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

Abstract

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.

Distinct modes of holobiont specialization among cryptic coral lineages

“…Increasing temperatures associated with global climate change can disrupt partnerships between corals and their photobionts by compromising photosynthetic activity, which can trigger photobiont loss (Baird et al, 2009;Weis, 2008) and disruption of bacterial communities (Vompe et al, 2024;Voolstra et al, 2024). The resultant nutritionally compromised "bleached" state can ultimately lead to mortality (Hughes et al, 2017).…”

“…Due to this tight partnership, variation in thermal tolerance among lineages is therefore likely the result of local adaptation in host and strain-level variation in photobiont associations, as well as interactions between other important holobiont members, such as bacteria (e.g., Ziegler et al, 2017). Bacterial communities of massive Porites are generally dominated by members of the family Endozoicomonadaceae, which can provide a variety of services to the coral holobiont, including nutritional benefits (Fifer et al, 2022;Pogoreutz & Ziegler, 2024;Vompe et al, 2024). However, high temperatures can disrupt partnerships with Endozoicomonadaceae, leading to shifts to less beneficial microbial communities (Vompe et al, 2024; but see Hadaidi et al, 2017).…”

“…Bacterial communities of massive Porites are generally dominated by members of the family Endozoicomonadaceae, which can provide a variety of services to the coral holobiont, including nutritional benefits (Fifer et al, 2022;Pogoreutz & Ziegler, 2024;Vompe et al, 2024). However, high temperatures can disrupt partnerships with Endozoicomonadaceae, leading to shifts to less beneficial microbial communities (Vompe et al, 2024; but see Hadaidi et al, 2017).…”