Trace mineral sources affect oxidized oil induced intestinal damage in chickens by modulation of gut microbiota and short-chain fatty acid metabolism

This study investigated in vivo interactions between oil quality and trace mineral sources (organic vs. inorganic) on oxidative stress and intestinal damage in chickens. A total of 360 one-day-old male Lingnan yellow-feathered chickens with similar initial body weight (40 ± 2 g) were randomly assigned to four treatments in a 2 × 2 factorial design, with two oil qualities (fresh or oxidized) and two trace mineral sources (inorganic or organic). The experiment lasted for 21 days, with 6 replicates per treatment and 15 birds per replicate. Results showed that oxidized soybean oil (OSO) impaired jejunal barrier function (damaged morphology, downregulated tight junction genes), associated with reduced antioxidant capacity, elevated proinflammatory cytokines, and altered gut microbiota/short-chain fatty acid (SCFA) metabolism. Significant interactions were observed between oil quality and trace mineral sources (<i>P</i> < 0.05): only in the OSO group, organic trace minerals (OTM) outperformed inorganic ones (ITM) in enhancing total antioxidant capacity (<i>P</i> = 0.005) and glutathione peroxidase activity (<i>P</i> = 0.001), suppressing proinflammatory cytokines (e.g., interleukin-1β, <i>P</i> = 0.019; interleukin-2, <i>P</i> = 0.019; interleukin-6, <i>P</i> = 0.014; tumor necrosis factor-α, <i>P</i> = 0.001), increasing SCFA-producing bacteria (e.g., <i>Lactobacillus</i> and <i>Butyricicoccus</i>) while reducing pathogens (e.g., <i>Helicobacter</i>), and elevating SCFAs (<i>P</i> = 0.030). Furthermore, targeted metabolomic analysis revealed that OTM significantly increased the production of SCFAs, especially butyric acid (<i>P</i> = 0.001), which were positively correlated with the OTM-enriched microbiota. Mantel-test analysis revealed that the altered microbiota and metabolites showed strong correlations with specific parameters of intestinal health. The fecal microbiota transplantation experiment further confirmed that the intestinal protective effect is likely mediated by OTM-altered gut microbiota and their metabolites. In summary, the replacement of ITM by OTM in chicken diets can minimize the negative impact on OSO induced intestinal damage by improving intestinal barrier function and alleviating inflammatory responses mediated by gut microbiota modulation and SCFA metabolism.