Cross-talk and mutual shaping between the immune system and the microbiota during an oyster's life
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,...
Published in: | Philosophical Transactions of the Royal Society B: Biological Sciences |
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crroyalsociety:10.1098/rstb.2023.0065 2024-06-02T08:05:37+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 Agence Nationale de la Recherche 2024 http://dx.doi.org/10.1098/rstb.2023.0065 https://royalsocietypublishing.org/doi/pdf/10.1098/rstb.2023.0065 https://royalsocietypublishing.org/doi/full-xml/10.1098/rstb.2023.0065 en eng The Royal Society http://creativecommons.org/licenses/by/4.0/ http://creativecommons.org/licenses/by/4.0/ Philosophical Transactions of the Royal Society B: Biological Sciences volume 379, issue 1901 ISSN 0962-8436 1471-2970 journal-article 2024 crroyalsociety https://doi.org/10.1098/rstb.2023.0065 2024-05-07T14:16:54Z 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 The Royal Society Pacific Philosophical Transactions of the Royal Society B: Biological Sciences 379 1901 |
institution |
Open Polar |
collection |
The Royal Society |
op_collection_id |
crroyalsociety |
language |
English |
description |
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 |
Agence Nationale de la Recherche |
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 |
spellingShingle |
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 |
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 |
The Royal Society |
publishDate |
2024 |
url |
http://dx.doi.org/10.1098/rstb.2023.0065 https://royalsocietypublishing.org/doi/pdf/10.1098/rstb.2023.0065 https://royalsocietypublishing.org/doi/full-xml/10.1098/rstb.2023.0065 |
geographic |
Pacific |
geographic_facet |
Pacific |
genre |
Crassostrea gigas Pacific oyster |
genre_facet |
Crassostrea gigas Pacific oyster |
op_source |
Philosophical Transactions of the Royal Society B: Biological Sciences volume 379, issue 1901 ISSN 0962-8436 1471-2970 |
op_rights |
http://creativecommons.org/licenses/by/4.0/ http://creativecommons.org/licenses/by/4.0/ |
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 |
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1800750486697017344 |