Acclimation mechanisms of reef-building coral Acropora gemmifera juveniles to long-term CO2-driven ocean acidification

Ocean acidification (OA) is a major threat to the sexual recruitment of reef-building corals. Acclimation mechanisms are critical but poorly understood in reef-building corals to OA during early life stages. Here, Acropora gemmifera, a common Indo-Pacific coral cultured in in situ seawater from Luhuitou reef at three levels of pCO₂ (pH 8.14, 7.83, 7.54), showed significantly delayed larval metamorphosis and juvenile growth, but adapted to long-term high pCO₂. Differentially expressed genes (DEGs) emerged as a time- and dose-dependent mode of short-term response (3 days post settlement, d p.s.) and long-term acclimation (40 d p.s.), with more DEGs responding to high pCO₂ (pH 7.54) than to medium pCO₂ (pH 7.83). High pCO₂, a presumed threatening seawater baseline for A. gemmifera juveniles, activated DNA repair, macroautophagy, microautophagy and mitophagy mechanisms to maintain cellular homeostasis, recycle cytosolic proteins and damaged organelles, and scavenge reactive oxygen species (ROS) and H⁺, but at the cost of delayed development through cell cycle arrest associated with epigenetic and genetic regulation at 3 d p.s.. However, A.gemmifera juveniles acclimated to high pCO₂ by up-regulating cell cycle, transcription, translation, cell proliferation, cell-extracellular matrix, cell adhesion, cell communication, signal transduction, transport, binding, Symbiodiniaceae symbiosis, development and calcification from 3 d p.s. to 40 d p.s., when energy reallocation and metabolic suppression occurred for high demand but short-term energy limitation in coral cells undergoing flexible symbiosis. All results indicate that acclimation mechanisms of complicated gene expression improve larval and juvenile resilience to OA for coral population recovery and reef restoration.