The major outer membrane protein OmpU of Vibrio splendidus contributes to host antimicrobial peptide resistance and is required for virulence in the oyster Crassostrea gigas

International audience Vibrio splendidus, strain LGP32, is an oyster pathogen associated with the summer mortalities affecting the production of Crassostrea gigas oysters worldwide. Vibrio splendidus LGP32 was shown to resist to up to 10 microM Cg-Def defensin and Cg-BPI bactericidal permeability in...

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Published in:Environmental Microbiology
Main Authors: Duperthuy, Marylise, Binesse, Johan, Le Roux, Frédérique, Romestand, Bernard, Caro, Audrey, Got, Patrice, Givaudan, Alain, Mazel, Didier, Bachère, Evelyne, Destoumieux-Garzón, Delphine
Other Authors: Université Montpellier 2 - Sciences et Techniques (UM2), Ecosystèmes lagunaires : organisation biologique et fonctionnement (ECOLAG), Université Montpellier 2 - Sciences et Techniques (UM2)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Centre National de la Recherche Scientifique (CNRS), Plasticité du Génome Bactérien (PGB), Institut Pasteur Paris -Centre National de la Recherche Scientifique (CNRS), Laboratoire de Génétique et Pathologie (LGP), Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER), Ecologie microbienne des insectes et interactions hôte-pathogène (EMIP), Institut National de la Recherche Agronomique (INRA)-Université Montpellier 2 - Sciences et Techniques (UM2), This work received financial support from Ifremer and CNRS. It was awarded a “chercheur(se) d'avenir” grant from the Languedoc-Roussillon region.
Format: Article in Journal/Newspaper
Language:English
Published: HAL CCSD 2010
Subjects:
Online Access:https://hal.inrae.fr/hal-02667966
https://doi.org/10.1111/j.1462-2920.2009.02138.x
id ftccsdartic:oai:HAL:hal-02667966v1
record_format openpolar
institution Open Polar
collection Archive ouverte HAL (Hyper Article en Ligne, CCSD - Centre pour la Communication Scientifique Directe)
op_collection_id ftccsdartic
language English
topic OYSTER
HUITRE CREUSE
OmpU
MESH: Adhesins
Bacterial
MESH: Animals
MESH: Vibrio Infections
MESH: Virulence
MESH: Antimicrobial Cationic Peptides
MESH: Blood Proteins
MESH: Crassostrea
MESH: Gene Deletion
MESH: Genetic Complementation Test
MESH: Humans
MESH: Mutation
MESH: Vibrio
[SDV.MP]Life Sciences [q-bio]/Microbiology and Parasitology
spellingShingle OYSTER
HUITRE CREUSE
OmpU
MESH: Adhesins
Bacterial
MESH: Animals
MESH: Vibrio Infections
MESH: Virulence
MESH: Antimicrobial Cationic Peptides
MESH: Blood Proteins
MESH: Crassostrea
MESH: Gene Deletion
MESH: Genetic Complementation Test
MESH: Humans
MESH: Mutation
MESH: Vibrio
[SDV.MP]Life Sciences [q-bio]/Microbiology and Parasitology
Duperthuy, Marylise
Binesse, Johan
Le Roux, Frédérique
Romestand, Bernard
Caro, Audrey
Got, Patrice
Givaudan, Alain
Mazel, Didier
Bachère, Evelyne
Destoumieux-Garzón, Delphine
The major outer membrane protein OmpU of Vibrio splendidus contributes to host antimicrobial peptide resistance and is required for virulence in the oyster Crassostrea gigas
topic_facet OYSTER
HUITRE CREUSE
OmpU
MESH: Adhesins
Bacterial
MESH: Animals
MESH: Vibrio Infections
MESH: Virulence
MESH: Antimicrobial Cationic Peptides
MESH: Blood Proteins
MESH: Crassostrea
MESH: Gene Deletion
MESH: Genetic Complementation Test
MESH: Humans
MESH: Mutation
MESH: Vibrio
[SDV.MP]Life Sciences [q-bio]/Microbiology and Parasitology
description International audience Vibrio splendidus, strain LGP32, is an oyster pathogen associated with the summer mortalities affecting the production of Crassostrea gigas oysters worldwide. Vibrio splendidus LGP32 was shown to resist to up to 10 microM Cg-Def defensin and Cg-BPI bactericidal permeability increasing protein, two antimicrobial peptides/proteins (AMPs) involved in C. gigas immunity. The resistance to both oyster Cg-Def and Cg-BPI and standard AMPs (polymyxin B, protegrin, human BPI) was dependent on the ompU gene. Indeed, upon ompU inactivation, minimal bactericidal concentrations decreased by up to fourfold. AMP resistance was restored upon ectopic expression of ompU. The susceptibility of bacterial membranes to AMP-induced damages was independent of the ompU-mediated AMP resistance. Besides its role in AMP resistance, ompU proved to be essential for the adherence of V. splendidus LGP32 to fibronectin. Interestingly, in vivo, ompU was identified as a major determinant of V. splendidus pathogenicity in oyster experimental infections. Indeed, the V. splendidus-induced oyster mortalities dropped from 56% to 11% upon ompU mutation (Kaplan-Meier survival curves, P < 0.01). Moreover, in co-infection assays, the ompU mutant was out competed by the wild-type strain with competitive indexes in the range of 0.1-0.2. From this study, ompU is required for virulence of V. splendidus. Contributing to AMP resistance, conferring adhesive properties to V. splendidus, and being essential for in vivo fitness, the OmpU porin appears as an essential effector of the C. gigas/V. splendidus interaction.
