Metabolism of dietary glycans is pivotal in shaping the human gut microbiota. However, the mechanisms that promote competition for glycans among gut commensals remain unclear. Roseburia intestinalis, an abundant butyrate-producing Firmicute, is a key degrader of the major dietary fibre xylan. Despite the association of this taxon to a healthy microbiota, insight is lacking into its glycan utilization machinery. This study examined the apparatus that confers the growth of R. intestinalis on arabino- and glucuronoxylans.
R. intestinalis displays a large cell-attached modular xylanase that promotes multivalent and dynamic association to xylan via four xylan-binding modules, one of which represents a previously unknown family of xylan binding modules with lower affinity than canonical xylan binding modules from known families.
This xylanase of glycoside hydrolase 10, which is conserved in the R. intestinalis species, operates in concert with an ATP-binding cassette (ABC) transporter to mediate breakdown and selective internalization of xylan oligomers. The solute binding protein of this ABC transporter was characterized to reveal the binding preference for oligomers of 4–5 xylosyl units, which is different from the corresponding transport protein from a model xylan-degrading Bacteroides commensal that targets larger ligands. Although R. intestinalis and the Bacteroides competitor co-grew in a mixed culture on xylan, R. intestinalis dominated on the preferred transport substrate xylotetraose. These findings highlight the differentiation of capture and transport preferences as a possible strategy to facilitate co-growth on abundant dietary fibres and may offer a unique route to manipulate the microbiota based on glycan transport preferences in therapeutic interventions to boost distinct taxa.
Danish Research Council for Independent Research, Natural Sciences (DFF, FNU) by a Research Project 2 grant (Grant ID: 4002-00297B to MAH), DTU for a PhD Scholarship to MLL, a BIONÆR project (grant number 244259) and the Norwegian NMR Platform, NNP (FLA) from the Research Council of Norway and (226244 to BW).
- Leth, M.L., Ejby, M., Workman, C., Ewald, D.A., Pedersen, S.S., Sternberg, C., Bahl, M.I., Licht, T.R., Aachmann, F.L., Westereng, B., and Abou Hachem, M. (2018) Differential bacterial capture and transport preferences facilitate co-growth on dietary xylan in the human gut. Nature Microbiology, 3: 570-580