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

Title: 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.

View Accepted Manuscript (DOE)

Cite

Export

Save

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

Journal Information:: 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

References (82)

Gut bacteria selectively promoted by dietary fibers alleviate type 2 diabetes Zhao, Liping; Zhang, Feng; Ding, Xiaoying Science, Vol. 359, Issue 6380 https://doi.org/10.1126/science.aao5774	journal	March 2018
Transfer of carbohydrate-active enzymes from marine bacteria to Japanese gut microbiota Hehemann, Jan-Hendrik; Correc, Gaëlle; Barbeyron, Tristan Nature, Vol. 464, Issue 7290 https://doi.org/10.1038/nature08937	journal	April 2010
SusE facilitates starch uptake independent of starch binding in B. thetaiotaomicron : SusE promotes starch uptake in Foley, Matthew H.; Martens, Eric C.; Koropatkin, Nicole M. Molecular Microbiology, Vol. 108, Issue 5 https://doi.org/10.1111/mmi.13949	journal	April 2018
Overview of the CCP 4 suite and current developments Winn, Martyn D.; Ballard, Charles C.; Cowtan, Kevin D. Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S0907444910045749	journal	March 2011
How members of the human gut microbiota overcome the sulfation problem posed by glycosaminoglycans Cartmell, Alan; Lowe, Elisabeth C.; Baslé, Arnaud Proceedings of the National Academy of Sciences, Vol. 114, Issue 27 https://doi.org/10.1073/pnas.1704367114	journal	June 2017
Iterative model building, structure refinement and density modification with the PHENIX AutoBuild wizard Terwilliger, Thomas C.; Grosse-Kunstleve, Ralf W.; Afonine, Pavel V. Acta Crystallographica Section D Biological Crystallography, Vol. 64, Issue 1 https://doi.org/10.1107/S090744490705024X	journal	December 2007
Multidomain Carbohydrate-binding Proteins Involved in Bacteroides thetaiotaomicron Starch Metabolism Cameron, Elizabeth A.; Maynard, Mallory A.; Smith, Christopher J. Journal of Biological Chemistry, Vol. 287, Issue 41 https://doi.org/10.1074/jbc.M112.397380	journal	August 2012
Molecular basis for the preferential recognition of β1,3‐1,4‐glucans by the family 11 carbohydrate‐binding module from Clostridium thermocellum Ribeiro, Diana O.; Viegas, Aldino; Pires, Virgínia M. R. The FEBS Journal, Vol. 287, Issue 13 https://doi.org/10.1111/febs.15162	journal	December 2019
DIALS : implementation and evaluation of a new integration package Winter, Graeme; Waterman, David G.; Parkhurst, James M. Acta Crystallographica Section D Structural Biology, Vol. 74, Issue 2 https://doi.org/10.1107/S2059798317017235	journal	February 2018
Glycan utilization systems in the human gut microbiota: a gold mine for structural discoveries Tamura, Kazune; Brumer, Harry Current Opinion in Structural Biology, Vol. 68 https://doi.org/10.1016/j.sbi.2020.11.001	journal	June 2021
Sorting the diverse: The sequencebased classifications of carbohydrateactive enzymes Davies, Gideon J.; Sinnott, Michael L. The Biochemist, Vol. 30, Issue 4 https://doi.org/10.1042/BIO03004026	journal	August 2008
MolProbity: More and better reference data for improved all-atom structure validation: PROTEIN SCIENCE.ORG Williams, Christopher J.; Headd, Jeffrey J.; Moriarty, Nigel W. Protein Science, Vol. 27, Issue 1 https://doi.org/10.1002/pro.3330	journal	November 2017
