Novel Strategies for Mitigating Disease Risks in Marine Bivalves: Immune Training and Microbial Education

Mollusks rank among the most diverse and abundant animal groups, both in terms of number of species and biomass. Marine mollusks, in particular, are a crucial component of the global food supply, significantly supporting aquaculture industries around the world. Due to socio-economic importance of these species, there is a great interest in studying mollusc immunity to mitigate the impact of infectious diseases that recurrently plague their productions. Recent discoveries on the adaptive abilities of the innate immune system to learn from past experiences, have spurred considerable interest in mollusk immunity. In bivalves, compelling evidence for the existence of innate immunological memory capacities (also called immune priming or training) came from studies on the Pacific oyster Crassostrea gigas, the most widely cultivated mollusk species globally.In this species, affected by recurrent mass mortalities notably caused by the herpes-like virus OsHV-1 µVar or vibrioses, we evidenced the potential to induce increased survival towards these pathogens in priming the immune system using either a viral mimic or inactivated natural pathogens but also following the early shaping of the immune system by microbiota-associated microorganisms. We showed that the exposure of oyster to the viral mimic called poly (I:C) or inactivated OsHV-1µVar can lead to long-term efficient protection by triggering a strong antiviral response preventing replication of the virus. We also demonstrated that early life microbial exposure could play a role in educating and training the immune system, durably enhancing oyster survival against OsHV-1 or Vibrio challenges. This beneficial effect was found to be maintained throughout the oyster’s lifespan and can even be passed on to subsequent generations. The memorization of this early microbial experience was associated with epigenetic remodeling and a reprogramming of immune gene expression.Overall, these findings reveal the remarkable ability of oysters to build an innate immune memory and adapt to their microbial environment. This knowledge opens up promising avenues for exploring novel strategies through immune training or microbial education to help mitigate disease risks in marine bivalves.