Dietary fatty acid composition modulates growth in the marine teleost Trachinotus ovatus by regulating the hepatic triglyceride to (phosphatidylcholine + phosphatidylethanolamine) ratio via the Ampk/Srebp signaling pathway

Abstract

Previous studies have demonstrated superior growth performance in Trachinotus ovatus fed a blended oil 1 (BO1, optimized for essential fatty acid requirements) compared to those receiving blended oil 2 (BO2, fish oil:soybean oil, 2:3). To elucidate the mechanistic basis of dietary fatty acid effects on growth, we conducted lipidomic, biochemical, and transcriptomic analyses using tissue samples from T. ovatus (initial weight: 7.63 ± 0.03 g) fed the BO1 or BO2 diets for 9 weeks. Fish fed BO1 exhibited elevated hepatic phosphatidylcholine (PC) and phosphatidylethanolamine (PE) levels, reduced lipid and triglyceride (TG) content, and lower TG/(PC + PE) ratio (P < 0.05). Serum analyses revealed significantly decreased TG, total cholesterol, and free fatty acid levels in BO1-fed fish (P < 0.05). Transcriptomic profiling demonstrated upregulation of fatty acid synthesis genes (srebp1c, fas, acc1, scd1), PC/PE synthesis genes (pcyt1, pcyt2), and TG catabolism gene (atgl) in the BO1 group, while TG synthesis (dgat) and energy metabolism (ampk) genes were downregulated (P < 0.05). In vitro experiments with T. ovatus hepatocytes showed that Ampk inhibition increased Pcyt1 and Atgl activities, elevated PC levels, and reduced TG/(PC + PE) ratios (P < 0.05). Srebp1c overexpression upregulated PC synthesis genes, increased PC content, and decreased TG/(PC + PE) ratios (P < 0.05). Treatment with BO1- or BO2-mimetic fatty acid blends recapitulated in vivo observations. These findings suggest that BO1's optimized fatty acid composition enhances PC and PE biosynthesis and TG catabolism via the Ampk/Srebp pathway, ultimately resulting in a reduced hepatic TG/(PC + PE) ratio, optimized lipid homeostasis, and enhanced T. ovatus growth.