Ocean acidification elicits differential bleaching and gene expression patterns in larval reef coral Pocillopora damicornis under heat stress

The successful dispersal of coral larvae is vital to the population replenishment and reef recovery and resilience. Despite that this critical early stage is susceptible to ocean warming and acidification, little is known about the responses of coral larvae to warming and acidification across different biological scales. This study explored the influences of elevated temperature (29 °C versus 33 °C) and pCO2 (500 μatm versus 1000 μatm) on brooded larvae of Pocillopora damicornis at the organismal, cellular and gene expression levels. Heat stress caused bleaching, depressed light-enhanced dark respiration, photosynthesis and autotrophy, whereas high pCO2 stimulated photosynthesis. Although survival was unaffected, larvae at 33 °C were ten-times more likely to settle than those at 29 °C, suggesting reduced capacity to disperse and differentiate suitable substrate. Remarkably, heat stress induced greater symbiont loss at ambient pCO2 than at high pCO2, while cell-specific pigment concentrations of symbionts at 33 °C increased twofold under ambient pCO2 relative to high pCO2, suggesting pCO2-dependent bleaching patterns. Considerable increases in activities of host antioxidants superoxide dismutase (SOD) and catalase (CAT) at 33 °C indicated oxidative stress, whereas lipid peroxidation and caspase activities were contained, thereby restraining larval mortality at 33 °C. Furthermore, the coral host mounted stronger transcriptional responses than symbionts. High pCO2 stimulated host metabolic pathways, possibly because of the boosted algal productivity. In contrast, host metabolic processes and symbiont photosystem genes were downregulated at 33 °C. Interestingly, the upregulation of extracellular matrix genes and glycosaminoglycan degradation pathway at 33 °C was more evident under ambient pCO2 than high pCO2, suggesting compromised host tissue integrity that could have facilitated symbiont expulsion and bleaching. Our results provide insights into how coral larvae respond to warming and acidification at different levels of biological organization, and demonstrate that ocean acidification can mediate thermal bleaching and gene expression in coral larvae under heat stress.