Low-temperature stress poses a critical challenge to the overwintering survival of black porgy (Acanthopagrus schlegelii), a commercially important marine fish distributed across the coastal waters of West Pacific region, including the continental shelves of China, Japan, and the Korean Peninsula. To unravel the molecular mechanisms underlying cold adaptation, this study employed quantitative proteomics was employed to analyze hepatic protein profiles of black porgy between three groups: control group (CG, 15 °C), cold-sensitive group (CS, 3.8 °C), and cold-tolerant group (CT, 2.8 °C). A total of 4437 proteins were identified, with 1616 differentially expressed protein (DEPs) detected among the groups. Bioinformatics analyses, including Gene Ontology (GO), Kyoto Encyclopedia of Genes and Genomes (KEGG) enrichment, Gene Set Enrichment Analysis (GSEA), and trend analysis, revealed distinct adaptive strategies between CT and CS groups. The CT group exhibited a coordinated “energy conservation - metabolic remodeling - antioxidation” strategy: (1) significant downregulation of ribosomal subunits and protein export pathways to reduce Adenosine Triphosphate (ATP) consumption from protein synthesis (called “ribosomal hibernation”); (2) upregulation of Peroxisome Proliferator-Activated Receptor (PPAR) signaling pathway and peroxisomal functions to enhance fatty acid β-oxidation and ketone body production, facilitating efficient energy supply; (3) activation of antioxidant systems to mitigate damage induced by reactive oxygen species (ROS). In contrast, the CS group showed dysregulated energy metabolism, characterized by enhanced but inefficient glycolysis, impaired endoplasmic reticulum function, and excessive inflammatory responses, which may contribute to protential proteotoxic stress and metabolic dysfunction. Key DEPs and pathways, such as ribosomal proteins, PPAR family proteins, and peroxisomal enzymes, were identified as protential core regulators of cold tolerance in black porgy. This study provides the first comprehensive proteomic insights into the molecular mechanisms of cold tolerance in black porgy, highlighting the evolutionary significance of energy allocation and metabolic plasticity in teleosts. These findings offer potential molecular markers for breeding cold-tolerant strains, addressing critical challenges in aquaculture sustainability.
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