author2 Université Montpellier 2 - Sciences et Techniques (UM2)
Ecosystèmes lagunaires : organisation biologique et fonctionnement (ECOLAG)
Université Montpellier 2 - Sciences et Techniques (UM2)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Centre National de la Recherche Scientifique (CNRS)
Plasticité du Génome Bactérien (PGB)
Institut Pasteur Paris -Centre National de la Recherche Scientifique (CNRS)
Laboratoire de Génétique et Pathologie (LGP)
Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)
Ecologie microbienne des insectes et interactions hôte-pathogène (EMIP)
Institut National de la Recherche Agronomique (INRA)-Université Montpellier 2 - Sciences et Techniques (UM2)
This work received financial support from Ifremer and CNRS. It was awarded a “chercheur(se) d'avenir” grant from the Languedoc-Roussillon region.
format Article in Journal/Newspaper
author Duperthuy, Marylise
Binesse, Johan
Le Roux, Frédérique
Romestand, Bernard
Caro, Audrey
Got, Patrice
Givaudan, Alain
Mazel, Didier
Bachère, Evelyne
Destoumieux-Garzón, Delphine
author_facet Duperthuy, Marylise
Binesse, Johan
Le Roux, Frédérique
Romestand, Bernard
Caro, Audrey
Got, Patrice
Givaudan, Alain
Mazel, Didier
Bachère, Evelyne
Destoumieux-Garzón, Delphine
author_sort Duperthuy, Marylise
title The major outer membrane protein OmpU of Vibrio splendidus contributes to host antimicrobial peptide resistance and is required for virulence in the oyster Crassostrea gigas
title_short The major outer membrane protein OmpU of Vibrio splendidus contributes to host antimicrobial peptide resistance and is required for virulence in the oyster Crassostrea gigas
title_full The major outer membrane protein OmpU of Vibrio splendidus contributes to host antimicrobial peptide resistance and is required for virulence in the oyster Crassostrea gigas
title_fullStr The major outer membrane protein OmpU of Vibrio splendidus contributes to host antimicrobial peptide resistance and is required for virulence in the oyster Crassostrea gigas
title_full_unstemmed The major outer membrane protein OmpU of Vibrio splendidus contributes to host antimicrobial peptide resistance and is required for virulence in the oyster Crassostrea gigas
title_sort major outer membrane protein ompu of vibrio splendidus contributes to host antimicrobial peptide resistance and is required for virulence in the oyster crassostrea gigas
publisher HAL CCSD
publishDate 2010
url https://hal.inrae.fr/hal-02667966
https://doi.org/10.1111/j.1462-2920.2009.02138.x
long_lat ENVELOPE(-45.900,-45.900,-60.633,-60.633)
geographic Meier
geographic_facet Meier
genre Crassostrea gigas
genre_facet Crassostrea gigas
op_source ISSN: 1462-2912
EISSN: 1462-2920
Environmental Microbiology
https://hal.inrae.fr/hal-02667966
Environmental Microbiology, Society for Applied Microbiology and Wiley-Blackwell, 2010, 12 (4), pp.951-963. &#x27E8;10.1111/j.1462-2920.2009.02138.x&#x27E9;
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doi:10.1111/j.1462-2920.2009.02138.x
PRODINRA: 41123
PUBMED: 20074236
WOS: 000277029900010
op_doi https://doi.org/10.1111/j.1462-2920.2009.02138.x
container_title Environmental Microbiology
container_volume 12
container_issue 4
container_start_page 951
op_container_end_page 963
