Short-term plasticity and long-term transcriptomic rewiring under natural ocean acidification in an...

Ocean acidification is reshaping coastal ecosystems as a consequence of anthropogenic CO₂ emissions. Natural CO₂ vent systems provide valuable analogues for investigating organismal responses to long-term acidified conditions under ecologically realistic scenarios. Here, we examined genome-wide transcriptomic responses of the sea urchin Arbacia lixula, an ecosystem-relevant grazer inhabiting a natural CO₂ vent system in La Palma (Canary Islands, Spain). Using RNA sequencing of 24 adults (n = 8 per treatment), we compared: (i) acute experimental exposure of ambient-origin individuals to low pH, (ii) chronic exposure by comparing ambient and vent-origin populations in their native pH conditions, and (iii) a genotype-of-origin comparison under shared low pH. Acute exposure triggered a limited transcriptional response (116 differentially expressed genes, DEG), characterized by activation of ion transport, redox regulation, and NAD-associated metabolism. In contrast, chronically exposed vent-origin urchins showed a tenfold increase in transcriptional changes (1053 DEG), reflecting metabolic reprogramming involving lipid, carbohydrate and amino acid pathways, and strengthened antioxidant capacity. Chronic low-pH exposure was also associated with suppression of biomineralization and developmental genes, alongside strong upregulation of collagen and extracellular matrix-associated genes that may help maintain skeletal performance under reduced carbonate availability. Genotype-of-origin effects (131 DEGs) revealed constitutive differences in metabolic, redox, extracellular matrix, and biomineralization pathways in vent populations. Together, these findings indicate that persistence under natural acidification involves both rapid plastic responses and sustained physiological reorganization, providing mechanistic insight into how calcifying species maintain functional performance under ongoing ocean acidification.