Convergent and divergent mechanisms of sugar recognition across kingdoms Taylor, Maureen E.; Drickamer, Kurt Current Opinion in Structural Biology, Vol. 28 https://doi.org/10.1016/j.sbi.2014.07.003	journal	October 2014
Molecular basis of an agarose metabolic pathway acquired by a human intestinal symbiont Pluvinage, Benjamin; Grondin, Julie M.; Amundsen, Carolyn Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-03366-x	journal	March 2018
How good are my data and what is the resolution? Evans, Philip R.; Murshudov, Garib N. Acta Crystallographica Section D Biological Crystallography, Vol. 69, Issue 7 https://doi.org/10.1107/S0907444913000061	journal	June 2013
Insights into the κ/ι-carrageenan metabolism pathway of some marine Pseudoalteromonas species Hettle, Andrew G.; Hobbs, Joanne K.; Pluvinage, Benjamin Communications Biology, Vol. 2, Issue 1 https://doi.org/10.1038/s42003-019-0721-y	journal	December 2019
Decision-making in structure solution using Bayesian estimates of map quality: the PHENIX AutoSol wizard Terwilliger, Thomas C.; Adams, Paul D.; Read, Randy J. Acta Crystallographica Section D Biological Crystallography, Vol. 65, Issue 6 https://doi.org/10.1107/S0907444909012098	journal	May 2009
β-1,3-Glucan Binding by a Thermostable Carbohydrate-Binding Module from Thermotoga maritima ^† Boraston, Alisdair B.; Warren, R. Antony J.; Kilburn, Douglas G. Biochemistry, Vol. 40, Issue 48 https://doi.org/10.1021/bi015760g	journal	December 2001
Methods used in the structure determination of bovine mitochondrial F1 ATPase Abrahams, J. P.; Leslie, A. G. W. Acta Crystallographica Section D Biological Crystallography, Vol. 52, Issue 1 https://doi.org/10.1107/S0907444995008754	journal	January 1996
You are what you eat: diet, health and the gut microbiota Zmora, Niv; Suez, Jotham; Elinav, Eran Nature Reviews Gastroenterology & Hepatology, Vol. 16, Issue 1 https://doi.org/10.1038/s41575-018-0061-2	journal	September 2018
Surface glycan-binding proteins are essential for cereal beta-glucan utilization by the human gut symbiont Bacteroides ovatus Tamura, Kazune; Foley, Matthew H.; Gardill, Bernd R. Cellular and Molecular Life Sciences, Vol. 76, Issue 21 https://doi.org/10.1007/s00018-019-03115-3	journal	May 2019
CCP 4 i 2: the new graphical user interface to the CCP 4 program suite Potterton, Liz; Agirre, Jon; Ballard, Charles Acta Crystallographica Section D Structural Biology, Vol. 74, Issue 2 https://doi.org/10.1107/S2059798317016035	journal	February 2018
Microbiota in Allergy and Asthma and the Emerging Relationship with the Gut Microbiome Fujimura, Kei E.; Lynch, Susan V. Cell Host & Microbe, Vol. 17, Issue 5 https://doi.org/10.1016/j.chom.2015.04.007	journal	May 2015
Carrageenan catabolism is encoded by a complex regulon in marine heterotrophic bacteria Ficko-Blean, Elizabeth; Préchoux, Aurélie; Thomas, François Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-01832-6	journal	November 2017
Structural basis for nutrient acquisition by dominant members of the human gut microbiota Glenwright, Amy J.; Pothula, Karunakar R.; Bhamidimarri, Satya P. Nature, Vol. 541, Issue 7637 https://doi.org/10.1038/nature20828	journal	January 2017
Super-Resolution Imaging of Live Anaerobic Bacteria: Assembly and Dynamics of the B. Theta Starch Utilization System Karunatilaka, Krishanthi; Cameron, Elizabeth; Coupland, Ben Biophysical Journal, Vol. 104, Issue 2 https://doi.org/10.1016/j.bpj.2012.11.2909	journal	January 2013
