Dataset Information

B-Vitamin Sharing Promotes Stability of Gut Microbial Communities.

ABSTRACT: Cross-feeding on intermediary and end-point metabolites plays an important role in the dynamic interactions of host-associated microbial communities. While gut microbiota possess inherent resilience to perturbation, variations in the intake of certain nutrients may lead to changes in the community composition with potential consequences on host physiology. Syntrophic relationships and mutualism at the level of major carbon and energy sources have been documented, however, relatively little is known about metabolic interactions involving micronutrients, such as B-vitamins, biosynthetic precursors of essential cofactors in the mammalian host and numerous members of the gut microbiota alike. In silico genomic reconstruction and prediction of community-wide metabolic phenotypes for eight major B-vitamins (B1, B2, B3, B5, B6, B7, B9, and B12), suggests that a significant fraction of microbial gut communities (>20% by abundance) are represented by auxotrophic species whose viability is strictly dependent on acquiring one or more B-vitamins from diet and/or prototrophic microbes via committed salvage pathways. Here, we report the stability of gut microbiota using humanized gnotobiotic mice and in vitro anaerobic fecal culture in the context of extreme variations of dietary B-vitamin supply as revealed by phylotype-to-phenotype prediction from 16S rRNA profiling and metabolomic measurements. The observed nearly unaltered relative abundance of auxotrophic species in gut communities in the face of diet or media lacking B-vitamins or containing them in great excess (?30-fold above normal) points to a strong contribution of metabolic cooperation (B-vitamin exchange and sharing) to the stability of gut bacterial populations.

SUBMITTER: Sharma V

PROVIDER: S-EPMC6615432 | biostudies-literature | 2019

REPOSITORIES: biostudies-literature

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B-Vitamin Sharing Promotes Stability of Gut Microbial Communities.

Sharma Vandana V Rodionov Dmitry A DA Leyn Semen A SA Tran David D Iablokov Stanislav N SN Ding Hua H Peterson Daniel A DA Osterman Andrei L AL Peterson Scott N SN

Frontiers in microbiology 20190702

Cross-feeding on intermediary and end-point metabolites plays an important role in the dynamic interactions of host-associated microbial communities. While gut microbiota possess inherent resilience to perturbation, variations in the intake of certain nutrients may lead to changes in the community composition with potential consequences on host physiology. Syntrophic relationships and mutualism at the level of major carbon and energy sources have been documented, however, relatively little is kn ...[more]

PMID: 31333610

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Project description:We investigated the requirement of 15 human butyrate-producing gut bacterial strains for eight B vitamins and the proteinogenic amino acids by a combination of genome sequence analysis and in vitro growth experiments. The Ruminococcaceae species Faecalibacterium prausnitzii and Subdoligranulum variabile were auxotrophic for most of the vitamins and the amino acid tryptophan. Within the Lachnospiraceae, most species were prototrophic for all amino acids and several vitamins, but biotin auxotrophy was widespread. In addition, most of the strains belonging to Eubacterium rectale and Roseburia spp., but few of the other Lachnospiraceae strains, were auxotrophic for thiamine and folate. Synthetic coculture experiments of five thiamine or folate auxotrophic strains with different prototrophic bacteria in the absence and presence of different vitamin concentrations were carried out. This demonstrated that cross-feeding between bacteria does take place and revealed differences in cross-feeding efficiency between prototrophic strains. Vitamin-independent growth stimulation in coculture compared to monococulture was also observed, in particular for F. prausnitzii A2-165, suggesting that it benefits from the provision of other growth factors from community members. The presence of multiple vitamin auxotrophies in the most abundant butyrate-producing Firmicutes species found in the healthy human colon indicates that these bacteria depend upon vitamins supplied from the diet or via cross-feeding from other members of the microbial community.IMPORTANCE Microbes in the intestinal tract have a strong influence on human health. Their fermentation of dietary nondigestible carbohydrates leads to the formation of health-promoting short-chain fatty acids, including butyrate, which is the main fuel for the colonic wall and has anticarcinogenic and anti-inflammatory properties. A good understanding of the growth requirements of butyrate-producing bacteria is important for the development of efficient strategies to promote these microbes in the gut, especially in cases where their abundance is altered. The demonstration of the inability of several dominant butyrate producers to grow in the absence of certain vitamins confirms the results of previous in silico analyses. Furthermore, establishing that strains prototrophic for thiamine or folate (butyrate producers and non-butyrate producers) were able to stimulate growth and affect the composition of auxotrophic synthetic communities suggests that the provision of prototrophic bacteria that are efficient cross feeders may stimulate butyrate-producing bacteria under certain in vivo conditions.

Dataset Information

B-Vitamin Sharing Promotes Stability of Gut Microbial Communities.

Publications

B-Vitamin Sharing Promotes Stability of Gut Microbial Communities.

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