Cross-talk and mutual shaping between the immune system and the microbiota during an oyster's life
International audience The Pacific oyster Crassostrea gigas lives in microbe-rich marine coastal systems subjected to rapid environmental changes. It harbours a diversified and fluctuating microbiota that cohabits with immune cells expressing a diversified immune gene repertoire. In the early stages...
Published in: | Philosophical Transactions of the Royal Society B: Biological Sciences |
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Main Authors: | , , , , , , , , , , |
Other Authors: | , , , , , , , |
Format: | Article in Journal/Newspaper |
Language: | English |
Published: |
HAL CCSD
2024
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Subjects: | |
Online Access: | https://hal.science/hal-04515139 https://hal.science/hal-04515139/document https://hal.science/hal-04515139/file/Destoumieux-2024-PhilTransRSocB-Cross-talk.pdf https://doi.org/10.1098/rstb.2023.0065 |
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ftanrparis:oai:HAL:hal-04515139v1 |
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record_format |
openpolar |
institution |
Open Polar |
collection |
Portail HAL-ANR (Agence Nationale de la Recherche) |
op_collection_id |
ftanrparis |
language |
English |
topic |
immunology microbiology health and disease and epidemiology holobiont microbiome immunity homeostasis immune priming ontogeny [SDE]Environmental Sciences |
spellingShingle |
immunology microbiology health and disease and epidemiology holobiont microbiome immunity homeostasis immune priming ontogeny [SDE]Environmental Sciences Destoumieux-Garzón, Delphine Montagnani, Caroline Dantan, Luc Nicolas, Noémie de San Travers, Marie-Agnès Duperret, Léo Charrière, Guillaume, M Toulza, Eve Mitta, Guillaume Cosseau, Céline Escoubas, Jean-Michel Cross-talk and mutual shaping between the immune system and the microbiota during an oyster's life |
topic_facet |
immunology microbiology health and disease and epidemiology holobiont microbiome immunity homeostasis immune priming ontogeny [SDE]Environmental Sciences |
description |
International audience The Pacific oyster Crassostrea gigas lives in microbe-rich marine coastal systems subjected to rapid environmental changes. It harbours a diversified and fluctuating microbiota that cohabits with immune cells expressing a diversified immune gene repertoire. In the early stages of oyster development, just after fertilization, the microbiota plays a key role in educating the immune system. Exposure to a rich microbial environment at the larval stage leads to an increase in immune competence throughout the life of the oyster, conferring a better protection against pathogenic infections at later juvenile/adult stages. This beneficial effect, which is intergenerational, is associated with epigenetic remodelling. At juvenile stages, the educated immune system participates in the control of the homeostasis. In particular, the microbiota is fine-tuned by oyster antimicrobial peptides acting through specific and synergistic effects. However, this balance is fragile, as illustrated by the Pacific Oyster Mortality Syndrome, a disease causing mass mortalities in oysters worldwide. In this disease, the weakening of oyster immune defences by OsHV-1 µVar virus induces a dysbiosis leading to fatal sepsis. This review illustrates the continuous interaction between the highly diversified oyster immune system and its dynamic microbiota throughout its life, and the importance of this cross-talk for oyster health. This article is part of the theme issue ‘Sculpting the microbiome: how host factors determine and respond to microbial colonization’. |
author2 |
Interactions Hôtes-Pathogènes-Environnements (IHPE) Université de Perpignan Via Domitia (UPVD)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM) Ecosystèmes Insulaires Océaniens (UMR 241) (EIO) Institut de Recherche pour le Développement (IRD)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Université de la Polynésie Française (UPF)-Institut Louis Malardé Papeete (ILM) Institut de Recherche pour le Développement (IRD) ANR-10-LABX-0004,CeMEB,Mediterranean Center for Environment and Biodiversity(2010) ANR-19-CE20-0004,DECICOMP,Déchiffrer toute la complexité du syndrome de mortalité des huîtres du Pacifique pour modéliser le risque épidémiologique.(2019) ANR-19-CE18-0025,MOSAR-DEF,Conception d'antimicrobiens actifs en milieu salin inspirée par la biodivesité marine.(2019) |
format |
Article in Journal/Newspaper |
author |
Destoumieux-Garzón, Delphine Montagnani, Caroline Dantan, Luc Nicolas, Noémie de San Travers, Marie-Agnès Duperret, Léo Charrière, Guillaume, M Toulza, Eve Mitta, Guillaume Cosseau, Céline Escoubas, Jean-Michel |
author_facet |
Destoumieux-Garzón, Delphine Montagnani, Caroline Dantan, Luc Nicolas, Noémie de San Travers, Marie-Agnès Duperret, Léo Charrière, Guillaume, M Toulza, Eve Mitta, Guillaume Cosseau, Céline Escoubas, Jean-Michel |
author_sort |
Destoumieux-Garzón, Delphine |
title |
Cross-talk and mutual shaping between the immune system and the microbiota during an oyster's life |
title_short |
Cross-talk and mutual shaping between the immune system and the microbiota during an oyster's life |
title_full |
Cross-talk and mutual shaping between the immune system and the microbiota during an oyster's life |
title_fullStr |
Cross-talk and mutual shaping between the immune system and the microbiota during an oyster's life |
title_full_unstemmed |
