Early life microbial exposures shape the Crassostrea gigas immune system for lifelong and intergenerational disease protection

Manon Fallet (1) , C. Montagnani (1) , Bruno Petton (2) , Luc Dantan (1) , Julien de Lorgeril (1, 3) , Sébastien Comarmond (1) , Cristian Chaparro (1) , Eve Toulza (1) , Jean-Michel Escoubas (1) , Agnès Vergnes (1) , Yannick Gueguen (1) , Ingo Bulla (1) , Jacqueline Le Grand (2) , Jérémie Vidal-Dupiol (1) , Christoph Grunau (1) , Simon Boitard (4) , Guillaume Mitta (1, 5, 6) , Céline Cosseau (1)

1 IHPE - Interactions Hôtes-Pathogènes-Environnements
2 LEMAR - Laboratoire des Sciences de l'Environnement Marin (LEMAR)
3 ENTROPIE [Réunion] - Ecologie marine tropicale dans les Océans Pacifique et Indien
4 UMR CBGP - Centre de Biologie pour la Gestion des Populations
5 EIO - Ecosystèmes Insulaires Océaniens (UMR 241)
6 LabEX CORAIL - Laboratoire d'Excellence CORAIL

Background: The interaction of organisms with their surrounding microbial communities influences many biological processes, a notable example of which is the shaping of the immune system in early life. In the Pacific oyster, Crassostrea gigas , the role of the environmental microbial community on immune system maturation – and, importantly, protection from infectious disease – is still an open question. Results: Here, we demonstrate that early life microbial exposure durably improves oyster survival when challenged with the pathogen causing Pacific Oyster Mortality Syndrome (POMS), both in the exposed generation and in the subsequent one. Combining microbiota, transcriptomic, genetic, and epigenetic analyses, we show that the microbial exposure induced changes in epigenetic marks and a reprogramming of immune gene expression leading to long-term and intergenerational immune protection against POMS. Conclusions: We anticipate that this protection likely extends to additional pathogens and may prove to be an important new strategy for safeguarding oyster aquaculture efforts from infectious disease.

Mots clés: Oyster; Aquaculture; Microbiota; Innate immune shaping; Epigenetic; DNA methylation

Domaines: Zoologie des invertébrés; Génomique, Transcriptomique et Protéomique [q-bio.GN]; Immunité innée

Manon Fallet, C. Montagnani, Bruno Petton, Luc Dantan, Julien de Lorgeril, et al.. Early life microbial exposures shape the Crassostrea gigas immune system for lifelong and intergenerational disease protection. Microbiome, 2022, 10, pp.85. ⟨10.1186/s40168-022-01280-5⟩. ⟨hal-03635473v2⟩