Cross-talk and mutual shaping between the immune system and the microbiota during an oyster's life

• Published in: Philosophical Transactions of the Royal Society B: Biological Sciences
• Main Authors: 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
• Other Authors: 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
• Language: English
• Published: HAL CCSD 2024
• Subjects: immunology; microbiology; health and disease and epidemiology holobiont; microbiome; immunity; homeostasis; immune priming; ontogeny; [SDE]Environmental Sciences; Crassostrea gigas; Pacific oyster
• 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

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’.