Phocaeicola vulgatus promote growth rate via tryptophan metabolism pathway mediated gut sIgA production in Taihe Silky fowl

INTRODUCTION: Taihe Silky Fowl (TSF) has a long growth cycle and slow growth rate, how to effectively improve the growth rate of TSF has become the primary concern for breeders. Currently, extensive research has established the gut microbiota's role in modulating growth rate of commercial chicken breeds, while the specific microbial mechanisms influencing TSF growth rate remain poorly understood. OBJECTIVES: Therefore, this study aimed to identify growth rate-associated key microbial species in TSF through multi-omics approaches, experimentally validate their growth-promoting roles via controlled interventions, and elucidate the species-metabolite-host interaction mechanisms. METHODS: Cecal metagenome and metabolome was used to search for differential key microbiota and metabolites of TSF with different growth rate, the whole genome of key microbiota was used to identify the relationship between microbiota and metabolites, and gavage key microbiota to TSF was used to demonstrate the effectiveness of probiotics and preliminarily explore their mechanisms of action. RESULTS: Cecal metagenome analysis demonstrated a significant enrichment of Phocaeicola vulgatus (P. vulgatus) in high-growth-rate fowls, Erysipelotrichaceae bacterium was significantly enriched in low-growth-rate fowls. The differential metabolites between the two groups were significantly enriched in tryptophan metabolism pathway. Subsequently, gene analysis revealed that P. vulgatus encoded tryptophan biosynthesis genes. In feeding experiment, oral gavage P. vulgatus improved the TSF final body weight, average growth rate and average daily gain, increased cecal P. vulgatus abundance, enriched the metabolites in tryptophan metabolism pathway both in the cecum and serum, and upregulated cecal tissue gene expression in the 'intestinal immune network for IgA production' pathway resulting in the higher secretory IgA (sIgA) concentrations in cecal tissue and luminal content than the control group. CONCLUSION: P. vulgatus promoted the growth rate of TSF by optimizing the cecal microbiota, elevating cecal tryptophan metabolites and stimulating sIgA production via sIgA gene upregulation in cecal tissues, thereby enhancing host immune modulation. These findings elucidated the microbiota-metabolite-host axis governing TSF growth regulation, providing both mechanistic insights and practical applications for probiotic-based strategies to enhance growth performance and gut health in this valuable poultry breed.