Proteome and microbiota analyses characterizing dynamic coral-algae-microbe tripartite interactions under simulated rapid ocean acidification.

Ocean acidification (OA) is a pressing issue currently and in the future for coral reefs. The importance of maintenance interactions among partners of the holobiont association in the stress response is well appreciated; however, the candidate molecular and microbial mechanisms that underlie holobiont stress resilience or susceptibility remain unclear. Here, to assess the effects of rapid pH change on coral holobionts at both the protein and microbe levels, combined proteomics and microbiota analyses of the scleractinian coral Galaxea fascicularis exposed to three relevant OA scenarios, including current (pH = 8.15), preindustrial (pH = 8.45) and future IPCC-2100 scenarios (pH = 7.85), were conducted. The results demonstrated that pH changes had no significant effect on the physiological calcification rate of G. fascicularis in a 10-day experiment; however, significant differences were recorded in the proteome and 16S profiling. Proteome variance analysis identified some of the core biological pathways in coral holobionts, including coral host infection and immune defence, and maintaining metabolic compatibility involved in energy homeostasis, nutrient cycling, antibiotic activity and carbon budgets of coral-Symbiodiniaceae interactions were key mechanisms in the early OA stress response. Furthermore, microbiota changes indicate substantial microbial community and functional disturbances in response to OA stress, potentially compromising holobiont health and fitness. Our results may help to elucidate many complex mechanisms to describe scleractinian coral holobiont responses to OA and raise interesting questions for future studies.