Metatranscriptomic and metagenomic analyses reveal the roles of coral holobionts in recovery phase during natural bleaching event: A case study of subtropical Acropora solitaryensis

Ocean warming has led to widespread coral bleaching over the past half-century. While many studies have explored potential bleaching mechanisms under controlled experiments, little is known about the responses and dynamics of coral holobionts that contribute to recovery during natural bleaching events. This study investigates the recovery process by analyzing physiological parameters, microbiome structures, metatranscriptomic, and metagenomic data in subtropical Acropora solitaryensis during the 2022 natural bleaching event. Bleached and non-bleached Acropora colonies were tagged and sampled across four recovery phases: 0, 1, 4, and 11 weeks, in Hong Kong waters. Our results showed that coral pigmentation and Fv/Fm increased after one month, returning to non-bleached levels by week 11. This recovery trajectory was reflected in the diversity and compositional patterns of both symbiotic zooxanthellae and bacterial communities. Specifically, zooxanthellae diversity increased, while bacterial diversity declined after four weeks. Metagenomic analysis revealed persistent differences in bacterial metabolic processes, including carbohydrate, amino acid, cofactor, vitamin, and energy metabolism, which contribute to nutrient cycling within the holobiont. Furthermore, metatranscriptomic analysis indicated significant transcriptional changes in the coral host, but not in the symbiotic zooxanthellae, with Acropora genes associated with stress response, immunity, embryonic and system development, and morphogenesis and tissue formation potentially facilitating cellular and physiological recovery of the coral host. Overall, this study enhances our understanding of coral recovery from natural bleaching, highlighting that visibly recovered corals still exhibit impairments in cellular metabolic and immune responses. This insight contributes to improved predictions of coral survival and resilience under climate change.