Metaproteome analysis of the coral holobiont demonstrates algal symbiont dampening under thermal stress

Abstract

The accelerating loss of coral reefs worldwide due to anthropogenic climate change has led to a myriad of studies aimed at understanding the basis of coral resilience to support reef conservation. Here, we integrate physiological measurements with proteomic and metabolomic profiles to examine species-specific responses to increased temperature in three sympatric reef-building corals from the Great Barrier Reef: Acropora hyacinthus, Porites lobata, and Stylophora pistillata. We find species-specific stress response strategies with A. hyacinthus, a thermally sensitive species, exhibiting rapid decline in endosymbiont physiology, coupled with a one-third reduction in protein abundance. In contrast, P. lobata displayed a delayed physiological response to stress and a muted proteome response, suggesting greater resilience. S. pistillata initially showed minor shifts in the proteome followed by colony "bail-out". Overall, we observed markedly different responses in most biochemical pathways in the three coral species. Nonetheless, some known biomarkers of stress, including heat-shock proteins, showed conserved responses to thermal stress with differences in temporal abundance reflecting bleaching resistance. Our results underscore the species-specific nature of coral responses to thermal stress and highlight proteomic signatures associated with symbiosis breakdown, offering mechanistic insights into coral bleaching susceptibility and resilience.