Integrated Physiological and Transcriptomic Analyses Suggest Key Adaptive Mechanisms of European Perch (Perca...

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.