped oyster, Crassostrea gigas. To investigate whether involved strains could present a clonal origin and to identify possible alternative background carriage animals or zooplankton, a large epidemiological survey was conducted on isolates of the splendidus clade. For this purpose, Vibrio strains were isolated from various samples including oysters, mussels, sediments, zooplankton, and sea water on the basis of a North/South gradient of the European sea water zone (Ireland, The Netherlands, France, Italy, and Spain). A total of 435 isolates were successfully associated to the V. splendidus clade using real time polymerase chain reaction with 16S specific primers and probes. A multiple-locus variable-number tandem-repeat analysis (VNTR) was conducted on all isolates based on a multiplex PCR–VNTR with a set of primer pairs designed from the V. tasmaniensis LGP32 genome. Preliminary validation of the primers on a set of collection strains from the V. splendidus clade confirmed that the former V. splendidus-related LGP32 and relative strains were related to V. tasmaniensis rather than to the type strain V. splendidus LMG 4042. The VNTR analysis was then successfully conducted on 335 isolates which led to the characterization of 87 different profiles. Our results showed that (1) the high diversity of VNTR did not enlighten significant correlation between a specific pattern and the origin of collected samples. However, populations isolated from animal samples tend to differ from those of the background environment; (2) oyster mortality events could not be linked to the clonal proliferation of a particular VNTR type. However, few different patterns seemed successively associated with samples collected during peaks of oyster’s mortality. (3) Finally, no correlation could be seen between specific VNTR patterns and sequence phylogeny of the virulence factors vsm and ompU that were detected among strains isolated during as well as outside mortality events. These results, combined with incongruence observed between the ompU and vsm phylogenetic trees, suggested both large diffusion of strains and massive lateral gene transfer within the V. splendidus clade.

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Acknowledgments

This study has been carried out in part with financial support from the Commission of the European Communities, under the EC’s Seventh Framework Program (FP7/2007-2013) in the grant funded “KBBE.2010.1.2-08: Improving European mollusc aquaculture: disease detection and management”. It does not necessarily reflect its views and in no way anticipates the Commission’s future policy in this area. We also aknowledge the EMIDA project MOLTRAQ for financial support, Egide for funding the Grant Number 18470SA, the CMCU for Grant Number 08G0908, and AUF for granting the second Ph.D. year from Hanen Nasfi. Finally, the data used in this work were partly produced through the technical facilities of the Centre Mediterranean Environment Biodiversity, University of Montpellier 2, France. Finally, special thanks to Mr. Marc Englezma for providing us with isolates from Netherlands.

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Authors and Affiliations

  1. CC 093 UMR 5119 “Ecologie des Systèmes Marins Côtiers”, Université de Montpellier 2, place Eugène Bataillon, 34095, Montpellier, France

    H. Nasfi, T. Sannie, L. Sorieul, J. Gerard & T. Vallaeys

  2. Laboratoire de Génétique et Pathologie des Mollusque Marins, Institut Français de Recherche pour l’Exploitation de la Mer, av. du Mus de Loup, 17390, La Tremblade, France

    M. A. Travers, P. Haffner, D. Tourbiez & T. Renault

  3. UMR 5119 “Ecologie des Systèmes Marins Côtiers”, Institut Français de Recherche pour l’Exploitation de la Mer, pl E. Bataillon, 34095, Montpellier, France

    J. de Lorgeril

  4. UR1077, Mathématique Informatique et Génome, Institut National de la Recherche Agronomique, Domaine de Vilvert, 78350, Jouy-en-Josas, France

    C. Habib

  5. UMR 226, ISEM, Institut Recherche pour le Développement, pl E. Bataillon, 34095, Montpellier, France

    J. C. Avarre

  6. IRTA-Sant Carles de la Ràpita, Crta. Poble Nou, km. 5, 5, 43540, Tarragona, Spain

    D. Furones & A. Roque

  7. Department of Life, Earth and Environmental Sciences (DISTAV), University of Genoa, Genoa, Italy

    C. Pruzzo

  8. Fish Health Unit, Marine Institute, Rinville, Oranmore, Co., Galway, Ireland

    D. Cheslett

  9. UR11ES70, Unité de recherche Toxicologie Microbiologie Environnementale et Santé, Faculté des sciences de Sfax, Université de Sfax, B.P. 1171, 3000, Sfax, Tunisia

    R. Gdoura

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  1. H. Nasfi
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Correspondence to T. Vallaeys.

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Supplementary Fig. 1. Factor analysis of the VNTR data on 335 European V. splendidus isolates. Factor analysis was performed on the Burt table of VNTR-ompU- and vsm -PCR fragments obtained, and mortality data converted into binary data using code 1 or 0 according to presence or absence of each fragment. ND: not determined, It: Italy, Sp: Spain, Fr: France, Noth: Netherlands, Ir: Ireland, Dim 1 and 2: coordinates in the two most representative axis of the factor analysis. A. Projection of strains coordinates using geographical origin and VNTR patterns (1 to 87) as supplementary variable in the analysis. B. Projection of strains coordinates using sample type and VNTR pattern (1 to 87) as supplementary variable in the analysis. C. Projection of variables coordinates. Red dots: b1 to b16-VNTR bands; vsm and ompU virulence factors both representing variables with two modes (P: present, A: absent) and mortality outbreaks representing variables with 3 modes. (P: present, A: absent, NA: Not determined). Grey triangles: strains factorial coordinates are projected as above in S1A and S1B (TIFF 2444 kb)

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11274_2015_1800_MOESM8_ESM.xls

Supplementary Table S1. Distribution of strains isolated (N = 435) by geographical origin and type of samples analyzed (XLS 21 kb)

11274_2015_1800_MOESM9_ESM.xls

Supplementary Table S2. Genbank accession numbers of ompU and vsm sequences from strains of the V. splendidus clade obtained in this study (XLS 26 kb)

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Nasfi, H., Travers, M.A., de Lorgeril, J. et al. A European epidemiological survey of Vibrio splendidus clade shows unexplored diversity and massive exchange of virulence factors. World J Microbiol Biotechnol 31, 461–475 (2015). https://doi.org/10.1007/s11274-015-1800-y

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