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

Type Article
Date 2022-06
Language English
Author(s) Fallet Manon7, Montagnani Caroline1, Petton Bruno2, Dantan Luc7, de Lorgeril JulienORCID1, 3, Comarmond Sébastien7, Chaparro Cristian7, Toulza Eve7, Boitard Simon4, Escoubas Jean Michel8, Vergnes Agnes1, Le Grand Jacqueline2, Bulla Ingo7, Gueguen Yannick1, 5, Vidal-Dupiol Jeremie1, Grunau Christoph7, Mitta Guillaume6, 7, Cossau Céline7
Affiliation(s) 1 : IHPE, CNRS, Ifremer, Univ. Montpellier, Univ. Perpignan via Domitia, Perpignan, France
2 : Ifremer, UBO CNRS IRD, LEMAR UMR 6539, Argenton, France
3 : Ifremer, IRD, Univ Nouvelle-Calédonie, Univ La Réunion, ENTROPIE, F-98800, Nouméa, Nouvelle-Calédonie, France
4 : CBGP, CIRAD, INRAE, Institut Agro, IRD, Université de Montpellier, Montpellier, France
5 : MARBEC, CNRS, Ifremer, IRD, Univ Montpellier, Sète, France
6 : Ifremer, UMR 241 Écosystèmes Insulaires Océaniens, Labex Corail, Centre Ifremer du Pacifique, BP 49, 98725, Tahiti, French Polynesia
7 : IHPE, CNRS, Ifremer, Univ. Montpellier, Univ. Perpignan via Domitia, Perpignan, France
8 : IHPE, CNRS, Ifremer, Univ. Montpellier, Univ. Perpignan via Domitia, Perpignan, France
Source Microbiome (2049-2618) (BMC), 2022-06 , Vol. 10 , N. 1 , P. 85 (21p.)
DOI 10.1186/s40168-022-01280-5
Keyword(s) Oyster, Aquaculture, Microbiota, Innate immune shaping, Epigenetic, DNA methylation
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.

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Additional file 1: Additional information related to the methodology (the origin of the biological samples , the experimental design for disease induction, the bioinformatic pipelines) 679 KB Open access
Additional file 2: Quality of the metrics for omic analysis (sheet 1: transcriptomic, sheet 2: genetic, sheet 3: epigenomic) 22 KB Open access
Additional file 3: Supplementary results on the phenotypes (Fertilisation success and survival rate of oysters) and on omics data (table 2 = genetic, table 3 = transcriptomic, table 4 = epigenomic,... 488 KB Open access
Additional file 4: OTU tables for 16S barcoding analysis. Each sheet correspond to a different time point. 157 KB Open access
Additional file 5: Results of two differential analyses comparing the proportion of OTUs: (1) ME exposed oysters vs control oysters and (2) ME water vs control water 13 KB Open access
Additional file 6: Compilation of differentially expressed genes at the time point indicated (All DEGs = all the differentially expressed genes, Other sheets = Immune related genes) 2 MB Open access
Additional file 7: Compilation of the RBGOA biological function which are significantly enriched in the transcriptomic dataset for each time point 68 KB Open access
Additional file 8: Compilation the differenttially expressed genes related to metabolic functions at the time point indicated 24 KB Open access
Additional file 9: Compilation of differentially methylated regions in any regions of the genomes (DMRs), within gene bodies (DMGs), within promoter regions (DMPs) 2 MB Open access
Additional file 10: Compilation the RBGOA biological functions which are significantly enriched in the epigenomic dataset for each time point (sheet 1 to 4) and comparison with RBGOA function from the 20 KB Open access
Additional file 11: Details for the statistical analysis performed to adress the significance of the inheritence in DMRs patterns 338 KB Open access
Publisher's official version 21 2 MB Open access
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How to cite 

Fallet Manon, Montagnani Caroline, Petton Bruno, Dantan Luc, de Lorgeril Julien, Comarmond Sébastien, Chaparro Cristian, Toulza Eve, Boitard Simon, Escoubas Jean Michel, Vergnes Agnes, Le Grand Jacqueline, Bulla Ingo, Gueguen Yannick, Vidal-Dupiol Jeremie, Grunau Christoph, Mitta Guillaume, Cossau Céline (2022). Early life microbial exposures shape the Crassostrea gigas immune system for lifelong and intergenerational disease protection. Microbiome, 10(1), 85 (21p.). Publisher's official version : https://doi.org/10.1186/s40168-022-01280-5 , Open Access version : https://archimer.ifremer.fr/doc/00753/86457/