Diel transcriptional responses of coral-Symbiodiniaceae holobiont to elevated temperature.

Coral exhibits diel rhythms in behavior and gene transcription. However, the influence of elevated temperature, a key factor causing coral bleaching, on these rhythms remains poorly understood. To address this, we examined physiological, metabolic, and gene transcription oscillations in the Acropora tenuis-Cladocopium sp. holobiont under constant darkness (DD), light-dark cycle (LD), and LD with elevated temperature (HLD). Under LD, the values of photosystem II efficiency, reactive oxygen species leakage, and lipid peroxidation exhibited significant diel oscillations. These oscillations were further amplified during coral bleaching under HLD. Gene transcription analysis identified 24-hour rhythms for specific genes in both coral and Symbiodiniaceae under LD. Notably, these rhythms were disrupted in coral and shifted in Symbiodiniaceae under HLD. Importantly, we identified over 20 clock or clock-controlled genes in this holobiont. Specifically, we suggested CIPC (CLOCK-interacting pacemaker-like) gene as a core clock gene in coral. We observed that the transcription of two abundant rhythmic genes encoding glycoside hydrolases (CBM21) and heme-binding protein (SOUL) were dysregulated by elevated temperature. These findings indicate that elevated temperatures disrupt diel gene transcription rhythms in the coral-Symbiodiniaceae holobiont, affecting essential symbiosis processes, such as carbohydrate utilization and redox homeostasis. These disruptions may contribute to the thermal bleaching of coral.