Different responses of scleractinian coral Acropora pruinosa from Weizhou Island during extreme high temperature events

Ecological surveys observe coral “winners” and “losers” in global coral bleaching events. However, the key contributors to holobiont tolerance and interactions between symbionts remain unclear. Herein, we compared bleaching and unbleaching Acropora pruinosa corals from Weizhou Island, during an extreme high-temperature event in the northern South China Sea in 2020. We found the dominant Symbiodiniaceae subclade in the bleaching and unbleaching corals to be C1; however, the density of Symbiodiniaceae in the latter was significantly higher than that in the former. Additionally, the symbiotic bacteria α diversity in the unbleaching coral was significantly higher than that in the bleaching coral, with a reorganized bacterial community structure. Core microbiome analyses revealed 55 bacterial core operational taxonomic units (OTUs), of which 10 were significantly differentially enriched between the two coral groups. The significantly enriched bacterial core OTUs in the unbleaching coral were primarily nitrogen cycling related, while those enriched in the bleaching coral were associated with antimicrobial activity. RNA-Seq analyses revealed that significantly upregulated genes in the bleaching coral were primarily associated with diseases and autophagy, while those in the unbleaching coral were associated with immune defense and maintenance of the symbiotic relationship between corals and symbionts. We propose that the differences in tolerance of A. pruinosa result from the cooperation between coral host, Symbiodiniaceae, and symbiotic bacteria. In extreme high-temperature events, unbleaching corals may maintain stable symbiotic relationships by increasing the diversity of symbiotic bacteria, regulating the structure of the symbiotic bacteria community, improving the interaction between coral host and symbiont and enhancing host immunity, thus avoiding coral bleaching. This study illuminates the relationship between the coral symbiont and tolerance differences of coral holobionts, providing new insights for further exploration into the adaptability of scleractinian corals in the context of global warming.