Dietary protein/carbohydrate ratio and swimming activity modulate mitochondrial performance and oxidative metabolism in gilthead sea bream (Sparus aurata) juveniles

Abstract

This study compares the effects of a high-protein diet (HP) and a high-carbohydrate diet (HC) on energy metabolism, mitochondrial homeostasis, and oxidative stress in gilthead sea bream juveniles, and examines how swimming activity modulates these effects in a 6-week trial. Both diet and exercise induced tissue-specific metabolic responses, adjusting enzyme activity and gene expression based on substrate availability and energy demands. HP-fed fish exhibited higher hepatic protein content and increased activity of enzymes involved in aerobic metabolism (Cs) and protein catabolism (Alat) compared to HC-fed fish. Hepatic expression of genes related to mitochondrial biogenesis (sirt1, tfam, pgc1a), dynamics (mfn1, mfn2, miffb, fis1), energy metabolism (cox4a, cs, ucp1, hadh), and oxidative stress (sod1, sod2, cat, gpx1, gpx4, gst3, prdx5) was also higher in the HP-fed group. In red muscle, mitochondrial activity was more pronounced in HC-fed fish, as evidenced by increased expression of sirt1, pgc1a, ucp2, and antioxidant-related genes. White muscle exhibited minimal changes in response to diet composition, with HP-fed fish displaying slightly higher oxidative capacity, and HC-fed fish showing stronger activation of glycolytic pathways. Exercise reduced plasma triglyceride levels and upregulated mfn1, glut4, and ucp2 expression in red muscle, while liver and white muscle function remained mostly unaffected by swimming activity. Gilthead sea bream juveniles demonstrated notable metabolic adaptation to a carbohydrate-rich diet, presenting minor diet-induced changes at the molecular level, with skeletal muscles showing high metabolic plasticity. Furthermore, exercise enhanced nutrient utilization, especially under high carbohydrate intake, providing a suitable strategy for using protein-adjusted diets to promote more sustainable farming of this species.