A single regulatory gene is sufficient to alter Vibrio aestuarianus pathogenicity in oysters
A utilisé MicroScope Platform International audience Oyster diseases caused by pathogenic vibrios pose a major challenge to the sustainability of oyster farming. In France, since 2012 a disease affecting specifically adult oysters has been associated with the presence of Vibrio aestuarianus. Here, b...
Published in: | Environmental Microbiology |
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Main Authors: | , , , , , , , , , , , , |
Other Authors: | , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
Format: | Article in Journal/Newspaper |
Language: | English |
Published: |
HAL CCSD
2015
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Subjects: | |
Online Access: | https://hal.science/hal-01444897 https://hal.science/hal-01444897/document https://hal.science/hal-01444897/file/Environ%20Microbiol_Jan%202015_merged_1410106529.pdf https://doi.org/10.1111/1462-2920.12699 |
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ftsorbonneuniv:oai:HAL:hal-01444897v1 |
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institution |
Open Polar |
collection |
HAL Sorbonne Université |
op_collection_id |
ftsorbonneuniv |
language |
English |
topic |
VIRULENCE METALLOPROTEASE CHOLERAE HEMAGGLUTININ PROTEASE CRASSOSTREA-GIGAS PACIFIC OYSTERS ACL LETHALITY FAMILY ALGORITHMS MORTALITIES CONSTRUCTION MESH: Animals MESH: Frameshift Mutation MESH: France MESH: Genes Regulator MESH: Genomics MESH: Ostreidae MESH: Phylogeny MESH: Protein Kinases MESH: Vibrio MESH: Virulence [SDV]Life Sciences [q-bio] [SDE.BE]Environmental Sciences/Biodiversity and Ecology |
spellingShingle |
VIRULENCE METALLOPROTEASE CHOLERAE HEMAGGLUTININ PROTEASE CRASSOSTREA-GIGAS PACIFIC OYSTERS ACL LETHALITY FAMILY ALGORITHMS MORTALITIES CONSTRUCTION MESH: Animals MESH: Frameshift Mutation MESH: France MESH: Genes Regulator MESH: Genomics MESH: Ostreidae MESH: Phylogeny MESH: Protein Kinases MESH: Vibrio MESH: Virulence [SDV]Life Sciences [q-bio] [SDE.BE]Environmental Sciences/Biodiversity and Ecology Goudenège, David Travers, Marie Agnès Lemire, Astrid Haffner, Philippe Labreuche, Yannick Tourbiez, Delphine Petton, Bruno Mangenot, Sophie Calteau, Alexandra Mazel, Didier Nicolas, Jean Louis Jacq, Annick Le Roux, Frédérique A single regulatory gene is sufficient to alter Vibrio aestuarianus pathogenicity in oysters |
topic_facet |
VIRULENCE METALLOPROTEASE CHOLERAE HEMAGGLUTININ PROTEASE CRASSOSTREA-GIGAS PACIFIC OYSTERS ACL LETHALITY FAMILY ALGORITHMS MORTALITIES CONSTRUCTION MESH: Animals MESH: Frameshift Mutation MESH: France MESH: Genes Regulator MESH: Genomics MESH: Ostreidae MESH: Phylogeny MESH: Protein Kinases MESH: Vibrio MESH: Virulence [SDV]Life Sciences [q-bio] [SDE.BE]Environmental Sciences/Biodiversity and Ecology |
description |
A utilisé MicroScope Platform International audience Oyster diseases caused by pathogenic vibrios pose a major challenge to the sustainability of oyster farming. In France, since 2012 a disease affecting specifically adult oysters has been associated with the presence of Vibrio aestuarianus. Here, by combining genome comparison, phylogenetic analyses and high-throughput infections of strains isolated before or during the recent outbreaks, we show that virulent strains cluster into two V. aestuarianus lineages independently of the sampling dates. The bacterial lethal dose was not different between strains isolated before or after 2012. Hence, the emergence of a new highly virulent clonal strain is unlikely. Each lineage comprises nearly identical strains, the majority of them being virulent, suggesting that within these phylogenetically coherent virulent lineages a few strains have lost their pathogenicity. Comparative genomics allowed the identification of a single frameshift in a non-virulent strain. This mutation affects the varS gene that codes for a signal transduction histidine-protein kinase. Genetic analyses confirmed that varS is necessary for infection of oysters and for a secreted metalloprotease expression. For the first time in a Vibrio species, we show here that VarS is a key factor of pathogenicity. |
