Bacteroides intestinalis DSM 17393, a member of the human colonic microbiome, upregulates multiple endoxylanases during growth on xylan

Kui Wang; Gabriel V Pereira; Janaina J V Cavalcante; Meiling Zhang; Roderick Mackie; Isaac Cann

doi:10.1038/srep34360

Bacteroides intestinalis DSM 17393, a member of the human colonic microbiome, upregulates multiple endoxylanases during growth on xylan

Sci Rep. 2016 Sep 29:6:34360. doi: 10.1038/srep34360.

Authors

Kui Wang^{1

2}, Gabriel V Pereira^{1

2

3}, Janaina J V Cavalcante^{1

2}, Meiling Zhang^{1

2

3}, Roderick Mackie^{1

2

3}, Isaac Cann^{1

2

3

4}

Affiliations

¹ Energy Biosciences Institute, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA.
² Carl R. Woese Institute for Genomic Biology, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA.
³ Department of Animal Science, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA.
⁴ Department of Microbiology, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA.

Abstract

Many human diets contain arabinoxylan, and the ease of genome sequencing coupled with reduced cost have led to unraveling the arsenal of genes utilized by the colonic Bacteroidetes to depolymerize this polysaccharide. The colonic Bacteroidetes with potential to ferment arabinoxylans include Bacteroides intestinalis. In this study, we analyzed the hydrolytic activities of members of a xylan degradation cluster encoded on the genome of Bacteroides intestinalis DSM 17393. Here, it is demonstrated that a cocktail of the xylanolytic enzymes completely hydrolyze arabinoxylans found in human diets. We show that this bacterium and relatives have evolved and secrete a unique bifunctional endoxylanase/arabinofuranosidase in the same polypeptide. The bifunctional enzyme and other secreted enzymes attack the polysaccharides extracellularly to remove the side-chains, exposing the xylan backbone for cleavage to xylo-oligosaccharides and xylose. These end products are transported into the cell where a β-xylosidase cleaves the oligosaccharides to fermentable sugars. While our experiments focused on B. intestinalis, it is likely that the extracellular enzymes also release nutrients to members of the colonic microbial community that practice cross-feeding. The presence of the genes characterized in this study in other colonic Bacteroidetes suggests a conserved strategy for energy acquisition from arabinoxylan, a component of human diets.