Abstract:
Xanthan gum is a branched polysaccharide with complex sugar linkage structure and unique rheological properties making it useful as a food additive in a variety of processed foods that are widely consumed in modern human diets. Here, we show that the ability to utilize xanthan gum is surprisingly common in human gut microbiomes and appears to be contingent on the activity of a single uncultured bacterium that is a member of Ruminococcaceae uncultured genus 13 (R. UCG13). Using genome-centric metatranscriptomics, activity-guided proteomics, and recombinant enzyme studies, we demonstrate that this keystone degrader cleaves xanthan gum with a novel glycoside hydrolase family 5 (GH5); the released oligosaccharides are subsequently depolymerized to monosaccharides by a series of intracellular enzymes. In some cases, oligosaccharide products of this pathway also cross-feed Bacteroides intestinalis strains equipped with their own distinct enzymatic pathway. Thus, introduction of this common food additive into the human diet in the past 50 years has promoted the establishment of a food web between members of two different phyla of gut bacteria on comparatively short timescales. We have recently found evidence of a similar xanthan degrading locus in the mouse microbiome, suggesting that this locus and organism may have been transferred to humans via environmental reservoirs in other mammalian microbiomes.