Comprehensive multi-omics and biochemical analysis to elucidate the molecular response mechanisms of gill and kidney tissues under acute salinity stress in Pseudobagras ussuriensis.

Acute salinity stress critically impacts aquaculture efficiency by inducing physiological disruptions in fish. This study investigated the molecular adaptation mechanisms of Pseudobagrus ussuriensis exposed to 10 ppt NaCl for 96 h, integrating transcriptomic and metabolomic analyses of gill and kidney tissues. In transcriptomics, 2,554 and 1,066 differentially expressed genes (DEGs) were identified in gills and kidneys, respectively, with significant enrichment in pathways related to energy metabolism (glycolysis, oxidative phosphorylation), membrane dynamics (glycerophospholipid metabolism), and immune-osmoregulatory crosstalk (HIF-1, TNF, and Jak-STAT signaling). Metabolomics revealed 85 and 433 differential metabolites (DMs) in gills and kidneys, highlighting tyrosine metabolism, amino acid biosynthesis/degradation, and lipid remodeling (e.g., glycerophospholipids, sphingolipids). Multi-organ coordination was observed: gills prioritized short-term osmotic adaptation via membrane lipid reorganization but suffered oxidative damage due to sustained downregulation of ALDH7 A1 and AOX/HADHA, triggering a “membrane injury–oxidative stress-ATP depletion” cycle. Conversely, kidneys-maintained energy homeostasis through purine/pyrimidine-TCA cycle reprogramming and autophagy-apoptosis balance. Critically, interorgan metabolic crosstalk-mediated by lipid mediators (prostaglandins, sphingolipids) and amino acid derivatives (branched-chain keto acids, glutamine)—orchestrated substrate shuttling (e.g., lactate for energy exchange) and systemic signaling, bridging local stress responses (gill ion regulation) with global metabolic adjustments (renal energy buffering). Notably, the levels of phosphatidylcholine (PC) and phosphatidylethanolamine (PE) in the kidney and phosphatidic acid (PA) and PC in the gills were significantly increased, while sphingomyelin (SM) decreased. Our findings demonstrate that acute salinity stress induces organ-specific metabolic reprogramming and interorgan crosstalk in P. ussuriensis, revealing a trade-off between osmotic adaptation and oxidative stress resilience mediated by lipid remodeling and energy metabolism dysregulation. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-025-11773-w.