In-depth characterisation of a selection of gut commensal bacteria reveals their functional capacities to metabolise dietary carbohydrates with prebiotic potential

Abstract

The microbial utilisation of dietary carbohydrates is closely linked to the pivotal role of the gut microbiome in human health. Inherent to the modulation of complex microbial communities, a prebiotic implies the selective utilisation of specific substrate, relying on the metabolic capacities of targeted microbes. In this study, we investigated the metabolic capacities of 17 commensal bacteria of the human gut microbiome toward dietary carbohydrates with prebiotic potential. First, in vitro experiments allowed the classification of bacterial growth and fermentation profiles in response to various carbon sources, including agave inulin, corn fiber, polydextrose and citrus pectin. The influence of phylogenetic affiliation appeared to statistically outweigh carbon sources in determining the degrees of carbohydrate utilisation. Secondly, we narrowed our focus on six commensal bacteria representative of the Bacteroidetes and Firmicutes phyla to perform an untargeted HR-LC/MS metabolomic analysis. Bacteroides xylanisolvens, Bacteroides thetaiotaomicron, Bacteroides intestinalis, Subdoligranulum variabile, Roseburia intestinalis and Eubacterium rectale exhibited distinct metabolomic profiles in response to different carbon sources. The relative abundance of bacterial metabolites was significantly influenced by dietary carbohydrates, with these effects being strain-specific and/or carbohydrate-specific. Particularly, the findings indicated an elevation in short-chain fatty acids and other metabolites, including succinate, gamma-aminobutyric acid, and nicotinic acid. These metabolites were associated with putative health benefits. Finally, an RNA-Seq transcriptomic approach provided deeper insights into the underlying mechanisms of carbohydrate metabolisation. Restricting our focus on four commensal bacteria, including B. xylanisolvens, B. thetaiotaomicron, S. variabile and R. intestinalis, carbon sources did significantly modulate the level of bacterial genes related to the enzymatic machinery involved in the metabolisation of dietary carbohydrates. This study provides a holistic view of the molecular strategies induced during the dynamic interplay between dietary carbohydrates with prebiotic potential and gut commensal bacteria.