Distinct protein architectures mediate species-specific beta-glucan binding and metabolism in the human gut microbiota
Abstract
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 obtainedmore »
- Authors:
-
[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
- Publication Date:
- Research Org.:
- 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 Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES); USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1832581
- Grant/Contract Number:
- AC02-06CH11357; AC02-76SF00515
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Journal of Biological Chemistry
- Additional Journal Information:
- Journal Volume: 296; Journal ID: ISSN 0021-9258
- Publisher:
- American Society for Biochemistry and Molecular Biology
- Country of Publication:
- United States
- Language:
- ENGLISH
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; human gut microbiota; Bacteroidetes; Bacteroides; polysaccharide utilization locus; beta-glucan; complex carbohydrate; dietary fiber; surface glycan-binding protein; SusD; carbohydrate-binding module
Citation Formats
Tamura, Kazune, Dejean, Guillaume, Van Petegem, Filip, and Brumer, Harry. Distinct protein architectures mediate species-specific beta-glucan binding and metabolism in the human gut microbiota. United States: N. p., 2021.
Web. doi:10.1016/j.jbc.2021.100415.
Tamura, Kazune, Dejean, Guillaume, Van Petegem, Filip, & Brumer, Harry. Distinct protein architectures mediate species-specific beta-glucan binding and metabolism in the human gut microbiota. United States. https://doi.org/10.1016/j.jbc.2021.100415
Tamura, Kazune, Dejean, Guillaume, Van Petegem, Filip, and Brumer, Harry. Sat .
"Distinct protein architectures mediate species-specific beta-glucan binding and metabolism in the human gut microbiota". United States. https://doi.org/10.1016/j.jbc.2021.100415. https://www.osti.gov/servlets/purl/1832581.
@article{osti_1832581,
title = {Distinct protein architectures mediate species-specific beta-glucan binding and metabolism in the human gut microbiota},
author = {Tamura, Kazune and Dejean, Guillaume and Van Petegem, Filip and Brumer, Harry},
abstractNote = {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.},
doi = {10.1016/j.jbc.2021.100415},
journal = {Journal of Biological Chemistry},
number = ,
volume = 296,
place = {United States},
year = {Sat Feb 13 00:00:00 EST 2021},
month = {Sat Feb 13 00:00:00 EST 2021}
}
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