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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Online Access: | http://www.ncbi.nlm.nih.gov/pmc/articles/PMC9167547/ http://www.ncbi.nlm.nih.gov/pubmed/35659369 https://doi.org/10.1186/s40168-022-01280-5 |
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ftpubmed:oai:pubmedcentral.nih.gov:9167547 2023-05-15T15:57:51+02:00 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 2022-06-04 http://www.ncbi.nlm.nih.gov/pmc/articles/PMC9167547/ http://www.ncbi.nlm.nih.gov/pubmed/35659369 https://doi.org/10.1186/s40168-022-01280-5 en eng BioMed Central http://www.ncbi.nlm.nih.gov/pmc/articles/PMC9167547/ http://www.ncbi.nlm.nih.gov/pubmed/35659369 http://dx.doi.org/10.1186/s40168-022-01280-5 © 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. CC0 PDM CC-BY Microbiome Research Text 2022 ftpubmed https://doi.org/10.1186/s40168-022-01280-5 2022-06-12T00:42:11Z 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. Text Crassostrea gigas Pacific oyster PubMed Central (PMC) Pacific Microbiome 10 1 |
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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 |
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Research |
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. |
format |
Text |
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 |
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 |
BioMed Central |
publishDate |
2022 |
url |
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC9167547/ http://www.ncbi.nlm.nih.gov/pubmed/35659369 https://doi.org/10.1186/s40168-022-01280-5 |
geographic |
Pacific |
geographic_facet |
Pacific |
genre |
Crassostrea gigas Pacific oyster |
genre_facet |
Crassostrea gigas Pacific oyster |
op_source |
Microbiome |
op_relation |
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC9167547/ http://www.ncbi.nlm.nih.gov/pubmed/35659369 http://dx.doi.org/10.1186/s40168-022-01280-5 |
op_rights |
© 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. |
op_rightsnorm |
CC0 PDM CC-BY |
op_doi |
https://doi.org/10.1186/s40168-022-01280-5 |
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Microbiome |
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10 |
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1766393568715341824 |