Glutamatergic system regulates feather pecking behaviors in laying hens: the gut-brain axis mechanism

Abstract

Abstract Background Feather pecking (FP), characterized by pecking at and pulling out of feathers of conspecifics, is a serious welfare and economic problem in laying hen husbandry. There is increasing evidence pointing pout to a critical role of gut microbiota in regulating host behaviors. However, the biological mechanism underlying the role of gut microbiota in FP is still unclear, evidenced by the lack of an appropriate treatment. Results In this work, we applied a multi-omics approach combined with a series of physiology assays to investigate the gut-brain axis of FP behavior. We show that chronic treatment with environmental stress induced severe FP accompanied by reduced production performance and increased anxiety- and depression-related behaviors, in comprison with control-treated laying hens. In addition, the immune system was severely suppressed in FP chickens. It is worth noting that the diversity and composition of gut microbiota were significantly altered, and thus leading to the reduced stability in microbial community. Importantly, a variety of differential metabolites were identified from non-targeted metabolomic analysis, which were mainly associated with arginine and histidine biosynthesis. A significant increase of glutamate levels was also observed in the hippocampus of FP chickens. Moreover, the eukaryotic transcriptome sequencing analysis revealed that the expressions of two glutamate-related receptors, GRIN2A and SLC17A6, were significantly upregulated in the hippocampus. Spearman correlation analysis showed that both genes GRIN2A and SLC17A6 in the hippocampus were significantly positively correlated with arginine levels in the duodenum, and Romboutsia in the duodenum were significantly negatively correlated with arginine. Conclusions Romboutsia and other bacteria genera in the intestine may increase the plasma levels of arginine and histidine by increasing the synthesis of arginine and histidine and decreasing the metabolism of arginine, which in turn increases glutamate levels and GRIN2A and SLC17A6 gene expression in the hippocampus, and regulates the glutamatergic system to influence the FP behavior of laying hens.