Surface Glycan-binding Proteins Are Essential for Cereal Beta-glucan Utilization by the Human Gut Symbiont Bacteroides Ovatus
Overview
Authors
Affiliations
The human gut microbiota, which underpins nutrition and systemic health, is compositionally sensitive to the availability of complex carbohydrates in the diet. The Bacteroidetes comprise a dominant phylum in the human gut microbiota whose members thrive on dietary and endogenous glycans by employing a diversity of highly specific, multi-gene polysaccharide utilization loci (PUL), which encode a variety of carbohydrases, transporters, and sensor/regulators. PULs invariably also encode surface glycan-binding proteins (SGBPs) that play a central role in saccharide capture at the outer membrane. Here, we present combined biophysical, structural, and in vivo characterization of the two SGBPs encoded by the Bacteroides ovatus mixed-linkage β-glucan utilization locus (MLGUL), thereby elucidating their key roles in the metabolism of this ubiquitous dietary cereal polysaccharide. In particular, molecular insight gained through several crystallographic complexes of SGBP-A and SGBP-B with oligosaccharides reveals that unique shape complementarity of binding platforms underpins specificity for the kinked MLG backbone vis-à-vis linear β-glucans. Reverse-genetic analysis revealed that both the presence and binding ability of the SusD homolog BoSGBP-A are essential for growth on MLG, whereas the divergent, multi-domain BoSGBP-B is dispensable but may assist in oligosaccharide scavenging from the environment. The synthesis of these data illuminates the critical role SGBPs play in concert with other MLGUL components, reveals new structure-function relationships among SGBPs, and provides fundamental knowledge to inform future (meta)genomic, biochemical, and microbiological analyses of the human gut microbiota.
Li X, Lippens G, Parrou J, Cioci G, Esque J, Wang Z mSphere. 2024; 9(8):e0027824.
PMID: 39012103 PMC: 11351036. DOI: 10.1128/msphere.00278-24.
Metagenome-derived SusD-homologs affiliated with Bacteroidota bind to synthetic polymers.
Silverio M, Neumann T, Schaubruch K, Heermann R, Perez-Garcia P, Chow J Appl Environ Microbiol. 2024; 90(7):e0093324.
PMID: 38953372 PMC: 11267923. DOI: 10.1128/aem.00933-24.
Ma X, Wang B, Wei W, Tan F, Su H, Zhang J Appl Environ Microbiol. 2024; 90(5):e0004624.
PMID: 38563787 PMC: 11107165. DOI: 10.1128/aem.00046-24.
Colosimo R, Harris H, Ahn-Jarvis J, Troncoso-Rey P, Finnigan T, Wilde P Commun Biol. 2024; 7(1):272.
PMID: 38443511 PMC: 10915147. DOI: 10.1038/s42003-024-05893-4.
Tannock G Microbiol Mol Biol Rev. 2023; 88(1):e0012722.
PMID: 38126754 PMC: 10966955. DOI: 10.1128/mmbr.00127-22.