Molecular Dissection of Xyloglucan Recognition in a Prominent Human Gut Symbiont

Tauzin, Alexandra S.; Kwiatkowski, Kurt J.; Orlovsky, Nicole I.; Smith, Christopher J.; Creagh, A. Louise; Haynes, Charles A.; Wawrzak, Zdzislaw; Brumer, Harry; Koropatkin, Nicole M.

doi:10.1128/mBio.02134-15

Molecular Dissection of Xyloglucan Recognition in a Prominent Human Gut Symbiont

Journal Article · Tue Apr 26 04:00:00 EDT 2016 · mBio (Online)

DOI:https://doi.org/10.1128/mBio.02134-15· OSTI ID:1498418

Tauzin, Alexandra S.; Kwiatkowski, Kurt J.; Orlovsky, Nicole I.; Smith, Christopher J.; Creagh, A. Louise; Haynes, Charles A.; Wawrzak, Zdzislaw; Brumer, Harry; Koropatkin, Nicole M.

ABSTRACT

Polysaccharide utilization loci (PUL) within the genomes of resident human gutBacteroidetesare central to the metabolism of the otherwise indigestible complex carbohydrates known as “dietary fiber.” However, functional characterization of PUL lags significantly behind sequencing efforts, which limits physiological understanding of the human-bacterial symbiosis. In particular, the molecular basis of complex polysaccharide recognition, an essential prerequisite to hydrolysis by cell surface glycosidases and subsequent metabolism, is generally poorly understood. Here, we present the biochemical, structural, and reverse genetic characterization of two unique cell surface glycan-binding proteins (SGBPs) encoded by a xyloglucan utilization locus (XyGUL) fromBacteroides ovatus, which are integral to growth on this key dietary vegetable polysaccharide. Biochemical analysis reveals that these outer membrane-anchored proteins are in fact exquisitely specific for the highly branched xyloglucan (XyG) polysaccharide. The crystal structure of SGBP-A, a SusD homolog, with a bound XyG tetradecasaccharide reveals an extended carbohydrate-binding platform that primarily relies on recognition of the β-glucan backbone. The unique, tetra-modular structure of SGBP-B is comprised of tandem Ig-like folds, with XyG binding mediated at the distal C-terminal domain. Despite displaying similar affinities for XyG, reverse-genetic analysis reveals that SGBP-B is only required for the efficient capture of smaller oligosaccharides, whereas the presence of SGBP-A is more critical than its carbohydrate-binding ability for growth on XyG. Together, these data demonstrate that SGBP-A and SGBP-B play complementary, specialized roles in carbohydrate capture byB. ovatusand elaborate a model of how vegetable xyloglucans are accessed by theBacteroidetes.

IMPORTANCETheBacteroidetesare dominant bacteria in the human gut that are responsible for the digestion of the complex polysaccharides that constitute “dietary fiber.” Although this symbiotic relationship has been appreciated for decades, little is currently known about howBacteroidetesseek out and bind plant cell wall polysaccharides as a necessary first step in their metabolism. Here, we provide the first biochemical, crystallographic, and genetic insight into how two surface glycan-binding proteins from the complexBacteroides ovatusxyloglucan utilization locus (XyGUL) enable recognition and uptake of this ubiquitous vegetable polysaccharide. Our combined analysis illuminates new fundamental aspects of complex polysaccharide recognition, cleavage, and import at theBacteroidetescell surface that may facilitate the development of prebiotics to target this phylum of gut bacteria.

Research Organization:: Advanced Photon Source (APS), Argonne National Laboratory (ANL), Argonne, IL (US)

Sponsoring Organization:: DOE - BASIC ENERGY SCIENCESFOREIGN

OSTI ID:: 1498418

Journal Information:: mBio (Online), Journal Name: mBio (Online) Journal Issue: 2 Vol. 7; ISSN 2150-7511

Publisher:: American Society for Microbiology

Country of Publication:: United States

Language:: ENGLISH

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