Molecular mechanisms of Patinopecten yessoensis responding to extreme high temperature: insights into cytoskeletal dynamics and immune activation adaptation

Ocean warming critically threatens the survival and ecological stability of cold-water bivalves. Yet, the temporal dynamics of molecular damage and recovery following extreme high temperature stress remain poorly understood. In this study, we examined the transcriptomic and physiological responses of Patinopecten yessoensis in gills at 1 h after extreme high temperature treatment (30 °C, H1) and at 1, 3 and 24 h during the recovery period ( 25 °C, alternatives: R1, R3, R24). The results revealed that extreme high-temperature stress caused widespread, delayed transcriptional disruption in P. yessoensis , highlighting its molecular response and recovery dynamics. During the recovery stages, and the R3 stage emerged as a critical transition window during which cellular homeostasis began to be restored, and key repair pathways were reactivated. Furthermore, a sequential recovery trajectory revealed by WGCNA indicated that the recovery began with early cytoskeletal destabilization and calcium-dependent signaling (H1, Myellow module), progressed through protein quality control and endoplasmic reticulum homeostasis (R1, Mbrown module), and culminated in cell death regulation, immune signaling, and tissue remodeling (R3, Mblue module). The microtubule system was identified as a primary target of thermal disruption, showing downregulation and structural disassembly immediately after stress and recovering in R3 stage. These findings collectively suggested that P. yessoensis employs a multi-tiered adaptive strategy to withstand and recover from temperature-induced injury, with tightly regulated temporal coordination between cytoskeletal integrity, genomic maintenance, and programmed cell death. This study enhances our understanding in high temperature response mechanism of cold-water bivalves, and have significant implications for ecological risk assessment and selective breeding in cold-water shellfish aquaculture. • The R3 stage represents a key transition from damage sensing to repair mechanisms. • Microtubule-related pathways play a pivotal role in structural recovery during high temperature stress adaptation. • Stage-specific co-expression modules reveal a temporally orchestrated transcriptional response. • The recovery process follows a sequential pattern: cytoskeletal remodeling, ER proteostasis, and immune-apoptotic regulation.