Synergy between Cell Surface Glycosidases and Glycan-Binding Proteins Dictates the Utilization of Specific Beta(1,3)-Glucans by Human Gut Bacteroides

Déjean, Guillaume; Tamura, Kazune; Cabrera, Adriana; Jain, Namrata; Pudlo, Nicholas A.; Pereira, Gabriel; Viborg, Alexander Holm; Van Petegem, Filip; Martens, Eric C.; Brumer, Harry; Comstock, Laurie E.

doi:10.1128/mBio.00095-20

Synergy between Cell Surface Glycosidases and Glycan-Binding Proteins Dictates the Utilization of Specific Beta(1,3)-Glucans by Human Gut Bacteroides

Journal Article · Tue Apr 07 00:00:00 EDT 2020 · mBio (Online)

DOI:https://doi.org/10.1128/mBio.00095-20· OSTI ID:1629655

Déjean, Guillaume ^[1]; Tamura, Kazune ^[2]; Cabrera, Adriana ^[3]; Jain, Namrata ^[4]; Pudlo, Nicholas A. ^[5]; Pereira, Gabriel ^[5]; Viborg, Alexander Holm ^[3]; ^[6]; Martens, Eric C. ^[5]; ^[7]; Comstock, Laurie E.

Univ. of British Columbia, Vancouver, BC (Canada). Michael Smith Labs.; DOE/OSTI
Univ. of British Columbia, Vancouver, BC (Canada). Michael Smith Labs.; Univ. of British Columbia, Vancouver, BC (Canada). Dept. of Biochemistry and Molecular Biology
Univ. of British Columbia, Vancouver, BC (Canada). Michael Smith Labs.
Univ. of British Columbia, Vancouver, BC (Canada). Michael Smith Labs.; Univ. of British Columbia, Vancouver, BC (Canada). Dept. of Chemistry
Univ. of Michigan, Ann Arbor, MI (United States). Medical School. Dept. of Microbiology and Immunology
Univ. of British Columbia, Vancouver, BC (Canada). Dept. of Biochemistry and Molecular Biology
Univ. of British Columbia, Vancouver, BC (Canada). Michael Smith Labs.; Univ. of British Columbia, Vancouver, BC (Canada). Dept. of Biochemistry and Molecular Biology; Univ. of British Columbia, Vancouver, BC (Canada). Dept. of Chemistry; Univ. of British Columbia, Vancouver, BC (Canada). Dept. of Botany

The human gut microbiota (HGM) has far-reaching impacts on human health and nutrition, which are fueled primarily by the metabolism of otherwise indigestible complex carbohydrates commonly known as dietary fiber. However, the molecular basis of the ability of individual taxa of the HGM to address specific dietary glycan structures remains largely unclear. In particular, the utilization of β(1,3)-glucans, which are widespread in the human diet as yeast, seaweed, and plant cell walls, had not previously been resolved. Through a systems-based approach, here we show that the symbiont Bacteroides uniformis deploys a single, exemplar polysaccharide utilization locus (PUL) to access yeast β(1,3)-glucan, brown seaweed β(1,3)-glucan (laminarin), and cereal mixed-linkage β(1,3)/β(1,4)-glucan. Combined biochemical, enzymatic, and structural analysis of PUL-encoded glycoside hydrolases (GHs) and surface glycan-binding proteins (SGBPs) illuminates a concerted molecular system by which B. uniformis recognizes and saccharifies these distinct β-glucans. Strikingly, the functional characterization of homologous β(1,3)-glucan utilization loci (1,3GUL) in other Bacteroides further demonstrated that the ability of individual taxa to utilize β(1,3)-glucan variants and/or β(1,3)/β(1,4)-glucans arises combinatorially from the individual specificities of SGBPs and GHs at the cell surface, which feed corresponding signals to periplasmic hybrid two-component sensors (HTCSs) via TonB-dependent transporters (TBDTs). These data reveal the importance of cooperativity in the adaptive evolution of GH and SGBP cohorts to address individual polysaccharide structures. We anticipate that this fine-grained knowledge of PUL function will inform metabolic network analysis and proactive manipulation of the HGM. Indeed, a survey of 2,441 public human metagenomes revealed the international, yet individual-specific, distribution of each 1,3GUL.

View Accepted Manuscript (DOE)

Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1629655

Alternate ID(s):: OSTI ID: 1745057

Journal Information:: mBio (Online), Journal Name: mBio (Online) Journal Issue: 2 Vol. 11; ISSN 2150-7511

Publisher:: American Society for Microbiology (ASM)Copyright Statement

Country of Publication:: United States

Language:: English

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