Integrated Physiological and Transcriptomic Analyses Suggest Key Adaptive Mechanisms of European Perch (Perca fluviatilis) to Acute Heat Stress

The European perch (Perca fluviatilis) is highly susceptible to heat stress, limiting its sustainable aquaculture. While single-organ thermal responses are partially understood, the systemic, multi-organ cooperative survival mechanisms under acute heat stress remain poorly characterized. To elucidate the underlying tolerance mechanisms and provide genetic markers for breeding, this study investigated the multi-organ responses of European perch (n = 90; body length: 13.15 ± 1.75 cm; body weight: 30.54 ± 7.17 g) transferred from 24 °C to an acute heat stress challenge (31 °C) at an increasing rate of 2 °C/h, and the histopathological changes (liver and gill), hepatic biochemical biomarkers (CAT, SOD, GSH-Px, GST, LDH, and MDA), and transcriptomic changes (liver and kidney) were evaluated over a 24 h period. Heat stress induced progressive structural damage, including gill lamellar edema and hepatocyte necrosis, accompanied by significant hepatic oxidative stress and lipid peroxidation. RNA-seq transcriptome profiling uncovered distinct sets of genes with significant expression changes, comprising 1343 DEGs in liver tissue and 722 DEGs in kidney samples. Both organs shared a systemic endoplasmic reticulum stress response but exhibited highly divergent survival strategies. The liver underwent severe metabolic reprogramming towards anaerobic glycolysis and gluconeogenesis, coupled with vesicle-mediated membrane repair attempts and apoptosis. Conversely, the kidney adopted a strict “energy triage” strategy, suppressing highly energy-consuming immune and osmoregulatory functions while actively silencing pro-apoptotic signals. These findings highlight organ-specific adaptations and identify potential metabolic markers for the future breeding of new heat-tolerant varieties.