Comparative chromatin dynamics reveal differential thermal tolerance mechanisms between two congeneric oyster species

Oysters, being globally farmed bivalve of significant economic and ecological value, are increasingly confronted with heat stress induced by global warming, such as the frequent occurrence of mass summer mortality events worldwide. The role of epigenetics in adapting to high-temperature environments has garnered growing attention; however, its application in oysters remains poorly understood. In this study, we conducted a comparative analysis between two closely related oyster species (the relatively thermosensitive Crassostrea gigas and the relatively thermotolerant Crassostrea angulata) using ATAC-Seq and RNA-Seq to reveal the differential thermal tolerance mechanisms at the chromatin dynamics level in response to high-temperature stress. The comparative analysis showed that the inhibitor of apoptosis protein (IAP) family and its associated apoptosis pathways were the major divergent pathway between the two species. The promoter regions of differentially expressed genes in C. gigas under heat stress were found to be enriched with motifs such as Foxp1, Foxk2, Myc, Cebpd, Foxo3, and Hsf1 motifs and expressed genes related to molecular chaperones, including heat shock protein family. And C. angulata activated the genes related to anti-apoptosis, DNA damage repair, and fatty acid synthesis (decreasing fatty acid unsaturation of membrane to regulate membrane fluidity). These findings suggest that C. angulata may have evolved a more centralized and energy-efficient transcriptional regulatory network at the genomic level, thereby facilitating its long-term adaptation to relatively high temperature environments. Furthermore, the key transcription factor Hsf1, involved in heat shock responses, may contribute to the differential heat response patterns in C. gigas and C. angulata through divergent expression levels of its alternatively spliced isoforms (Hsf1a and Hsf1d). Our work will contribute to predicting the adaptive potential of oysters and other marine invertebrates in facing future global warming, and provide a theoretical foundation for genetic improvement of resistance traits and sustainable development of oyster industry.