Glycan recognition by the Bacteroidetes Sus-like systems Bolam, David N.; Koropatkin, Nicole M. Current Opinion in Structural Biology, Vol. 22, Issue 5 https://doi.org/10.1016/j.sbi.2012.06.006	journal	October 2012
Prediction of lipoprotein signal peptides in Gram-negative bacteria Juncker, Agnieszka S.; Willenbrock, Hanni; von Heijne, Gunnar Protein Science, Vol. 12, Issue 8 https://doi.org/10.1110/ps.0303703	journal	August 2003
Molecular recognition of the beta‐glucans laminarin and pustulan by a SusD‐like glycan‐binding protein of a marine Bacteroidetes Mystkowska, Agata Anna; Robb, Craig; Vidal‐Melgosa, Silvia The FEBS Journal, Vol. 285, Issue 23 https://doi.org/10.1111/febs.14674	journal	October 2018
Scaling and assessment of data quality Evans, Philip Acta Crystallographica Section D Biological Crystallography, Vol. 62, Issue 1, p. 72-82 https://doi.org/10.1107/S0907444905036693	journal	December 2005
The abundance and variety of carbohydrate-active enzymes in the human gut microbiota Kaoutari, Abdessamad El; Armougom, Fabrice; Gordon, Jeffrey I. Nature Reviews Microbiology, Vol. 11, Issue 7 https://doi.org/10.1038/nrmicro3050	journal	June 2013
DALI and the persistence of protein shape Holm, Liisa Protein Science, Vol. 29, Issue 1 https://doi.org/10.1002/pro.3749	journal	November 2019
The Starch Utilization System Assembles around Stationary Starch-Binding Proteins Tuson, Hannah H.; Foley, Matthew H.; Koropatkin, Nicole M. Biophysical Journal, Vol. 115, Issue 2 https://doi.org/10.1016/j.bpj.2017.12.015	journal	July 2018
XDS Kabsch, Wolfgang Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2 https://doi.org/10.1107/S0907444909047337	journal	January 2010
Insights into SusCD-mediated glycan import by a prominent gut symbiont Gray, Declan A.; White, Joshua B. R.; Oluwole, Abraham O. Nature Communications, Vol. 12, Issue 1 https://doi.org/10.1038/s41467-020-20285-y	journal	January 2021
Molecular Dissection of Xyloglucan Recognition in a Prominent Human Gut Symbiont Tauzin, Alexandra S.; Kwiatkowski, Kurt J.; Orlovsky, Nicole I. mBio, Vol. 7, Issue 2 https://doi.org/10.1128/mBio.02134-15	journal	April 2016
PULDB: the expanded database of Polysaccharide Utilization Loci Terrapon, Nicolas; Lombard, Vincent; Drula, Élodie Nucleic Acids Research, Vol. 46, Issue D1 https://doi.org/10.1093/nar/gkx1022	journal	October 2017
Structural dissection of a complex Bacteroides ovatus gene locus conferring xyloglucan metabolism in the human gut Hemsworth, Glyn R.; Thompson, Andrew J.; Stepper, Judith Open Biology, Vol. 6, Issue 7 https://doi.org/10.1098/rsob.160142	journal	July 2016
Transforming medicine with the microbiome Zmora, Niv; Soffer, Eliran; Elinav, Eran Science Translational Medicine, Vol. 11, Issue 477 https://doi.org/10.1126/scitranslmed.aaw1815	journal	January 2019
A comparative study on structure–function relations of mixed-linkage (1→3), (1→4) linear β-d-glucans Lazaridou, A.; Biliaderis, C. G.; Micha-Screttas, M. Food Hydrocolloids, Vol. 18, Issue 5 https://doi.org/10.1016/j.foodhyd.2004.01.002	journal	September 2004
Tandem Repeat of a Seven-Bladed β-Propeller Domain in Oligoxyloglucan Reducing-End-Specific Cellobiohydrolase Yaoi, Katsuro; Kondo, Hidemasa; Noro, Natsuko Structure, Vol. 12, Issue 7 https://doi.org/10.1016/j.str.2004.04.020	journal	July 2004
