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

Phenotypic plasticity is a critical strategy for sessile marine invertebrates that cannot escape changing environmental conditions. For corals facing intensifying climate change, the molecular mechanisms that generate and regulate acclimatory responses are central to understanding performance and persistence. MicroRNAs (miRNAs), small non-coding RNAs that regulate gene expression via translational repression and transcript degradation, are compelling candidates for mediating such plasticity, but their role in coral biology remains poorly characterized. Here, we use Astrangia poculata, a temperate coral that endures annual temperature ranges exceeding 25{degrees}C, to investigate the potential for miRNA-mediated plasticity across seasonal and thermal contexts. We exposed adult aposymbiotic colonies to ambient seasonal temperatures ([~]5-22{degrees}C) and a chronic +3{degrees}C warming treatment from February to August 2021, sampling monthly for physiological analyses and at three time points (February, June, August) for molecular analyses. Seasonal change drove significant shifts in photosynthesis, respiration, and soluble protein, whereas the +3{degrees}C treatment had minimal physiological effect. RNA-seq analysis identified the strongest response across seasons, with transcriptional functional enrichment shifting from protein homeostasis, and cellular integrity in the winter, to immunity, metabolism, and reproduction in the summer. We identified 51 miRNAs in A. poculata, 46 of which are novel to this species, providing the first characterization of the miRNA repertoire in this species. Target prediction and co-expression analyses revealed that while mRNA-miRNA networks maintain a stable infrastructure across seasons and treatments, specific interactions are rewired to drive seasonal biology. This dynamic regulation suppresses 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.