Pathogen priming reveals host immune training and microbiome conditioning in corals
Matteo MontiiD, Neus Garcías-BonetiD, Francisca C García, Érika P. SantoroiD, Ghaida M. AljuaidiD, Kevin Schuster, Chakkiath Paul AntonyiD, Marco CasartelliiD, Laura BeenhamiD, Aurora GiorgiiD, Luigi ColiniD, Christian Robert VoolstraiD, Raquel Silva PeixotoiD
Abstract
UNSTRUCTURED ABSTRACTIn several species, vaccine-like approaches, where hosts are primed through controlled pathogen exposure, have proven effective in enhancing responses to subsequent infections. This principle remains unexplored in corals. Here, we demonstrate that chronic exposure to non-lethal concentrations of live or inactivated Vibrio coralliilyticus primes the coral holobiont to counter subsequent infections under heat stress. Non-primed corals experienced greater heat stress pathogen-driven bleaching and a significant decline in their photosynthetic efficiency compared to primed samples. These results were linked to microbiome conditioning and host gene expression modulation, including a layered, fine-tuned immune and cellular response to microbial invasion. This proof-of-concept challenges strictly innate immune responses in corals and positions immune priming and microbiome conditioning as integrated mechanisms of coral holobiont resilience. Together, these findings can contribute to redefine coral immunity concepts and lay the groundwork for developing new microbiome-based strategies to enhance coral health for reef conservation under climate change. LAY SUMMARYCoral reefs are increasingly threatened by rising seawater temperatures and disease. Unlike vertebrates, corals do not possess a classical adaptive immune system, so they have been thought to rely only on innate defenses. However, our study shows that corals may be more capable than previously believed. We demonstrate that exposing corals to non-lethal doses of a widespread bacterial pathogen can train them to better withstand subsequent infections under heat stress. Corals that were not pre-exposed suffered more pathogen caused bleaching and showed a stronger decline in physiological performance, while those that were primed were more resilient. This improved resistance appears to come from two coordinated processes. First, the corals associated bacterial community shifted in a way that seems to help protect the host. Second, the coral itself adjusted its gene expression, mounting a more effective and controlled response to infection. These findings suggest that corals may be able to remember past exposures and respond more effectively to future infections, even without a traditional adaptive immune system, providing a foundation for developing new strategies to support coral resilience.
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