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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ftsorbonneuniv:oai:HAL:hal-01936591v1 2024-09-15T18:03:15+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 ftsorbonneuniv https://doi.org/10.1038/s41396-018-0245-3 2024-08-30T00:00:54Z 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 HAL Sorbonne Université The ISME Journal 12 12 2954 2966 |
institution |
Open Polar |
collection |
HAL Sorbonne Université |
op_collection_id |
ftsorbonneuniv |
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 |
_version_ |
1810440767093604352 |