Duodenal resident Limosilactobacillus improves feed efficiency through ornithine-mediated optimization of gut microbiota and nutrient absorption via the Nrf2 signaling.

BACKGROUND

The small intestinal microbiota directly influences host intestinal digestive and absorptive responses to dietary nutrients and plays a crucial role in optimizing feed efficiency in food-producing animals. However, the microbial functions of small intestine in regulating feed efficiency in broiler chickens remain to be elucidated.

METHODS

A total of 150 healthy broilers were individually housed under identical feeding conditions to accurately calculate their feed efficiency. The gut microbiota in different intestinal segments of high and low feed efficiency chickens were compared using 16S rRNA sequencing. Gut bacterial candidates associated with feed efficiency were identified through a two-part model, LEfSe, and the Wilcoxon rank-sum test. Another 1725 1-day-old male broiler chicks were fed either a basal diet (BD) or BD supplemented with four different bacterial candidates isolated from the chicken gut to investigate their roles in regulating gut microbiota and nutrient absorption. The underlying molecular mechanisms by which key Limosilactobacillus strains and their metabolite ornithine improve intestinal health were also examined using an intestinal epithelial cell line.

RESULTS

This study found that chickens with high feed efficiency exhibited greater microbial community stability and stronger cooperative interactions compared to low feed efficiency chickens, particularly within the duodenal microbiota. Meanwhile, duodenal resident Limosilactobacillus were significantly positively correlated with feed efficiency. Further validation trials revealed that specific Limosilactobacillus strains (L. vaginalis LD11 and L. ingluviei CC32) significantly improved feed efficiency, concurrently enhancing antioxidant capacity, barrier function, nutrient absorption, as well as increasing Limosilactobacillus abundance in the duodenum. These two bacterial strains could produce high concentrations of ornithine in the duodenum, which effectively alleviated LPS-induced intestinal cell damage by enhancing antioxidant capacity and upregulating the protein expression of nutrient transporters. Mechanistically, both bacterial strains and ornithine enhanced antioxidant capacity and nutrient uptake by activating Nrf2 signaling.

CONCLUSIONS

Dietary intervention using L. vaginalis LD11 and L. ingluviei CC32 contributes to high feed efficiency by producing ornithine, which modulates the duodenal microbiota and enhances the intestinal physiological functions for nutrient absorption Video Abstract.