Ancestral gene acquisition as the key to virulence potential in environmental Vibrio populations

International audience Diseases of marine animals caused by bacteria of the genus Vibrio are on the rise worldwide. Understanding the eco-evolutionary dynamics of these infectious agents is important for predicting and managing these diseases. Yet, compared to Vibrio infecting humans, knowledge of t...

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Published in:The ISME Journal
Main Authors: Bruto, Maxime, Labreuche, Yannick, James, Adèle, Piel, Damien, Chenivesse, Sabine, Petton, Bruno, Polz, Martin, F, Le Roux, Frédérique
Other Authors: Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER), 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), MIT Parsons Laboratory, Massachusetts Institute of Technology (MIT), ANR-16-CE32-0008,REVENGE,L'huître comme niche de l'évolution et l'émergence de vibrios pathogènes(2016)
Format: Article in Journal/Newspaper
Language:English
Published: HAL CCSD 2018
Subjects:
ACL
Online Access:https://hal.science/hal-01936591
https://hal.science/hal-01936591/document
https://hal.science/hal-01936591/file/s41396-018-0245-3.pdf
https://doi.org/10.1038/s41396-018-0245-3
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record_format openpolar
spelling ftinsu:oai:HAL:hal-01936591v1 2024-04-28T08:16:40+00:00 Ancestral gene acquisition as the key to virulence potential in environmental Vibrio populations Bruto, Maxime Labreuche, Yannick James, Adèle Piel, Damien Chenivesse, Sabine Petton, Bruno Polz, Martin, F Le Roux, Frédérique Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER) 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) MIT Parsons Laboratory Massachusetts Institute of Technology (MIT) ANR-16-CE32-0008,REVENGE,L'huître comme niche de l'évolution et l'émergence de vibrios pathogènes(2016) 2018-12 https://hal.science/hal-01936591 https://hal.science/hal-01936591/document https://hal.science/hal-01936591/file/s41396-018-0245-3.pdf https://doi.org/10.1038/s41396-018-0245-3 en eng HAL CCSD Nature Publishing Group info:eu-repo/semantics/altIdentifier/doi/10.1038/s41396-018-0245-3 hal-01936591 https://hal.science/hal-01936591 https://hal.science/hal-01936591/document https://hal.science/hal-01936591/file/s41396-018-0245-3.pdf doi:10.1038/s41396-018-0245-3 info:eu-repo/semantics/OpenAccess ISSN: 1751-7362 EISSN: 1751-7370 The International Society of Microbiologial Ecology Journal https://hal.science/hal-01936591 The International Society of Microbiologial Ecology Journal, 2018, 12 (12), pp.2954 - 2966. ⟨10.1038/s41396-018-0245-3⟩ ACL Functional genomics Microbial ecology Molecular evolution [SDV.MP.BAC]Life Sciences [q-bio]/Microbiology and Parasitology/Bacteriology [SDV.GEN.GPO]Life Sciences [q-bio]/Genetics/Populations and Evolution [q-bio.PE] [SDE.BE]Environmental Sciences/Biodiversity and Ecology info:eu-repo/semantics/article Journal articles 2018 ftinsu https://doi.org/10.1038/s41396-018-0245-3 2024-04-05T00:44:36Z International audience Diseases of marine animals caused by bacteria of the genus Vibrio are on the rise worldwide. Understanding the eco-evolutionary dynamics of these infectious agents is important for predicting and managing these diseases. Yet, compared to Vibrio infecting humans, knowledge of their role as animal pathogens is scarce. Here we ask how widespread is virulence among ecologically differentiated Vibrio populations, and what is the nature and frequency of virulence genes within these populations? We use a combination of population genomics and molecular genetics to assay hundreds of Vibrio strains for their virulence in the oyster Crassostrea gigas, a unique animal model that allows high-throughput infection assays. We show that within the diverse Splendidus clade, virulence represents an ancestral trait but has been lost from several populations. Two loci are necessary for virulence, the first being widely distributed across the Splendidus clade and consisting of an exported conserved protein (R5.7). The second is a MARTX toxin cluster, which only occurs within V. splendidus and is for the first time associated with virulence in marine invertebrates. Varying frequencies of both loci among populations indicate different selective pressures and alternative ecological roles, based on which we suggest strategies for epidemiological surveys. Article in Journal/Newspaper Crassostrea gigas Institut national des sciences de l'Univers: HAL-INSU The ISME Journal 12 12 2954 2966
institution Open Polar
collection Institut national des sciences de l'Univers: HAL-INSU
op_collection_id ftinsu
language English
topic ACL
Functional genomics
Microbial ecology
Molecular evolution
