Multi-omics-based study on metabolic-physiological response to heat stress in rainbow trout (Oncorhynchus mykiss)

Abstract

Global warming poses a critical survival challenge for cold-water economic fish, necessitating elucidation of their physiological and metabolic responses to heat stress. This study established a rainbow trout heat stress model using a gradual temperature increase protocol (from 16 °C to 20 °C over 8 days, followed by maintenance at 20 °C for 22 days) and investigated the adverse effects and adaptive strategies of rainbow trout under heat stress. Extensive congestion and steatosis observed in liver tissues suggested that heat stress induced inflammatory responses and dysregulation of lipid metabolism. Significant increases in antioxidant enzyme activities and reactive oxygen species levels (1.29-fold) indicated activation of the antioxidant defense system, and this response was insufficient to alleviate oxidative damage. Integrative transcriptomic and metabolomic analyses revealed that lipid metabolism was the most significantly altered biological process. Elevated prostaglandin D2 (1.64-fold change), driven by disruption of arachidonic acid metabolism, triggered inflammatory responses. Adaptive upregulation of linoleic acid and α-linolenic acid metabolism likely maintained membrane fluidity, enhancing the capacity for heat stress adaptation. Concurrently, adaptive activation of both GPX4A (6.73-fold change) and the heat shock proteins (LOC118938277 and hsp47) likely mitigated oxidative damage associated with heat stress in the liver. Overall, this study advances the understanding of pathological injuries and adaptive strategies in rainbow trout under heat stress and identifies candidate genes for breeding heat-tolerant strains.