author2 |
Physiologie Fonctionnelle des Organismes Marins (PFOM) Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER) Unité Santé, Génétique et Microbiologie des Mollusques (SGMM) Station biologique de Roscoff = Roscoff Marine Station (SBR) Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS) Laboratoire des Sciences de l'Environnement Marin (LEMAR) (LEMAR) Institut de Recherche pour le Développement (IRD)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Université de Brest (UBO)-Institut Universitaire Européen de la Mer (IUEM) Institut de Recherche pour le Développement (IRD)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS) Institut de Génomique d'Evry (IG) Université Paris-Saclay-Institut de Biologie François JACOB (JACOB) Direction de Recherche Fondamentale (CEA) (DRF (CEA)) Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Direction de Recherche Fondamentale (CEA) (DRF (CEA)) Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA) Analyse Bio-Informatique pour la Génomique et le Métabolisme (LABGeM) Génomique métabolique (UMR 8030) Genoscope - Centre national de séquençage Evry (GENOSCOPE) Université Paris-Saclay-Direction de Recherche Fondamentale (CEA) (DRF (CEA)) Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Direction de Recherche Fondamentale (CEA) (DRF (CEA)) Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université d'Évry-Val-d'Essonne (UEVE)-Centre National de la Recherche Scientifique (CNRS)-Genoscope - Centre national de séquençage Evry (GENOSCOPE) Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université d'Évry-Val-d'Essonne (UEVE)-Centre National de la Recherche Scientifique (CNRS) Plasticité du Génome Bactérien - Bacterial Genome Plasticity (PGB) Institut Pasteur Paris (IP)-Centre National de la Recherche Scientifique (CNRS) Institut de génétique et microbiologie Orsay (IGM) Université Paris-Sud - Paris 11 (UP11)-Centre National de la Recherche Scientifique (CNRS) The present study has been supported by the DPMA (Convention DPMA 2013- IFREMER 12/1210320/NYF), the ANR Blanc (11-BSV7-023-01 «VIBRIOGEN», D. G. funding), the EMBRC France (A. L. funding) and the ANR Bioadapt (13-ADAP-0007-01 «OPOPOP»). We warmly thank Dr Maurizio Labbate (University of Technology, Sydney, Australia), Dr Maxime Bruto (Station Biologique de Roscoff) and Dr Marianne Alunno-Bruscia (Ifremer Argenton) for critically reading the manuscript. We also thank Pr Joël Henry and Dr Céline Zatylny-Gaudin (Université de Caen Basse-Normandie, Institut de Biologie Fondamentale et Appliquée) for kindly performing mass spectrometry analyses. We thank Dr Carla Pruzzo (University of Genoa, Italy) and Dr Ana Roque (IRTA, Spain) for providing U_17 and KB19 strains. We acknowledge the staff of the station Ifremer Argenton, La Tremblade, Bouin, particularly Max Nourry, the ABIMS (SBR Roscoff) and LABGeM (Evry) platforms for technical support. MicroScope Platform ANR-11-BSV7-0023,VIBRIOGEN,Les vibrios pathogènes d'invertébrés marins : un nouveau regard sur la virulence et les réservoirs de gènes permettant l'adaptation à la niche écologique(2011) ANR-13-ADAP-0007,OPOPOP,Emergence de pathogènes opportunistes d'huîtres dans des populations naturelles de Vibrio(2013) |
format |
Article in Journal/Newspaper |
author |
Goudenège, David Travers, Marie Agnès Lemire, Astrid Haffner, Philippe Labreuche, Yannick Tourbiez, Delphine Petton, Bruno Mangenot, Sophie Calteau, Alexandra Mazel, Didier Nicolas, Jean Louis Jacq, Annick Le Roux, Frédérique |
author_facet |
Goudenège, David Travers, Marie Agnès Lemire, Astrid Haffner, Philippe Labreuche, Yannick Tourbiez, Delphine Petton, Bruno Mangenot, Sophie Calteau, Alexandra Mazel, Didier Nicolas, Jean Louis Jacq, Annick Le Roux, Frédérique |
author_sort |
Goudenège, David |
title |
A single regulatory gene is sufficient to alter Vibrio aestuarianus pathogenicity in oysters |
title_short |
