Distinct protein architectures mediate species-specific beta-glucan binding and metabolism in the human gut microbiota

Tamura, Kazune; Dejean, Guillaume; Van Petegem, Filip; Brumer, Harry

doi:10.1016/j.jbc.2021.100415

Distinct protein architectures mediate species-specific beta-glucan binding and metabolism in the human gut microbiota

Journal Article · Sat Feb 13 00:00:00 EST 2021 · Journal of Biological Chemistry

DOI:https://doi.org/10.1016/j.jbc.2021.100415· OSTI ID:1832581

Tamura, Kazune ^[1]; ^[2]; ^[3]; ^[4]

Univ. of British Columbia, Vancouver, BC (Canada). Michael Smith Laboratories. Dept. of Biochemistry and Molecular Biology. The Life Sciences Inst.
Univ. of British Columbia, Vancouver, BC (Canada). Michael Smith Laboratories
Univ. of British Columbia, Vancouver, BC (Canada). Dept. of Biochemistry and Molecular Biology. The Life Sciences Inst.
Univ. of British Columbia, Vancouver, BC (Canada). Michael Smith Laboratories. Dept. of Biochemistry and Molecular Biology. The Life Sciences Inst. Dept. of Chemistry

Complex glycans that evade our digestive system are major nutrients that feed the human gut microbiota (HGM). The prevalence of Bacteroidetes in the HGM of populations worldwide is engendered by the evolution of polysaccharide utilization loci (PULs), which encode concerted protein systems to utilize the myriad complex glycans in our diets. Despite their crucial roles in glycan recognition and transport, cell-surface glycan-binding proteins (SGBPs) remained understudied cogs in the PUL machinery. Here, we report the structural and biochemical characterization of a suite of SGBP-A and SGBP-B structures from three syntenic β(1,3)-glucan utilization loci (1,3GULs) from Bacteroides thetaiotaomicron (Bt), Bacteroides uniformis (Bu), and B. fluxus (Bf), which have varying specificities for distinct β-glucans. Ligand complexes provide definitive insight into β(1,3)-glucan selectivity in the HGM, including structural features enabling dual β(1,3)-glucan/mixed-linkage β(1,3)/β(1,4)-glucan-binding capability in some orthologs. The tertiary structural conservation of SusD-like SGBPs-A is juxtaposed with the diverse architectures and binding modes of the SGBPs-B. Specifically, the structures of the trimodular BtSGBP-B and BuSGBP-B revealed a tandem repeat of carbohydrate-binding module-like domains connected by long linkers. In contrast, BfSGBP-B comprises a bimodular architecture with a distinct β-barrel domain at the C terminus that bears a shallow binding canyon. The molecular insights obtained here contribute to our fundamental understanding of HGM function, which in turn may inform tailored microbial intervention therapies.

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Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS); SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States). Stanford Synchrotron Radiation Lightsource (SSRL)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES); USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC02-06CH11357; AC02-76SF00515

OSTI ID:: 1832581

Alternate ID(s):: OSTI ID: 1834915

Journal Information:: Journal of Biological Chemistry, Journal Name: Journal of Biological Chemistry Vol. 296; ISSN 0021-9258

Publisher:: American Society for Biochemistry and Molecular BiologyCopyright Statement

Country of Publication:: United States

Language:: ENGLISH

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59 BASIC BIOLOGICAL SCIENCES
Bacteroides
Bacteroidetes
SusD
beta-glucan
carbohydrate-binding module
complex carbohydrate
dietary fiber
human gut microbiota
polysaccharide utilization locus
surface glycan-binding protein

Distinct protein architectures mediate species-specific beta-glucan binding and metabolism in the human gut microbiota

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References (86)

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