Cross-talk and mutual shaping between the immune system and the microbiota during an oyster's life |
title_sort |
cross-talk and mutual shaping between the immune system and the microbiota during an oyster's life |
publisher |
HAL CCSD |
publishDate |
2024 |
url |
https://hal.science/hal-04515139 https://hal.science/hal-04515139/document https://hal.science/hal-04515139/file/Destoumieux-2024-PhilTransRSocB-Cross-talk.pdf https://doi.org/10.1098/rstb.2023.0065 |
genre |
Crassostrea gigas Pacific oyster |
genre_facet |
Crassostrea gigas Pacific oyster |
op_source |
ISSN: 0962-8436 EISSN: 1471-2970 Philosophical Transactions of the Royal Society B: Biological Sciences https://hal.science/hal-04515139 Philosophical Transactions of the Royal Society B: Biological Sciences, 2024, 379 (1901), ⟨10.1098/rstb.2023.0065⟩ https://royalsocietypublishing.org/doi/full/10.1098/rstb.2023.0065 |
op_relation |
info:eu-repo/semantics/altIdentifier/doi/10.1098/rstb.2023.0065 hal-04515139 https://hal.science/hal-04515139 https://hal.science/hal-04515139/document https://hal.science/hal-04515139/file/Destoumieux-2024-PhilTransRSocB-Cross-talk.pdf doi:10.1098/rstb.2023.0065 |
op_rights |
info:eu-repo/semantics/OpenAccess |
op_doi |
https://doi.org/10.1098/rstb.2023.0065 |
container_title |
Philosophical Transactions of the Royal Society B: Biological Sciences |
container_volume |
379 |
container_issue |
1901 |
_version_ |
1810440776406007808 |
spelling |
ftanrparis:oai:HAL:hal-04515139v1 2024-09-15T18:03:16+00:00 Cross-talk and mutual shaping between the immune system and the microbiota during an oyster's life Destoumieux-Garzón, Delphine Montagnani, Caroline Dantan, Luc Nicolas, Noémie de San Travers, Marie-Agnès Duperret, Léo Charrière, Guillaume, M Toulza, Eve Mitta, Guillaume Cosseau, Céline Escoubas, Jean-Michel Interactions Hôtes-Pathogènes-Environnements (IHPE) Université de Perpignan Via Domitia (UPVD)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM) Ecosystèmes Insulaires Océaniens (UMR 241) (EIO) Institut de Recherche pour le Développement (IRD)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Université de la Polynésie Française (UPF)-Institut Louis Malardé Papeete (ILM) Institut de Recherche pour le Développement (IRD) ANR-10-LABX-0004,CeMEB,Mediterranean Center for Environment and Biodiversity(2010) ANR-19-CE20-0004,DECICOMP,Déchiffrer toute la complexité du syndrome de mortalité des huîtres du Pacifique pour modéliser le risque épidémiologique.(2019) ANR-19-CE18-0025,MOSAR-DEF,Conception d'antimicrobiens actifs en milieu salin inspirée par la biodivesité marine.(2019) 2024-03-18 https://hal.science/hal-04515139 https://hal.science/hal-04515139/document https://hal.science/hal-04515139/file/Destoumieux-2024-PhilTransRSocB-Cross-talk.pdf https://doi.org/10.1098/rstb.2023.0065 en eng HAL CCSD Royal Society, The info:eu-repo/semantics/altIdentifier/doi/10.1098/rstb.2023.0065 hal-04515139 https://hal.science/hal-04515139 https://hal.science/hal-04515139/document https://hal.science/hal-04515139/file/Destoumieux-2024-PhilTransRSocB-Cross-talk.pdf doi:10.1098/rstb.2023.0065 info:eu-repo/semantics/OpenAccess ISSN: 0962-8436 EISSN: 1471-2970 Philosophical Transactions of the Royal Society B: Biological Sciences https://hal.science/hal-04515139 Philosophical Transactions of the Royal Society B: Biological Sciences, 2024, 379 (1901), ⟨10.1098/rstb.2023.0065⟩ https://royalsocietypublishing.org/doi/full/10.1098/rstb.2023.0065 immunology microbiology health and disease and epidemiology holobiont microbiome immunity homeostasis immune priming ontogeny [SDE]Environmental Sciences info:eu-repo/semantics/article Journal articles 2024 ftanrparis https://doi.org/10.1098/rstb.2023.0065 2024-07-12T10:42:05Z International audience The Pacific oyster Crassostrea gigas lives in microbe-rich marine coastal systems subjected to rapid environmental changes. It harbours a diversified and fluctuating microbiota that cohabits with immune cells expressing a diversified immune gene repertoire. In the early stages of oyster development, just after fertilization, the microbiota plays a key role in educating the immune system. Exposure to a rich microbial environment at the larval stage leads to an increase in immune competence throughout the life of the oyster, conferring a better protection against pathogenic infections at later juvenile/adult stages. This beneficial effect, which is intergenerational, is associated with epigenetic remodelling. At juvenile stages, the educated immune system participates in the control of the homeostasis. In particular, the microbiota is fine-tuned by oyster antimicrobial peptides acting through specific and synergistic effects. However, this balance is fragile, as illustrated by the Pacific Oyster Mortality Syndrome, a disease causing mass mortalities in oysters worldwide. In this disease, the weakening of oyster immune defences by OsHV-1 µVar virus induces a dysbiosis leading to fatal sepsis. This review illustrates the continuous interaction between the highly diversified oyster immune system and its dynamic microbiota throughout its life, and the importance of this cross-talk for oyster health. This article is part of the theme issue ‘Sculpting the microbiome: how host factors determine and respond to microbial colonization’. Article in Journal/Newspaper Crassostrea gigas Pacific oyster Portail HAL-ANR (Agence Nationale de la Recherche) Philosophical Transactions of the Royal Society B: Biological Sciences 379 1901 |