Transcriptomic responses reveal impaired physiological performance of the pearl oyster following repeated exposure to marine heatwaves

Marine heatwaves are predicted to become more intense and frequent in the future, possibly threatening the survival of marine organisms and devastating their communities. While recent evidence reveals the adaptability of marine organisms to heatwaves, substantially overlooked is whether they can also adjust to repeated heatwave exposure, which can occur in nature. By analysing transcriptome, we examined the fitness and recoverability of the pearl oyster (Pinctada maxima) after two consecutive heatwaves (24 °C to 32 °C for 3 days; recovery at 24 °C for 4 days). In the first heatwave, 331 differentially expressed genes (DEGs) were found, such as AGE-RAGE, MAPK, JAK-STAT, FoxO and mTOR. Despite the recovery after the first heatwave, 2511 DEGs related to energy metabolism, body defence, cell proliferation and biomineralization were found, where 1655 of them were downregulated, suggesting a strong negative response to the second heatwave. Our findings imply that some marine organisms can indeed tolerate heatwaves by boosting energy metabolism to support molecular defence, cell proliferation and biomineralization, but this capacity can be overwhelmed by repeated exposure to heatwaves. Since recurrence of heatwaves within a short period of time is predicted to be more prevalent in the future, the functioning of marine ecosystems would be disrupted if marine organisms fail to accommodate repeated extreme thermal stress.