Structure and mechanism of endo/exocellulase E4 from Thermomonospora fusca Sakon, Joshua; Irwin, Diana; Wilson, David B. Nature Structural Biology, Vol. 4, Issue 10 https://doi.org/10.1038/nsb1097-810	journal	October 1997
A surface endogalactanase in Bacteroides thetaiotaomicron confers keystone status for arabinogalactan degradation Cartmell, Alan; Muñoz-Muñoz, Jose; Briggs, Jonathon A. Nature Microbiology, Vol. 3, Issue 11 https://doi.org/10.1038/s41564-018-0258-8	journal	October 2018
Complex N-glycan breakdown by gut Bacteroides involves an extensive enzymatic apparatus encoded by multiple co-regulated genetic loci Briliūtė, Justina; Urbanowicz, Paulina A.; Luis, Ana S. Nature Microbiology, Vol. 4, Issue 9 https://doi.org/10.1038/s41564-019-0466-x	journal	June 2019
The Buccaneer software for automated model building. 1. Tracing protein chains Cowtan, Kevin Acta Crystallographica Section D Biological Crystallography, Vol. 62, Issue 9 https://doi.org/10.1107/S0907444906022116	journal	August 2006
The Crystal Structure of the Family 6 Carbohydrate Binding Module from Cellvibrio mixtus Endoglucanase 5A in Complex with Oligosaccharides Reveals Two Distinct Binding Sites with Different Ligand Specificities Pires, Virgínia M. R.; Henshaw, Joanna L.; Prates, José A. M. Journal of Biological Chemistry, Vol. 279, Issue 20 https://doi.org/10.1074/jbc.M401599200	journal	May 2004
Structure and Ligand Binding of Carbohydrate-binding Module CsCBM6-3 Reveals Similarities with Fucose-specific Lectins and “Galactose-binding” Domains Boraston, Alisdair B.; Notenboom, Valerie; Warren, R. Antony J. Journal of Molecular Biology, Vol. 327, Issue 3 https://doi.org/10.1016/S0022-2836(03)00152-9	journal	March 2003
Reduction in circulating bile acid and restricted diffusion across the intestinal epithelium are associated with a decrease in blood cholesterol in the presence of oat β-glucan Gunness, Purnima; Michiels, Joris; Vanhaecke, Lynn The FASEB Journal, Vol. 30, Issue 12 https://doi.org/10.1096/fj.201600465R	journal	December 2016
Privateer: software for the conformational validation of carbohydrate structures Agirre, Jon; Iglesias-Fernández, Javier; Rovira, Carme Nature Structural & Molecular Biology, Vol. 22, Issue 11 https://doi.org/10.1038/nsmb.3115	journal	November 2015
xia2 : an expert system for macromolecular crystallography data reduction Winter, G. Journal of Applied Crystallography, Vol. 43, Issue 1 https://doi.org/10.1107/S0021889809045701	journal	December 2009
A Dietary Fiber-Deprived Gut Microbiota Degrades the Colonic Mucus Barrier and Enhances Pathogen Susceptibility Desai, Mahesh S.; Seekatz, Anna M.; Koropatkin, Nicole M. Cell, Vol. 167, Issue 5 https://doi.org/10.1016/j.cell.2016.10.043	journal	November 2016
Ten years of CAZypedia: a living encyclopedia of carbohydrate-active enzymes Glycobiology, Vol. 28, Issue 1, p. 3-8 https://doi.org/10.1093/glycob/cwx089	journal	October 2017
The carbohydrate-active enzymes database (CAZy) in 2013 Lombard, Vincent; Golaconda Ramulu, Hemalatha; Drula, Elodie Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1178	journal	November 2013
Starch Catabolism by a Prominent Human Gut Symbiont Is Directed by the Recognition of Amylose Helices Koropatkin, Nicole M.; Martens, Eric C.; Gordon, Jeffrey I. Structure, Vol. 16, Issue 7 https://doi.org/10.1016/j.str.2008.03.017	journal	July 2008
