Effects of Diets with Different Energy Levels at Cold Temperatures on Gut Microbiota and Metabolic State in Growing–Finishing Pigs

In cold-temperature regions, particularly on family farms, threats to livestock health constrain the potential of livestock husbandry. This study aimed to explore the effects of different dietary energy levels, adjusted by oil addition, on gut microbiota and metabolic homeostasis at cold temperatures. Twenty-four healthy pigs were randomly divided into two groups and fed a basal diet (BD) or a basal diet supplemented with oil (OD, with net energy increased by 100 kcal/kg) for 103 days. The cold temperature and humidity were maintained at 14 ± 2 °C and 65 ± 10%, respectively. On day 103 of the experiment, six pigs per group (three barrows and three females) were slaughtered after an overnight fast for sample collection: colon, colonic contents, plasma, and liver. The results showed that dietary oil addition remodeled the gut microbiota, forming a healthier microbial community characterized by a higher abundance of <i>Paludibacter</i>, <i>Parabacteroides</i>, <i>Peptococcaceae</i>, and <i>UCG-008</i> and a lower abundance of <i>Actinomyces</i>, <i>Turicibacter</i>, <i>Staphylococcus</i>, <i>Megamonas</i>, <i>Fusobacterium</i>, and <i>Achromobacter</i> (<i>p</i> < 0.05). Consistently, dietary oil addition resulted in higher levels of short-chain fatty acids (isobutyrate and isovalerate) and the Claudin-1 protein in the colon (<i>p</i> < 0.05). Plasma analysis showed that dietary oil addition increased energy metabolism and decreased inflammation. This change was characterized by higher levels of glucocorticoid, citrate, corticosterone, taurodeoxycholic acid, and ascorbic acid and lower levels of <i>IL-6</i> and hypoxanthine (<i>p</i> < 0.05). Transcriptomic and protein expression results in the liver further indicated that dietary oil addition alleviated energy stress and apoptosis by modulating metabolic states at cold temperatures. In conclusion, dietary oil addition improved gut health at cold temperatures in growing-finishing pigs, which was inextricably linked to the remodeling of the gut microbiota and metabolic states.