A single regulatory gene is sufficient to alter Vibrio aestuarianus pathogenicity in oysters |
title_full |
A single regulatory gene is sufficient to alter Vibrio aestuarianus pathogenicity in oysters |
title_fullStr |
A single regulatory gene is sufficient to alter Vibrio aestuarianus pathogenicity in oysters |
title_full_unstemmed |
A single regulatory gene is sufficient to alter Vibrio aestuarianus pathogenicity in oysters |
title_sort |
single regulatory gene is sufficient to alter vibrio aestuarianus pathogenicity in oysters |
publisher |
HAL CCSD |
publishDate |
2015 |
url |
https://hal.science/hal-01444897 https://hal.science/hal-01444897/document https://hal.science/hal-01444897/file/Environ%20Microbiol_Jan%202015_merged_1410106529.pdf https://doi.org/10.1111/1462-2920.12699 |
geographic |
Pacific |
geographic_facet |
Pacific |
genre |
Crassostrea gigas |
genre_facet |
Crassostrea gigas |
op_source |
ISSN: 1462-2912 EISSN: 1462-2920 Environmental Microbiology https://hal.science/hal-01444897 Environmental Microbiology, 2015, 17 (11), pp.4189-4199. ⟨10.1111/1462-2920.12699⟩ |
op_relation |
info:eu-repo/semantics/altIdentifier/doi/10.1111/1462-2920.12699 info:eu-repo/semantics/altIdentifier/pmid/25384557 hal-01444897 https://hal.science/hal-01444897 https://hal.science/hal-01444897/document https://hal.science/hal-01444897/file/Environ%20Microbiol_Jan%202015_merged_1410106529.pdf doi:10.1111/1462-2920.12699 PUBMED: 25384557 |
op_rights |
info:eu-repo/semantics/OpenAccess |
op_doi |
https://doi.org/10.1111/1462-2920.12699 |
container_title |
Environmental Microbiology |
container_volume |
17 |
container_issue |
11 |
container_start_page |
4189 |
op_container_end_page |
4199 |
_version_ |
1802643560572387328 |
spelling |
ftsorbonneuniv:oai:HAL:hal-01444897v1 2024-06-23T07:52:18+00:00 A single regulatory gene is sufficient to alter Vibrio aestuarianus pathogenicity in oysters Goudenège, David Travers, Marie Agnès Lemire, Astrid Haffner, Philippe Labreuche, Yannick Tourbiez, Delphine Petton, Bruno Mangenot, Sophie Calteau, Alexandra Mazel, Didier Nicolas, Jean Louis Jacq, Annick Le Roux, Frédérique Physiologie Fonctionnelle des Organismes Marins (PFOM) Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER) Unité Santé, Génétique et Microbiologie des Mollusques (SGMM) Station biologique de Roscoff = Roscoff Marine Station (SBR) Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS) Laboratoire des Sciences de l'Environnement Marin (LEMAR) (LEMAR) Institut de Recherche pour le Développement (IRD)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Université de Brest (UBO)-Institut Universitaire Européen de la Mer (IUEM) Institut de Recherche pour le Développement (IRD)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS) Institut de Génomique d'Evry (IG) Université Paris-Saclay-Institut de Biologie François JACOB (JACOB) Direction de Recherche Fondamentale (CEA) (DRF (CEA)) Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Direction de Recherche Fondamentale (CEA) (DRF (CEA)) Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA) Analyse Bio-Informatique pour la Génomique et le Métabolisme (LABGeM) Génomique métabolique (UMR 8030) Genoscope - Centre national de séquençage Evry (GENOSCOPE) Université Paris-Saclay-Direction de Recherche Fondamentale (CEA) (DRF (CEA)) Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Direction de Recherche Fondamentale (CEA) (DRF (CEA)) Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université d'Évry-Val-d'Essonne (UEVE)-Centre National de la Recherche Scientifique (CNRS)-Genoscope - Centre national de séquençage Evry (GENOSCOPE) Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université d'Évry-Val-d'Essonne (UEVE)-Centre National de la Recherche Scientifique (CNRS) Plasticité du Génome Bactérien - Bacterial Genome Plasticity (PGB) Institut Pasteur Paris (IP)-Centre National de la Recherche Scientifique (CNRS) Institut de génétique et microbiologie Orsay (IGM) Université Paris-Sud - Paris 11 (UP11)-Centre National de la Recherche Scientifique (CNRS) The present study has been supported by