Features and development of Coot Emsley, P.; Lohkamp, B.; Scott, W. G. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/S0907444910007493	journal	March 2010
Complex pectin metabolism by gut bacteria reveals novel catalytic functions Ndeh, Didier; Rogowski, Artur; Cartmell, Alan Nature, Vol. 544, Issue 7648 https://doi.org/10.1038/nature21725	journal	March 2017
REFMAC 5 for the refinement of macromolecular crystal structures Murshudov, Garib N.; Skubák, Pavol; Lebedev, Andrey A. Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S0907444911001314	journal	March 2011
Molecular Mechanism by which Prominent Human Gut Bacteroidetes Utilize Mixed-Linkage Beta-Glucans, Major Health-Promoting Cereal Polysaccharides Tamura, Kazune; Hemsworth, Glyn R.; Déjean, Guillaume Cell Reports, Vol. 21, Issue 2 https://doi.org/10.1016/j.celrep.2017.09.049	journal	October 2017
Polysaccharide Utilization Loci: Fueling Microbial Communities Grondin, Julie M.; Tamura, Kazune; Déjean, Guillaume Journal of Bacteriology, Vol. 199, Issue 15 https://doi.org/10.1128/JB.00860-16	journal	January 2017
Dietary pectic glycans are degraded by coordinated enzyme pathways in human colonic Bacteroides Luis, Ana S.; Briggs, Jonathon; Zhang, Xiaoyang Nature Microbiology, Vol. 3, Issue 2 https://doi.org/10.1038/s41564-017-0079-1	journal	December 2017
Expression and Purification of Soluble His6-Tagged TEV Protease Tropea, Joseph E.; Cherry, Scott; Waugh, David S. Methods in Molecular Biology https://doi.org/10.1007/978-1-59745-196-3_19	book	January 2009
Glycan complexity dictates microbial resource allocation in the large intestine Rogowski, Artur; Briggs, Jonathon A.; Mortimer, Jennifer C. Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms8481	journal	June 2015
PHENIX: a comprehensive Python-based system for macromolecular structure solution Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221 https://doi.org/10.1107/S0907444909052925	journal	January 2010
Diet–microbiota interactions and personalized nutrition Kolodziejczyk, Aleksandra A.; Zheng, Danping; Elinav, Eran Nature Reviews Microbiology, Vol. 17, Issue 12 https://doi.org/10.1038/s41579-019-0256-8	journal	September 2019
A discrete genetic locus confers xyloglucan metabolism in select human gut Bacteroidetes Larsbrink, Johan; Rogers, Theresa E.; Hemsworth, Glyn R. Nature, Vol. 506, Issue 7489 https://doi.org/10.1038/nature12907	journal	January 2014
How glycan metabolism shapes the human gut microbiota Koropatkin, Nicole M.; Cameron, Elizabeth A.; Martens, Eric C. Nature Reviews Microbiology, Vol. 10, Issue 5 https://doi.org/10.1038/nrmicro2746	journal	April 2012
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 mBio, Vol. 11, Issue 2 https://doi.org/10.1128/mBio.00095-20	journal	April 2020
Recognition and Degradation of Plant Cell Wall Polysaccharides by Two Human Gut Symbionts Martens, Eric C.; Lowe, Elisabeth C.; Chiang, Herbert PLoS Biology, Vol. 9, Issue 12 https://doi.org/10.1371/journal.pbio.1001221	journal	December 2011
Bacteria of the human gut microbiome catabolize red seaweed glycans with carbohydrate-active enzyme updates from extrinsic microbes Hehemann, J. -H.; Kelly, A. G.; Pudlo, N. A. Proceedings of the National Academy of Sciences, Vol. 109, Issue 48 https://doi.org/10.1073/pnas.1211002109	journal	November 2012
Diet rapidly and reproducibly alters the human gut microbiome David, Lawrence A.; Maurice, Corinne F.; Carmody, Rachel N. Nature, