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.
Highlights
Understanding metabolic interactions underlying assembly, maintenance, and dietary response of gut microbial communities is expected to provide a foundation for diagnostics, disease prevention, and therapeutic treatment of dysbiosis-related syndromes and diseases via rational nutritional supplementation
To test whether the abundance of B-vitamin auxotrophs in gut microbial communities are affected by the dietary supply of these micronutrients, we have established a model using gnotobiotic mice colonized with human fecal samples
This study of syntrophic metabolism of B-vitamins was to a large extent inspired by groundbreaking work by Goodman et al (2009) which provided the first strong evidence of syntrophy in metabolism of vitamin B12 in the gut microbial community
Summary
Understanding metabolic interactions underlying assembly, maintenance, and dietary response of gut microbial communities is expected to provide a foundation for diagnostics, disease prevention, and therapeutic treatment of dysbiosis-related syndromes and diseases via rational nutritional supplementation. This concept is illustrated by studies evaluating the effects of complementary foods on healthy maturation of infant gut microbiota that were convincingly demonstrated in the context of severe acute malnutrition (Blanton et al, 2016). These gene functions provide the driving force for the establishment and maintenance of mutualistic relationships including both microbe-microbe and host-microbe interactions. A combination of in vitro microbiological co-culture studies and the use of gnotobiotic mice have led to a broadened appreciation of the evolutionary strategies underlying functional interactions that define higher-order networks within microbial communities (Faith et al, 2010; Rey et al, 2010)
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