A miRNA-mediated gene regulatory network supports seasonal plasticity in the temperate coral Astrangia poculata

Phenotypic plasticity is critical for sessile marine invertebrates facing intensifying climate change. MicroRNAs (miRNAs)-small non-coding RNAs that regulate gene expression-are compelling candidates for mediating such plasticity, but their role in coral biology remains poorly characterized. We used the temperate coral Astrangia poculata, which endures annual temperature ranges exceeding 25°C, to investigate miRNA-mediated plasticity across seasonal and thermal contexts. Adult aposymbiotic colonies were exposed to ambient seasonal temperatures (∼5-22°C) and a chronic +3°C warming treatment from February to August 2021. Monthly physiological sampling showed that seasonal temperature variation drove significant shifts in photosynthesis, respiration, and soluble protein, whereas the +3°C treatment had minimal physiological effect. RNA-seq across three time points (February, June, and August) revealed that seasonal temperature variation also drove the strongest molecular response. Transcriptional functional enrichment shifted from winter protein homeostasis and cellular integrity to summer immunity, metabolism, and reproduction. We also identified 51 A. poculata miRNAs (46 novel), providing the first characterization of the miRNA repertoire in this species. Target prediction and co-expression analyses revealed that while mRNA-miRNA networks appear to maintain a stable infrastructure across seasons and treatments, specific interactions may be rewired to drive seasonal biology. This dynamic regulation is associated with putative suppression of energy-intensive cell division and morphogenesis during winter quiescence, while shifting to regulate tissue remodeling and reproduction genes during the summer. These results establish miRNAs as seasonal gene regulators in a temperate coral and suggest that the molecular infrastructure underlying its plasticity may also confer resilience to moderate thermal stress.