Effects of Dietary Steroid Saponins on Growth Performance, Serum and Liver Glucose, Lipid Metabolism and Immune Molecules of Hybrid Groupers (♀Epinephelus fuscoguttatus × ♂Epinephelus lanceolatu) Fed High-Lipid Diets

Abstract

High-lipid diets are attributed to excessive lipid deposition and metabolic disturbances in fish. The aim of this experiment was to investigate the effects of steroidal saponins on growth performance, immune molecules and metabolism of glucose and lipids in hybrid groupers (initial weight 22.71 ± 0.12 g) fed high-lipid diets. steroidal saponins (0%, 0.1% and 0.2%) were added to the basal diet (crude lipid, 14%) to produce three experimental diets, designated S0, S0.1 and S0.2, respectively. After an 8-week feeding trial, no significant differences were found between the S0 and S0.1 groups in percent weight gain, specific growth rate, feed conversion ratio, protein efficiency ratio and protein deposition rate (p > 0.05). All those in the S0.2 group were significantly decreased (p < 0.05). Compared to the S0 group, fish in the S0.1 group had lower contents of serum triglyceride and low-density lipoprotein cholesterol and higher high-density lipoprotein cholesterol and glucose (p < 0.05). The activities of superoxide dismutase, catalase and glutathione peroxidase were significantly higher, and malondialdehyde contents were significantly lower in the S0.1 group than in the S0 group (p < 0.05). Hepatic triglyceride, total cholesterol and glycogen were significantly lower in the S0.1 group than in the S0 group (p < 0.05). Activities of lipoprotein lipase, total lipase, glucokinase and pyruvate kinase, and gene expression of lipoprotein lipase, triglyceride lipase and glucokinase, were significantly higher in the S0.1 group than in the S0 group. Interleukin-10 mRNA expression in the S0.1 group was significantly higher than that in the S0 group, while the expression of interleukin-6 and tumor necrosis factor-α genes were significantly lower than those in the S0 group. In summary, adding 0.1% steroidal saponins to a high-lipid diet not only promoted lipolysis in fish livers, but also activated glycolysis pathways, thus enhancing the utilization of the dietary energy of the groupers, as well as supporting the fish’s nonspecial immune-defense mechanism.

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

“…In carp [ 17 ], white shrimp [ 28 ], and swimming crab ( Portunus trituberculatus ) [ 29 ], studies have demonstrated that saponins can decrease serum ALB, AST, and ALT enzyme activities and increase antioxidant and nonspecific immune enzyme activities in the liver to enhance the immune capacity of the body. A previous study demonstrated that 0.1% steroidal saponin significantly increased the activities and gene expression of SOD, CAT, GSH-PX, and GR in hybrid grouper liver and serum and decreased the MDA content [ 21 ]. In the present experiment, compared to the control group, supplementation of 0.1% steroidal saponins to a 14% crude lipid diet significantly increased LZM, ACP, and AKP enzyme activities and decreased ALB, ALT, and AST enzyme activities in the serum of hybrid grouper.…”

“…A previous study showed that supplementation of 0.1% steroidal saponins to high-lipid diets significantly increased the activity and gene expression of hexokinase, pyruvate kinase, and phosphofructokinase in the liver and significantly decreased glucose and glycogen content in the liver and serum of grouper [ 21 ]. Those phenomena indicated that steroid saponins had a potential role in stimulating carbohydrate utilization by the organism by elevating the activity and gene expression of the enzymes mentioned above.…”

“…During the experiment, the fish were continuously oxygenated every day, dissolved oxygen 5–6 mg/L, ammonia nitrogen <0.2 mg/L, temperature 30.5 ± 0.8 °C, salinity 28–32. Please refer to our previous study for the detailed feeding process [ 21 ].…”

“…The grouper were anesthetized with MS-222 (1:10,000), and then the fresh soybean-sized liver was cut from living fish fed diets S 0 and S 0.1 and immediately washed with saline to clean the surface of blood remaining on the tissue [ 21 ]. The liver samples were numbered, stored in 2 mL freeze tubes, quickly put in liquid nitrogen, and subsequently transferred to −80 °C for metabolome and transcriptome analyses.…”

“…Saikosaponin d has been confirmed to alleviate high-fat-diet-induced hepatic steatosis in hybrid grouper by targeting the AMPK/PPARα pathway [ 20 ]. Our previous study found that steroidal saponins improve the utilization of lipids and glucose in grouper liver when the fish ingested a high-lipid diet [ 21 ]. What is the exact mechanism?…”