the DPMA (Convention DPMA 2013- IFREMER 12/1210320/NYF), the ANR Blanc (11-BSV7-023-01 «VIBRIOGEN», D. G. funding), the EMBRC France (A. L. funding) and the ANR Bioadapt (13-ADAP-0007-01 «OPOPOP»). We warmly thank Dr Maurizio Labbate (University of Technology, Sydney, Australia), Dr Maxime Bruto (Station Biologique de Roscoff) and Dr Marianne Alunno-Bruscia (Ifremer Argenton) for critically reading the manuscript. We also thank Pr Joël Henry and Dr Céline Zatylny-Gaudin (Université de Caen Basse-Normandie, Institut de Biologie Fondamentale et Appliquée) for kindly performing mass spectrometry analyses. We thank Dr Carla Pruzzo (University of Genoa, Italy) and Dr Ana Roque (IRTA, Spain) for providing U_17 and KB19 strains. We acknowledge the staff of the station Ifremer Argenton, La Tremblade, Bouin, particularly Max Nourry, the ABIMS (SBR Roscoff) and LABGeM (Evry) platforms for technical support. MicroScope Platform ANR-11-BSV7-0023,VIBRIOGEN,Les vibrios pathogènes d'invertébrés marins : un nouveau regard sur la virulence et les réservoirs de gènes permettant l'adaptation à la niche écologique(2011) ANR-13-ADAP-0007,OPOPOP,Emergence de pathogènes opportunistes d'huîtres dans des populations naturelles de Vibrio(2013) 2015-11-25 https://hal.science/hal-01444897 https://hal.science/hal-01444897/document https://hal.science/hal-01444897/file/Environ%20Microbiol_Jan%202015_merged_1410106529.pdf https://doi.org/10.1111/1462-2920.12699 en eng HAL CCSD Society for Applied Microbiology and Wiley-Blackwell info:eu-repo/semantics/altIdentifier/doi/10.1111/1462-2920.12699 info:eu-repo/semantics/altIdentifier/pmid/25384557 hal-01444897 https://hal.science/hal-01444897 https://hal.science/hal-01444897/document https://hal.science/hal-01444897/file/Environ%20Microbiol_Jan%202015_merged_1410106529.pdf doi:10.1111/1462-2920.12699 PUBMED: 25384557 info:eu-repo/semantics/OpenAccess ISSN: 1462-2912 EISSN: 1462-2920 Environmental Microbiology https://hal.science/hal-01444897 Environmental Microbiology, 2015, 17 (11), pp.4189-4199. ⟨10.1111/1462-2920.12699⟩ VIRULENCE METALLOPROTEASE CHOLERAE HEMAGGLUTININ PROTEASE CRASSOSTREA-GIGAS PACIFIC OYSTERS ACL LETHALITY FAMILY ALGORITHMS MORTALITIES CONSTRUCTION MESH: Animals MESH: Frameshift Mutation MESH: France MESH: Genes Regulator MESH: Genomics MESH: Ostreidae MESH: Phylogeny MESH: Protein Kinases MESH: Vibrio MESH: Virulence [SDV]Life Sciences [q-bio] [SDE.BE]Environmental Sciences/Biodiversity and Ecology info:eu-repo/semantics/article Journal articles 2015 ftsorbonneuniv https://doi.org/10.1111/1462-2920.12699 2024-06-06T23:49:24Z A utilisé MicroScope Platform International audience Oyster diseases caused by pathogenic vibrios pose a major challenge to the sustainability of oyster farming. In France, since 2012 a disease affecting specifically adult oysters has been associated with the presence of Vibrio aestuarianus. Here, by combining genome comparison, phylogenetic analyses and high-throughput infections of strains isolated before or during the recent outbreaks, we show that virulent strains cluster into two V. aestuarianus lineages independently of the sampling dates. The bacterial lethal dose was not different between strains isolated before or after 2012. Hence, the emergence of a new highly virulent clonal strain is unlikely. Each lineage comprises nearly identical strains, the majority of them being virulent, suggesting that within these phylogenetically coherent virulent lineages a few strains have lost their pathogenicity. Comparative genomics allowed the identification of a single frameshift in a non-virulent strain. This mutation affects the varS gene that codes for a signal transduction histidine-protein kinase. Genetic analyses confirmed that varS is necessary for infection of oysters and for a secreted metalloprotease expression. For the first time in a Vibrio species, we show here that VarS is a key factor of pathogenicity. Article in Journal/Newspaper Crassostrea gigas HAL Sorbonne Université Pacific Environmental Microbiology 17 11 4189 4199 |