Effects of parental nutritional programming on the hatching parameters, metabolome, glucose metabolism-related gene expressions, and global DNA methylation in larvae of yellow catfish Tachysurus fulvidraco

Nutritional programming has the potential to enhance digestible carbohydrate utilization in fish; however, the underlying mechanisms remain unclear. The present study compared the metabolome, glucose metabolism-related gene expressions, and global DNA methylation between yellow catfish larvae, which were parental programmed by a high carbohydrate diet (HC) or not (CON). In total, 1509 differentially altered metabolites (DAMs) were identified. Among them, the contents of key intermediates of TCA cycle and pentose phosphate pathway, citrate, and D-glycero-L-galacto-octulose were higher in HC than in CON. Meanwhile, the contents of two epigenetic modification-related metabolites, 2-hydroxyglutaric acid and N1-acetylspermidine, differed significantly between HC and CON. Thirteen KEGG pathways were significantly enriched and were mainly linked to amino acid and lipid metabolism. Additionally, the pentose phosphate pathway was enriched. The mRNA expressions of glycolytic genes gk, pk, and pfk, as well as the glucose transport gene sglt1, were significantly higher in HC than in CON. Global DNA methylation was significantly higher in HC than in CON. These results suggested that high carbohydrate programming could improve glucose utilization in yellow catfish larvae by modulating the TCA cycle and pentose phosphate pathway, and enhancing the conversion of glucose to amino acids. Epigenetic modifications might be the underlying mechanisms by which nutritional programming affects glucose metabolism in fish, while 2-hydroxyglutaric acid and N1-acetylspermidine are two critical metabolites that mediate epigenetic modifications.