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

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 imm...

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Autores principales: Fallet, Manon, Montagnani, Caroline, Petton, Bruno, Dantan, Luc, de Lorgeril, Julien, Comarmond, Sébastien, Chaparro, Cristian, Toulza, Eve, Boitard, Simon, Escoubas, Jean-Michel, Vergnes, Agnès, Le Grand, Jacqueline, Bulla, Ingo, Gueguen, Yannick, Vidal-Dupiol, Jérémie, Grunau, Christoph, Mitta, Guillaume, Cosseau, Céline
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9167547/
https://www.ncbi.nlm.nih.gov/pubmed/35659369
http://dx.doi.org/10.1186/s40168-022-01280-5
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author Fallet, Manon
Montagnani, Caroline
Petton, Bruno
Dantan, Luc
de Lorgeril, Julien
Comarmond, Sébastien
Chaparro, Cristian
Toulza, Eve
Boitard, Simon
Escoubas, Jean-Michel
Vergnes, Agnès
Le Grand, Jacqueline
Bulla, Ingo
Gueguen, Yannick
Vidal-Dupiol, Jérémie
Grunau, Christoph
Mitta, Guillaume
Cosseau, Céline
author_facet Fallet, Manon
Montagnani, Caroline
Petton, Bruno
Dantan, Luc
de Lorgeril, Julien
Comarmond, Sébastien
Chaparro, Cristian
Toulza, Eve
Boitard, Simon
Escoubas, Jean-Michel
Vergnes, Agnès
Le Grand, Jacqueline
Bulla, Ingo
Gueguen, Yannick
Vidal-Dupiol, Jérémie
Grunau, Christoph
Mitta, Guillaume
Cosseau, Céline
author_sort Fallet, Manon
collection PubMed
description 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 SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-022-01280-5.
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spelling pubmed-91675472022-06-06 Early life microbial exposures shape the Crassostrea gigas immune system for lifelong and intergenerational disease protection Fallet, Manon Montagnani, Caroline Petton, Bruno Dantan, Luc de Lorgeril, Julien Comarmond, Sébastien Chaparro, Cristian Toulza, Eve Boitard, Simon Escoubas, Jean-Michel Vergnes, Agnès Le Grand, Jacqueline Bulla, Ingo Gueguen, Yannick Vidal-Dupiol, Jérémie Grunau, Christoph Mitta, Guillaume Cosseau, Céline Microbiome Research 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 SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-022-01280-5. BioMed Central 2022-06-04 /pmc/articles/PMC9167547/ /pubmed/35659369 http://dx.doi.org/10.1186/s40168-022-01280-5 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Fallet, Manon
Montagnani, Caroline
Petton, Bruno
Dantan, Luc
de Lorgeril, Julien
Comarmond, Sébastien
Chaparro, Cristian
Toulza, Eve
Boitard, Simon
Escoubas, Jean-Michel
Vergnes, Agnès
Le Grand, Jacqueline
Bulla, Ingo
Gueguen, Yannick
Vidal-Dupiol, Jérémie
Grunau, Christoph
Mitta, Guillaume
Cosseau, Céline
Early life microbial exposures shape the Crassostrea gigas immune system for lifelong and intergenerational disease protection
title 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_short 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
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9167547/
https://www.ncbi.nlm.nih.gov/pubmed/35659369
http://dx.doi.org/10.1186/s40168-022-01280-5
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