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

Abstract 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 communit...

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Published in:Microbiome
Main Authors: Manon Fallet, Caroline Montagnani, Bruno Petton, Luc Dantan, Julien de Lorgeril, Sébastien Comarmond, Cristian Chaparro, Eve Toulza, Simon Boitard, Jean-Michel Escoubas, Agnès Vergnes, Jacqueline Le Grand, Ingo Bulla, Yannick Gueguen, Jérémie Vidal-Dupiol, Christoph Grunau, Guillaume Mitta, Céline Cosseau
Format: Article in Journal/Newspaper
Language:English
Published: BMC 2022
Subjects:
Online Access:https://doi.org/10.1186/s40168-022-01280-5
https://doaj.org/article/297fecc7f9314cc98ea991c74702f997
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spelling ftdoajarticles:oai:doaj.org/article:297fecc7f9314cc98ea991c74702f997 2023-05-15T15:57:52+02:00 Early life microbial exposures shape the Crassostrea gigas immune system for lifelong and intergenerational disease protection Manon Fallet Caroline Montagnani Bruno Petton Luc Dantan Julien de Lorgeril Sébastien Comarmond Cristian Chaparro Eve Toulza Simon Boitard Jean-Michel Escoubas Agnès Vergnes Jacqueline Le Grand Ingo Bulla Yannick Gueguen Jérémie Vidal-Dupiol Christoph Grunau Guillaume Mitta Céline Cosseau 2022-06-01T00:00:00Z https://doi.org/10.1186/s40168-022-01280-5 https://doaj.org/article/297fecc7f9314cc98ea991c74702f997 EN eng BMC https://doi.org/10.1186/s40168-022-01280-5 https://doaj.org/toc/2049-2618 doi:10.1186/s40168-022-01280-5 2049-2618 https://doaj.org/article/297fecc7f9314cc98ea991c74702f997 Microbiome, Vol 10, Iss 1, Pp 1-21 (2022) Oyster Aquaculture Microbiota Innate immune shaping Epigenetic DNA methylation Microbial ecology QR100-130 article 2022 ftdoajarticles https://doi.org/10.1186/s40168-022-01280-5 2022-12-30T21:37:09Z Abstract 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. tag the videobyte/videoabstract in this section Video Abstract Article in Journal/Newspaper Crassostrea gigas Pacific oyster Directory of Open Access Journals: DOAJ Articles Pacific Microbiome 10 1
institution Open Polar
collection Directory of Open Access Journals: DOAJ Articles
op_collection_id ftdoajarticles
language English
topic Oyster
Aquaculture
Microbiota
Innate immune shaping
Epigenetic
DNA methylation
Microbial ecology
QR100-130
spellingShingle Oyster
Aquaculture
Microbiota
Innate immune shaping
Epigenetic
DNA methylation
Microbial ecology
QR100-130
Manon Fallet
Caroline Montagnani
Bruno Petton
Luc Dantan
Julien de Lorgeril
Sébastien Comarmond
Cristian Chaparro
Eve Toulza
Simon Boitard
Jean-Michel Escoubas
Agnès Vergnes
Jacqueline Le Grand
Ingo Bulla
Yannick Gueguen
Jérémie Vidal-Dupiol
Christoph Grunau
Guillaume Mitta
Céline Cosseau
Early life microbial exposures shape the Crassostrea gigas immune system for lifelong and intergenerational disease protection
topic_facet Oyster
Aquaculture
Microbiota
Innate immune shaping
Epigenetic
DNA methylation
Microbial ecology
QR100-130
description Abstract 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. tag the videobyte/videoabstract in this section Video Abstract
format Article in Journal/Newspaper
author Manon Fallet
Caroline Montagnani
Bruno Petton
Luc Dantan
Julien de Lorgeril
Sébastien Comarmond
Cristian Chaparro
Eve Toulza
Simon Boitard
Jean-Michel Escoubas
Agnès Vergnes
Jacqueline Le Grand
Ingo Bulla
Yannick Gueguen
Jérémie Vidal-Dupiol
Christoph Grunau
Guillaume Mitta
Céline Cosseau
author_facet Manon Fallet
Caroline Montagnani
Bruno Petton
Luc Dantan
Julien de Lorgeril
Sébastien Comarmond
Cristian Chaparro
Eve Toulza
Simon Boitard
Jean-Michel Escoubas
Agnès Vergnes
Jacqueline Le Grand
Ingo Bulla
Yannick Gueguen
Jérémie Vidal-Dupiol
Christoph Grunau
Guillaume Mitta
Céline Cosseau
author_sort Manon Fallet
title Early life microbial exposures shape the Crassostrea gigas immune system for lifelong and intergenerational disease protection
title_short Early life microbial exposures shape the Crassostrea gigas immune system for lifelong and intergenerational disease protection
title_full Early life microbial exposures shape the Crassostrea gigas immune system for lifelong and intergenerational disease protection
title_fullStr Early life microbial exposures shape the Crassostrea gigas immune system for lifelong and intergenerational disease protection
title_full_unstemmed Early life microbial exposures shape the Crassostrea gigas immune system for lifelong and intergenerational disease protection
title_sort early life microbial exposures shape the crassostrea gigas immune system for lifelong and intergenerational disease protection
publisher BMC
publishDate 2022
url https://doi.org/10.1186/s40168-022-01280-5
https://doaj.org/article/297fecc7f9314cc98ea991c74702f997
geographic Pacific
geographic_facet Pacific
genre Crassostrea gigas
Pacific oyster
genre_facet Crassostrea gigas
Pacific oyster
op_source Microbiome, Vol 10, Iss 1, Pp 1-21 (2022)
op_relation https://doi.org/10.1186/s40168-022-01280-5
https://doaj.org/toc/2049-2618
doi:10.1186/s40168-022-01280-5
2049-2618
https://doaj.org/article/297fecc7f9314cc98ea991c74702f997
op_doi https://doi.org/10.1186/s40168-022-01280-5
container_title Microbiome
container_volume 10
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