Cold stress disrupts gill homeostasis in juvenile yellowfin tuna (Thunnus albacares) by altering oxidative, metabolic, and immune responses

Abstract

Acute cold stress can disrupt physiological homeostasis in marine fish and may induce pronounced metabolic and immune responses in pelagic species such as yellowfin tuna (Thunnus albacares), which possess regional endothermic capabilities. As a key tissue interfacing with the environment, the gill plays essential roles in gas exchange, ion regulation, immune defense, and energy metabolism, making it highly susceptible to thermal fluctuations. This study investigated the physiological responses of gill tissue in juvenile yellowfin tuna under acute cold stress, using two treatment groups—LT (24 °C) and ULT (18 °C)—with a control group (CG, 30 °C). Sampling was conducted at 0, 12, 24, and 36 h to assess antioxidant and metabolic enzyme activities, histopathological alterations, and the expression of immune- and metabolism-related genes. Results showed time-dependent changes in antioxidant enzymes (SOD, CAT, POD, GSH-Px), with significantly elevated MDA and LPO levels at 12 h and 24 h (p < 0.05), especially under 18 °C, indicating intensified oxidative stress. Significant alterations in AST, LDH, ACP, and AKP suggested metabolic reprogramming and membrane function changes. Variations in Na⁺/K⁺-ATPase and Ca²⁺/Mg²⁺-ATPase activity reflected ion regulation under thermal stress. Gene expression of hspa8b, heat shock cognate 71 kDa protein, irf3, lpl, and pck2 demonstrated temperature- and time-dependent adaptive responses. Histological analysis revealed progressive edema, necrosis, and lamellar disruption with decreasing temperature. Collectively, these findings highlight a multilayered stress response in yellowfin tuna gill tissue under cold exposure and provide new insights into thermal adaptation and cold-tolerant aquaculture strategies for pelagic species.