Phenotypic plasticity in Mediterranean gorgonians Eunicella singularis and Paramuricea clavata at high temperature...

The Mediterranean gorgonian octocorals are threatened by acidification, warming and marine heat waves. Phenotypic plasticity is critical for slow-growing gorgonians, as adaptation through natural selection might not be fast enough to cope with rapid environmental changes. DNA methylation (DNAm) is a type of (trans)generational phenotypic plasticity mechanism that may help slow-growing corals better withstand the effects of environmental changes by adjusting gene expression. This study aimed to assess the physiological responses and epigenetic modifications associated with phenotypic plasticity in the Mediterranean gorgonians Eunicella singularis and Paramuricea clavata exposed to warming (+4 °C), acidification (-0.35 pH_T units) and their combination over two weeks. In addition, RNA-Seq-based differential gene expression analysis was performed for E. singularis. High temperature, low pH and their combination did not cause tissue death or necrosis in the corals. Polyp activity in E. singularis increased at high temperatures. Warming increased oxygen consumption in both species. Energy reserves (protein, lipid, carbohydrate contents) were not affected by temperature, pH or their interaction in either species. The global DNA methylation (gDNAm) rate was ten times higher in P. clavata than in E. singularis. There was no effect of temperature, pH or their interaction on gDNAm in E. singularis. gDNAm in P. clavata decreased at high temperatures and low pH. Differential gene expression analysis indicated that high temperature induced the most extensive transcriptional changes in E. singularis, while low pH alone had the least impact. The combined stress of high temperature and low pH also led to notable up- and downregulation of gene expression. Heat stress in E. singularis caused widespread downregulation of transcription factors (TFs), particularly those in the zf-C2H2, AP-2, and HMG families. Conversely, the IRF, RFX, P53, and NRF1 families were upregulated, highlighting the complex transcriptional response to thermal stress. Overall, these physiological, transcriptomic and epigenetic alterations have the potential to negatively impact the fitness of these emblematic species and their associated ecosystems.