Microbiome ecological memory and responses to repeated marine heatwaves clarify variation in coral bleaching and mortality

Microbiomes are essential features of holobionts, providing their hosts with key metabolic and functional traits like resistance to environmental disturbances and diseases. In scleractinian corals, questions remain about the microbiome's role in resistance and resilience to factors contributing to the ongoing global coral decline and whether microbes serve as a form of holobiont ecological memory. To test if and how coral microbiomes affect host health outcomes during repeated disturbances, we conducted a large-scale (32 exclosures, 200 colonies, and 3 coral species sampled) and long-term (28 months, 2018-2020) manipulative experiment on the forereef of Mo'orea, French Polynesia. In 2019 and 2020, this reef experienced the two most severe marine heatwaves on record for the site. Our experiment and these events afforded us the opportunity to test microbiome dynamics and roles in the context of coral bleaching and mortality resulting from these successive and severe heatwaves. We report unique microbiome responses to repeated heatwaves in Acropora retusa, Porites lobata, and Pocillopora spp., which included: microbiome acclimatization in A. retusa, and both microbiome resilience to the first marine heatwave and microbiome resistance to the second marine heatwave in Pocillopora spp. Moreover, observed microbiome dynamics significantly correlated with coral species-specific phenotypes. For example, bleaching and mortality in A. retusa both significantly increased with greater microbiome beta dispersion and greater Shannon Diversity, while P. lobata colonies had different microbiomes across mortality prevalence. Compositional microbiome changes, such as changes to proportions of differentially abundant putatively beneficial to putatively detrimental taxa to coral health outcomes during repeated heat stress, also correlated with host mortality, with higher proportions of detrimental taxa yielding higher mortality in A. retusa. This study reveals evidence for coral species-specific microbial responses to repeated heatwaves and, importantly, suggests that host-dependent microbiome dynamics may provide a form of holobiont ecological memory to repeated heat stress. Severe marine heatwaves have been a major force behind the decline of coral reefs. However, some coral species seem to have an ecological memory of past heatwaves, and microbiomes may be the mechanism of such a memory. We found evidence for microbiome and coral ecological memory in Acropora retusa, microbiome and host health responses independent from marine heatwaves and high host mortality in Porites lobata, and microbiome ecological memory in Pocillopora spp.image