Resilience in a time of stress: revealing the molecular underpinnings of coral survival following thermal bleaching events

Abstract

Coral bleaching events from thermal stress are increasing globally in duration, frequency, and intensity. Bleaching occurs when a corals algal symbionts are expelled, resulting in a loss of color. Some coral colonies survive bleaching, reacquire their symbionts and recover. In this study, we experimentally bleached Montipora capitata colonies to examine molecular and physiological signatures of intrinsic differences between corals that recover (resilient) compared to those that die (susceptible). All colonies were collected from the same bay and monitored for eight months post-bleaching to identify specific colonies exhibiting long-term resilience and survival. Using an integrated systems-biology approach that included quantitative mass spectrometry-based proteomics, 16S rRNA of the microbiome, total lipids, symbiont density and diversity, we explored molecular-level mechanisms of tolerance in pre- and post-bleached colonies and found biomarkers of resilience that can confidently identify resilient and susceptible corals before thermal-induced bleaching events. Prior to thermal stress, resilient corals were characterized by a more diverse microbiome and increased abundances of proteins involved in multiple carbon and nitrogen acquisition strategies, symbiont retention and acquisition, and pathogen resistance. Susceptible corals had early signs of symbiont rejection and had resorted to utilizing urea uptake pathways for carbon and nitrogen. Further, molecular signatures identified prior to bleaching were amplified after bleaching, suggesting these pathways may be deterministic in a colonys fate. Our results have important implications for the future of reefs, revealing molecular factors necessary for survival through thermally-induced bleaching events and providing diagnostic biomarkers for coral reef management. Significance statementCorals are being negatively impacted by the increase in the number and duration of thermal-induced bleaching events. There are, however, some individuals within a single species that will bleach and, after time, reacquire symbionts and physiologically recover while neighboring colonies will die. Here, we used a multidisciplinary approach to understand the biochemical details of the physiological changes of resilient and susceptible Montipora capitata to thermal-induced bleaching. Resilient corals were characterized by their use of multiple carbon and nitrogen acquisition strategies, metabolically active symbiont relationships, abundant antiviral proteins, and a diverse microbiome. We reveal a multi-factor molecular-level approach for confidently identifying resilient and susceptible coral colonies so that environmental managers can rapidly select quality candidates for propagation while in the field.