[SDV.MP.BAC]Life Sciences [q-bio]/Microbiology and Parasitology/Bacteriology
[SDV.GEN.GPO]Life Sciences [q-bio]/Genetics/Populations and Evolution [q-bio.PE]
[SDE.BE]Environmental Sciences/Biodiversity and Ecology
spellingShingle ACL
Functional genomics
Microbial ecology
Molecular evolution
[SDV.MP.BAC]Life Sciences [q-bio]/Microbiology and Parasitology/Bacteriology
[SDV.GEN.GPO]Life Sciences [q-bio]/Genetics/Populations and Evolution [q-bio.PE]
[SDE.BE]Environmental Sciences/Biodiversity and Ecology
Bruto, Maxime
Labreuche, Yannick
James, Adèle
Piel, Damien
Chenivesse, Sabine
Petton, Bruno
Polz, Martin, F
Le Roux, Frédérique
Ancestral gene acquisition as the key to virulence potential in environmental Vibrio populations
topic_facet ACL
Functional genomics
Microbial ecology
Molecular evolution
[SDV.MP.BAC]Life Sciences [q-bio]/Microbiology and Parasitology/Bacteriology
[SDV.GEN.GPO]Life Sciences [q-bio]/Genetics/Populations and Evolution [q-bio.PE]
[SDE.BE]Environmental Sciences/Biodiversity and Ecology
description International audience Diseases of marine animals caused by bacteria of the genus Vibrio are on the rise worldwide. Understanding the eco-evolutionary dynamics of these infectious agents is important for predicting and managing these diseases. Yet, compared to Vibrio infecting humans, knowledge of their role as animal pathogens is scarce. Here we ask how widespread is virulence among ecologically differentiated Vibrio populations, and what is the nature and frequency of virulence genes within these populations? We use a combination of population genomics and molecular genetics to assay hundreds of Vibrio strains for their virulence in the oyster Crassostrea gigas, a unique animal model that allows high-throughput infection assays. We show that within the diverse Splendidus clade, virulence represents an ancestral trait but has been lost from several populations. Two loci are necessary for virulence, the first being widely distributed across the Splendidus clade and consisting of an exported conserved protein (R5.7). The second is a MARTX toxin cluster, which only occurs within V. splendidus and is for the first time associated with virulence in marine invertebrates. Varying frequencies of both loci among populations indicate different selective pressures and alternative ecological roles, based on which we suggest strategies for epidemiological surveys.
author2 Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)
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)
MIT Parsons Laboratory
Massachusetts Institute of Technology (MIT)
ANR-16-CE32-0008,REVENGE,L'huître comme niche de l'évolution et l'émergence de vibrios pathogènes(2016)
format Article in Journal/Newspaper
author Bruto, Maxime
Labreuche, Yannick
James, Adèle
Piel, Damien
Chenivesse, Sabine
Petton, Bruno
Polz, Martin, F
Le Roux, Frédérique
author_facet Bruto, Maxime
Labreuche, Yannick
James, Adèle
Piel, Damien
Chenivesse, Sabine
Petton, Bruno
Polz, Martin, F
Le Roux, Frédérique
author_sort Bruto, Maxime
title Ancestral gene acquisition as the key to virulence potential in environmental Vibrio populations
title_short Ancestral gene acquisition as the key to virulence potential in environmental Vibrio populations
title_full Ancestral gene acquisition as the key to virulence potential in environmental Vibrio populations
title_fullStr Ancestral gene acquisition as the key to virulence potential in environmental Vibrio populations
title_full_unstemmed Ancestral gene acquisition as the key to virulence potential in environmental Vibrio populations
title_sort ancestral gene acquisition as the key to virulence potential in environmental vibrio populations
publisher HAL CCSD
publishDate 2018
url https://hal.science/hal-01936591
https://hal.science/hal-01936591/document
https://hal.science/hal-01936591/file/s41396-018-0245-3.pdf
https://doi.org/10.1038/s41396-018-0245-3
genre Crassostrea gigas
genre_facet Crassostrea gigas
op_source ISSN: 1751-7362
EISSN: 1751-7370
The International Society of Microbiologial Ecology Journal
https://hal.science/hal-01936591
The International Society of Microbiologial Ecology Journal, 2018, 12 (12), pp.2954 - 2966. ⟨10.1038/s41396-018-0245-3⟩
op_relation info:eu-repo/semantics/altIdentifier/doi/10.1038/s41396-018-0245-3
hal-01936591
https://hal.science/hal-01936591
https://hal.science/hal-01936591/document
https://hal.science/hal-01936591/file/s41396-018-0245-3.pdf
doi:10.1038/s41396-018-0245-3
op_rights info:eu-repo/semantics/OpenAccess
op_doi https://doi.org/10.1038/s41396-018-0245-3
container_title The ISME Journal
container_volume 12
container_issue 12
container_start_page 2954
op_container_end_page 2966
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