Multi-omics insights into energy metabolism changes in response to salinity adaptation in mud crab (Scylla...

Salinity is a major environmental factor influencing the energy metabolism of aquatic organisms. However, multi-omics evidence explaining how energy metabolism supports long-term salinity adaptation in euryhaline species remains limited. Here, we used the mud crab Scylla paramamosain as a model organism, exposing individuals to control (30 ppt), moderate (15 ppt), and low (5 ppt) salinity for 40 days, followed by integrated transcriptomic, metabolomic, lipidomic, and enzyme activity analyses of muscle tissue. The CS group exhibited the better growth performance, while reduced salinity adversely impacted body growth and carapace development. Key metabolic enzymes hexokinase (HK), pyruvate kinase (PK), and lactate dehydrogenase (LDH) were significantly suppressed under low salinity, indicating suppressed glycolysis. Transcriptomic data revealed downregulation of genes involved in the tricarboxylic acid (TCA) cycle, including citrate synthase (CS) and isocitrate dehydrogenase (IDH), as well as multiple subunits of NADH dehydrogenase and ATP synthase associated with oxidative phosphorylation (OXPHOS). Metabolites central to amino acid and energy metabolism, such as L-glutamic acid, L-glutamate, and citric acid, were markedly reduced, indicating suppression of glutamate-dependent pathways and TCA cycle activity. Lipidomic data revealed elevated levels of phosphatidylcholine (PC), phosphatidylethanolamine (PE), and sphingomyelins (SM), indicating membrane remodeling, while triglyceride depletion suggests energy mobilization. Pathway enrichment highlighted AMPK and FoxO signaling as central regulators of energy and metabolic homeostasis under salinity exposure. Integrated multi-omics analysis revealed coordinated downregulation of TCA cycle genes and depletion of citric acid, suggesting systemic attenuation of energy metabolism as an adaptive strategy. Overall, S. paramamosain adapts to prolonged low salinity through metabolic reprogramming toward energy conservation, with specific enzymes, metabolites, and lipids serving as potential biomarkers of salinity adaptation.