Integrated Metabolome and Transcriptome Analyses Reveal the Efficacy of Steroidal Saponins for Glucose and Lipid Metabolism in Hybrid Grouper (♀Epinephelus fuscoguttatus × ♂Epinephelus lanceolatu) Fed Higher-Lipid Diets

Abstract

An analysis of the extent of the effect of steroidal saponin addition on glucose and lipid metabolism in hybrid grouper liver was performed at the transcriptomic and metabolomic levels. Feeds (52% crude protein, 14% crude lipid) were prepared containing 0% (S0), 0.1% (S0.1), and 0.2% (S0.2) steroidal saponins. After eight weeks of feeding trial, compared to the S0 group, the activities of serum albumin, alanine aminotransferase, and aspartate transaminase were significantly lower and the activities of lysozyme, acid phosphatase, and alkaline phosphatase were significantly higher in the S0.1 group (p < 0.05). The superoxide dismutase, catalase, and glutathione peroxidase activities in the livers of the S0.1 group were significantly higher than those of the S0 group, while the malondialdehyde content was significantly lower than that of the S0 group (p < 0.05). There were forty-two differentially expressed genes and thirty-two differential metabolites associated with glucose and lipid metabolism enriched using KEGG and GO. In the S0 group, the expression of prostaglandin-endoperoxide synthase 1, prostaglandin E synthase 1, and thromboxane-2 synthase mRNA was significantly higher than in the S0.1 group (p < 0.05). The expression levels of genes in the S0 group were significantly higher than those in the S0.1 group (p < 0.05), including for glycogen synthase kinase, glucose-6-phosphatase catalytic subunit 2, fructose-1,6-bisphosphatase, phosphoenolpyruvate carboxykinase, glucose transporter 4, and malate dehydrogenase. The expression of mRNA such as fatty acid synthase, acetyl-CoA carboxylase, and sterol regulatory element-binding protein 1 was significantly lower in the S0.1 group than in the S0 group, while the expression of carnitine acyltransferase 1, acyl-CoA synthetase, and acyl-CoA dehydrogenase genes was significantly higher in the S0 group (p < 0.05). In summary, glycogen synthesis, gluconeogenesis, and the arachidonic acid metabolism pathway were inhibited by 0.1% steroidal saponins, and glycogenolysis, glycolysis, the tricarboxylic acid cycle, and the fatty acid β-oxidation pathway were activated. This study aims to provide a reference for the formulation of grouper feeds with a higher crude-lipid level.