» Articles » PMID: 35659369

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 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.

Citing Articles

Hemolymph microbiota and immune effectors' expressions driven by geographical rearing acclimation of the aquacultured Penaeus stylirostris.

Perez V, Boulo V, de Lorgeril J, Pham D, Ansquer D, Plougoulen G Anim Microbiome. 2025; 7(1):5.

PMID: 39799372 PMC: 11725212. DOI: 10.1186/s42523-025-00376-1.


Parent-Specific Transgenerational Immune Priming Enhances Offspring Defense-Unless Heat Stress Negates It All.

Schneider R, Dubin A, Marten S, Roth O Ecol Evol. 2024; 14(11):e70552.

PMID: 39588349 PMC: 11586686. DOI: 10.1002/ece3.70552.


Hatchery type influences the gill microbiome of Atlantic farmed salmon (Salmo salar) after transfer to sea.

Stewart K, Boerlage A, Barr W, Ijaz U, Smith C Anim Microbiome. 2024; 6(1):65.

PMID: 39516952 PMC: 11549768. DOI: 10.1186/s42523-024-00347-y.


Microbial education plays a crucial role in harnessing the beneficial properties of microbiota for infectious disease protection in Crassostrea gigas.

Dantan L, Carcassonne P, Degremont L, Morga B, Travers M, Petton B Sci Rep. 2024; 14(1):26914.

PMID: 39505929 PMC: 11541537. DOI: 10.1038/s41598-024-76096-4.


Diseases of marine fish and shellfish in an age of rapid climate change.

Rowley A, Baker-Austin C, Boerlage A, Caillon C, Davies C, Duperret L iScience. 2024; 27(9):110838.

PMID: 39318536 PMC: 11420459. DOI: 10.1016/j.isci.2024.110838.


References
1.
Zhang T, Qiu L, Sun Z, Wang L, Zhou Z, Liu R . The specifically enhanced cellular immune responses in Pacific oyster (Crassostrea gigas) against secondary challenge with Vibrio splendidus. Dev Comp Immunol. 2014; 45(1):141-50. DOI: 10.1016/j.dci.2014.02.015. View

2.
Pan W, Sommer F, Falk-Paulsen M, Ulas T, Best L, Fazio A . Exposure to the gut microbiota drives distinct methylome and transcriptome changes in intestinal epithelial cells during postnatal development. Genome Med. 2018; 10(1):27. PMC: 5899322. DOI: 10.1186/s13073-018-0534-5. View

3.
Ichinohe T, Pang I, Kumamoto Y, Peaper D, Ho J, Murray T . Microbiota regulates immune defense against respiratory tract influenza A virus infection. Proc Natl Acad Sci U S A. 2011; 108(13):5354-9. PMC: 3069176. DOI: 10.1073/pnas.1019378108. View

4.
de Lorgeril J, Lucasson A, Petton B, Toulza E, Montagnani C, Clerissi C . Immune-suppression by OsHV-1 viral infection causes fatal bacteraemia in Pacific oysters. Nat Commun. 2018; 9(1):4215. PMC: 6182001. DOI: 10.1038/s41467-018-06659-3. View

5.
Lafont M, Vergnes A, Vidal-Dupiol J, de Lorgeril J, Gueguen Y, Haffner P . A Sustained Immune Response Supports Long-Term Antiviral Immune Priming in the Pacific Oyster, Crassostrea gigas. mBio. 2020; 11(2). PMC: 7064767. DOI: 10.1128/mBio.02777-19. View