Temporal transcriptional rhythms govern coral-symbiont function and microbiome dynamics

Diel rhythms align physiological processes with light/dark cycles, driving predictable oscillations in gene expression and protein activity through tightly controlled transcriptional-translational feedback loops. Transcriptomic analyses in the stony coral Pseudodiploria strigosa revealed tightly regulated transcriptional control: dawn triggers a molecular reset marked by RNA metabolism and protein turnover; midday emphasizes anabolic and phosphate-regulated pathways; dusk reflects transitional lipid and amino acid metabolism; and midnight reveals stress-responses, mRNA catabolism, and mitochondrial organization. The photosymbiont Breviolum sp. exhibits subtler but distinct diel regulation, with photoprotective activation at dawn, metabolite transport and nitrogen cycling through midday and dusk, and cell cycle and ion homeostasis at night. Microbial communities show time-dependent restructuring of co-occurrence networks. Carbohydrate-catabolizing taxa associated with Symbiodiniaceae during daylight, while nighttime assemblages feature methylotrophs likely facilitating dimethylsulfoniopropionate (DMSP) metabolism. Together, these findings present the first system-level molecular framework of diel regulation across the coral-photosymbiont-microbe holobiont, revealing strong time-specific transcriptional control as a key driver of coordinated function and homeostasis.