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

SIMPLE SUMMARY: The ingestion of higher-lipid diets by fish could lead to excessive lipid deposition and metabolic disorders in vivo. This experiment analyzed the effects of steroidal saponins on hepatic glucose and lipid metabolism in hybrid grouper fed higher-lipid diets using a multi-omics approach. Data from grouper fed diets with 0% and 0.1% steroidal saponins show that 0.1% steroidal saponins inhibited glycogen synthesis, gluconeogenesis, and the arachidonic acid metabolism pathway and activated glycogenolysis, glycolysis, and the fatty acid β-oxidation pathway. This study provides a deeper insight into the glycolipid metabolic processes in the liver of grouper fed higher crude-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% (S(0)), 0.1% (S(0.1)), and 0.2% (S(0.2)) steroidal saponins. After eight weeks of feeding trial, compared to the S(0) 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 S(0.1) group (p < 0.05). The superoxide dismutase, catalase, and glutathione peroxidase activities in the livers of the S(0.1) group were significantly higher than those of the S(0) group, while the malondialdehyde content was significantly lower than that of the S(0) 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 S(0) group, the expression of prostaglandin-endoperoxide synthase 1, prostaglandin E synthase 1, and thromboxane-2 synthase mRNA was significantly higher than in the S(0.1) group (p < 0.05). The expression levels of genes in the S(0) group were significantly higher than those in the S(0.1) 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 S(0.1) group than in the S(0) group, while the expression of carnitine acyltransferase 1, acyl-CoA synthetase, and acyl-CoA dehydrogenase genes was significantly higher in the S(0) 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.