Synthetic microbial community improves chicken intestinal homeostasis and provokes anti-Salmonella immunity mediated by segmented filamentous bacteria

Abstract Applying synthetic microbial communities to manipulate the gut microbiota is a promising manner for reshaping the chicken gut microbial community. However, it remains elusive the role of a designed microbial community in chicken physiological metabolism and immune responses. In this study, we constructed a 10-member synthetic microbial community (SynComBac10) that recapitulated the phylogenetic diversity and functional capability of adult chicken intestinal microbiota. We found that early-life SynComBac10 exposure significantly enhanced chicken growth performance and facilitated the maturation of both the intestinal epithelial barrier function and the gut microbiota. Additionally, SynComBac10 promoted the pre-colonization and growth of segmented filamentous bacteria (SFB), which in turn induced Th17 cell-mediated immune responses, thereby conferring resistance to Salmonella infection. Through metagenomic sequencing, we assembled the genomes of two distinct species of SFB from the chicken gut microbiota, which displayed common metabolic deficiencies with SFB of other host origins. In silico analyses indicated that the SynComBac10-stimulated early establishment of SFB in the chicken intestine was likely through SynComBac10-derived metabolite cross-feeding. Our study demonstrated the pivotal role of a designed microbial consortium in promoting chicken gut homeostasis and anti-infection immunity, providing a new avenue for engineering chicken gut microbiota.