Deciphering Bifidobacterial-mediated Metabolic Interactions and Their Impact on Gut Microbiota by a Multi-omics Approach

The intricacies of cooperation and competition between microorganisms are poorly investigated for particular components of the gut microbiota. In order to obtain insights into the manner by which different bifidobacterial species coexist in the mammalian gut, we investigated possible interactions between four human gut commensals, Bifidobacterium bifidum PRL2010, Bifidobacterium adolescentis 22L, Bifidobacterium breve 12L and Bifidobacterium longum subsp. infantis ATCC15697, in the intestine of conventional mice. The generated information revealed various ecological/metabolic strategies, including glycan-harvesting, glycan-breakdown and cross-feeding behavior, adopted by bifidobacteria in the highly competitive environment of the mammalian intestine. Introduction of two or multiple bifidobacterial strains caused a clear shift in the microbiota composition of the murine cecum. Whole-genome transcription profiling coupled with metagenomic analyses of single, dual or multiple associations of bifidobacterial strains revealed an expansion of the murine gut glycobiome toward enzymatic degradation of plant-derived carbohydrates, such as xylan, arabinoxylan, starch and host-derived glycan substrates. Furthermore, these bifidobacterial communities evoked major changes in the metabolomic profile of the microbiota as observed by shifts in short chain fatty acid production and carbohydrate availability in the murine cecum. Overall, these data support an ecological role of bifidobacteria acting directly or through cross-feeding activities in shaping the gut murine microbiome to instigate an enrichment of saccharolytic microbiota.