Excessive Effects of Extreme Energy Levels on Lipid Metabolism in Ningxiang Pigs: Insights from Gut Microbiota and Glycerophospholipid Metabolism

Objectives: This experiment investigated the response of carcass composition, digestive function, hepatic lipid metabolism, intestinal microbiota, and serum metabolomics to excessive or restrictive dietary energy in Ningxiang pigs. Methods: A total of 36 Ningxiang pigs (210 ± 2d, 43.26 ± 3.21 kg) were randomly assigned to three treatments (6 pens of 2 piglets each) and fed a control diet (CON, digestive energy (DE) 13.02 MJ/kg,), excessive energy diet (EE, 15.22 MJ/kg,), and restrictive energy diet (RE, DE 10.84 MJ/kg), respectively. Results: Results showed that EE significantly increased the apparent digestibility of crude protein and total energy (p < 0.01), as well as the activities of jejunum neutral protease and ileal lipase (p < 0.05). With the increase in energy level, the apparent digestibility of ash, dry matter, and ether extract significantly increased (p < 0.01). RE significantly increased high-density lipoprotein cholesterol (HDL-C) content, significantly decreased triglycerides (TG), free fatty acid (NEFA), and total cholesterol (TC) contents, and up-regulated lipoprotein lipase (LPL) mRNA expression in the liver (p < 0.05). EE significantly increased the hepatosomatic index, the contents of low-density lipoprotein cholesterol (LDL-C) and total bile acids (TBA), and significantly up-regulated the mRNA expression of lipogenic genes acetyl-CoA carboxylase (ACC), fatty acid synthase (FAS), and sterol regulatory element-binding protein-1C (SREBP-1C) in the liver (p < 0.05). The abundance of p_Firmicutes was significantly increased and the abundance of p_Bacteroidetes was significantly decreased in test groups, while the ratio of the two was significantly increased in the RE group (p < 0.05). EE also significantly increased the abundance of g_Clostridium_sensu_stricto_1 (p < 0.05). The identical serum differential metabolites between the EE and RE group belong to phosphatidylcholine (PC), mostly being up-regulated in the EE group and down-regulated in the RE group (p < 0.05), one of which was mapped to the pathway of glycerophospholipid metabolism (KEGG ID: C00157). The relative content of serum trimethylamine N-oxide (TMAO, a microbial metabolite) was significantly decreased in the EE group (p < 0.05). Conclusions: The findings suggest RE had no obvious negative effect on carcass traits of Ningxiang pigs. Apart from exacerbated body fat deposition, EE promoted fat accumulation in the liver by up-regulating the expression of lipogenic genes. Dietary energy changes affect hepatic bile acid metabolism, which may be mediated through the glycerophospholipid metabolism pathway, as well as disturbances in the gut microbiota.