Prebiotic galactooligosaccharide feed modifies the chicken gut microbiota to efficiently clear Salmonella

Richards, Philip J.; Almutrafy, Abeer; Liang, Lu; Flaujac Lafontaine, Geraldine M.; King, Elizabeth; Fish, Neville M.; Connerton, Amber J.; Connerton, Phillippa L.; Connerton, Ian F.

Abstract

Chicken meat is contaminated with Salmonella from the gut of infected chickens during slaughter. Eradication of Salmonella from broiler chickens through hygiene measures and/or vaccination is not cost-effective; complementary approaches are required. A mature gut microbiota obstructs Salmonella infection in chickens, and deliberate fortification of colonization resistance through prebiotic feed formulations would benefit public health and poultry production. Prebiotic galactooligosaccharides hastens Salmonella clearance from the gut of infected chickens. To better understand the role of galactooligosaccharides in colonization resistance, broiler chickens were raised on a wheat-soybean meal-based feed, with or without galactooligosaccharides for the first 24 days of life. Chickens were orally challenged with Salmonella enterica serovar Enteritidis at 20 days and the effect of supplementary galactooligosaccharides characterized by profiling Salmonella colonization, gut microbiota, innate immune response, and cecal short-chain fatty acid concentrations. Exposure to dietary galactooligosaccharides shortened the time to clear S. Enteritidis from the ceca. Differential abundance analysis of the cecal microbiota associated Salmonella challenge with a bacterial taxon belonging to the Acidaminococcaceae family (P < 0.005). Increased cecal concentrations of the short-chain fatty acids propionate and valerate were measured in Salmonella-challenged chickens sustained on either control or galactooligosaccharide-supplemented feed relative to mock-challenged controls; but far greater concentrations were detected in chickens fed a galactooligosaccharide-supplemented diet in early life. The abundance of the Acidaminococcaceae taxon exhibited a positive correlation with the cecal concentrations of propionate (ρ = 0.724, P = 0.008) and valerate (ρ = 0.71, P = 0.013). The absence of cecal pro-inflammatory transcriptional responses suggest that the rapid Salmonella clearance observed for the galactooligosaccharide-supplemented diet was not linked to innate immune function. IMPORTANCE: Work presented here identifies bacterial taxa responsible for colonization resistance to Salmonella in broiler chickens. Deliberate cultivation of these taxa with prebiotic galactooligosaccharide has potential as a straight-forward, safe, and cost-effective intervention against Salmonella. We hypothesize that catabolism of galactooligosaccharide and its breakdown products by indigenous microorganisms colonizing the chicken gut produce excess levels of propionate. In the absence of gross inflammation, propionate is inimical to Salmonella and hastens intestinal clearance.

Citation

Richards, P. J., Almutrafy, A., Liang, L., Flaujac Lafontaine, G. M., King, E., Fish, N. M., Connerton, A. J., Connerton, P. L., & Connerton, I. F. (2024). Prebiotic galactooligosaccharide feed modifies the chicken gut microbiota to efficiently clear Salmonella. mSystems, 9(8), Article e00754-24. https://doi.org/10.1128/msystems.00754-24

• Journal Article Type: Article
• Acceptance Date: Jun 8, 2024
• Online Publication Date: Jul 31, 2024
• Publication Date: 2024-08
• Deposit Date: Aug 29, 2024
• Publicly Available Date: Sep 3, 2024
• Journal: mSystems
• Electronic ISSN: 2379-5077
• Publisher: American Society for Microbiology
• Peer Reviewed: Peer Reviewed
• Volume: 9
• Issue: 8
• Article Number: e00754-24
• DOI: https://doi.org/10.1128/msystems.00754-24
• Public URL: https://nottingham-repository.worktribe.com/output/37943685
• Publisher URL: https://journals.asm.org/doi/10.1128/msystems.00754-24