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spelling ftccsdartic:oai:HAL:hal-02667966v1 2023-05-15T15:58:24+02:00 The major outer membrane protein OmpU of Vibrio splendidus contributes to host antimicrobial peptide resistance and is required for virulence in the oyster Crassostrea gigas Duperthuy, Marylise Binesse, Johan Le Roux, Frédérique Romestand, Bernard Caro, Audrey Got, Patrice Givaudan, Alain Mazel, Didier Bachère, Evelyne Destoumieux-Garzón, Delphine Université Montpellier 2 - Sciences et Techniques (UM2) Ecosystèmes lagunaires : organisation biologique et fonctionnement (ECOLAG) Université Montpellier 2 - Sciences et Techniques (UM2)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Centre National de la Recherche Scientifique (CNRS) Plasticité du Génome Bactérien (PGB) Institut Pasteur Paris -Centre National de la Recherche Scientifique (CNRS) Laboratoire de Génétique et Pathologie (LGP) Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER) Ecologie microbienne des insectes et interactions hôte-pathogène (EMIP) Institut National de la Recherche Agronomique (INRA)-Université Montpellier 2 - Sciences et Techniques (UM2) This work received financial support from Ifremer and CNRS. It was awarded a “chercheur(se) d'avenir” grant from the Languedoc-Roussillon region. 2010 https://hal.inrae.fr/hal-02667966 https://doi.org/10.1111/j.1462-2920.2009.02138.x en eng HAL CCSD Society for Applied Microbiology and Wiley-Blackwell info:eu-repo/semantics/altIdentifier/doi/10.1111/j.1462-2920.2009.02138.x info:eu-repo/semantics/altIdentifier/pmid/20074236 hal-02667966 https://hal.inrae.fr/hal-02667966 doi:10.1111/j.1462-2920.2009.02138.x PRODINRA: 41123 PUBMED: 20074236 WOS: 000277029900010 ISSN: 1462-2912 EISSN: 1462-2920 Environmental Microbiology https://hal.inrae.fr/hal-02667966 Environmental Microbiology, Society for Applied Microbiology and Wiley-Blackwell, 2010, 12 (4), pp.951-963. &#x27E8;10.1111/j.1462-2920.2009.02138.x&#x27E9; OYSTER HUITRE CREUSE OmpU MESH: Adhesins Bacterial MESH: Animals MESH: Vibrio Infections MESH: Virulence MESH: Antimicrobial Cationic Peptides MESH: Blood Proteins MESH: Crassostrea MESH: Gene Deletion MESH: Genetic Complementation Test MESH: Humans MESH: Mutation MESH: Vibrio [SDV.MP]Life Sciences [q-bio]/Microbiology and Parasitology info:eu-repo/semantics/article Journal articles 2010 ftccsdartic https://doi.org/10.1111/j.1462-2920.2009.02138.x 2021-12-25T23:41:12Z International audience Vibrio splendidus, strain LGP32, is an oyster pathogen associated with the summer mortalities affecting the production of Crassostrea gigas oysters worldwide. Vibrio splendidus LGP32 was shown to resist to up to 10 microM Cg-Def defensin and Cg-BPI bactericidal permeability increasing protein, two antimicrobial peptides/proteins (AMPs) involved in C. gigas immunity. The resistance to both oyster Cg-Def and Cg-BPI and standard AMPs (polymyxin B, protegrin, human BPI) was dependent on the ompU gene. Indeed, upon ompU inactivation, minimal bactericidal concentrations decreased by up to fourfold. AMP resistance was restored upon ectopic expression of ompU. The susceptibility of bacterial membranes to AMP-induced damages was independent of the ompU-mediated AMP resistance. Besides its role in AMP resistance, ompU proved to be essential for the adherence of V. splendidus LGP32 to fibronectin. Interestingly, in vivo, ompU was identified as a major determinant of V. splendidus pathogenicity in oyster experimental infections. Indeed, the V. splendidus-induced oyster mortalities dropped from 56% to 11% upon ompU mutation (Kaplan-Meier survival curves, P < 0.01). Moreover, in co-infection assays, the ompU mutant was out competed by the wild-type strain with competitive indexes in the range of 0.1-0.2. From this study, ompU is required for virulence of V. splendidus. Contributing to AMP resistance, conferring adhesive properties to V. splendidus, and being essential for in vivo fitness, the OmpU porin appears as an essential effector of the C. gigas/V. splendidus interaction. Article in Journal/Newspaper Crassostrea gigas Archive ouverte HAL (Hyper Article en Ligne, CCSD - Centre pour la Communication Scientifique Directe) Meier ENVELOPE(-45.900,-45.900,-60.633,-60.633) Environmental Microbiology 12 4 951 963