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

Abstract Background Chicken meat can be contaminated with Salmonella originating from the gastrointestinal tract of infected chickens during slaughter. Total eradication of Salmonella from flocks of broiler (meat) chickens through hygiene measures and/or vaccination regimes is not deemed cost-effective, so complementary approaches are sought. A mature gut microbiota is an obstruction to Salmonella infection in chickens and deliberate fortification of colonization resistance in juvenile chickens through prebiotic feed formulations would benefit both public health and the poultry industry. Prebiotic galactooligosaccharides have been shown to hasten clearance of Salmonellafrom 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 added galactooligosaccharide for the first 24-days of life. Chickens were then orally challenged with Salmonella enterica serovar Enteritidis at 20-days-old and the effect of supplementary galactooligosaccharides characterized by profiling Salmonella colonization, gut microbiota, host innate immune response and cecal SCFA concentrations. Results Exposure to dietary galactooligosaccharides shortened the time required for chickens 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. Increased concentrations of the short chain fatty acids propionate and valerate were measured in the ceca of 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. Propionate and valerate concentrations corresponded with the abundance of the Acidaminococcaceae taxon. The absence of cecal proinflammatory chemokine/cytokine transcriptional responses suggest that the Salmonella-clearance observed for the galactooligosaccharide-supplemented diet was not linked to the modulation of innate immune function. Conclusions We hypothesise that catabolism of galactooligosaccharide and its breakdown products by indigenous taxa colonizing the cecal pouches yield excess levels of propionate. In the absence of gross inflammation propionate is inimical to Salmonellawhich hastens the clearance time. Work presented here identifies some of the bacterial taxa responsible for colonization resistance to Salmonellacolonization in broiler chickens. Deliberate cultivation of these taxa with prebiotic galactooligosaccharide presents a straight-forward, safe and cost-effective intervention against Salmonella.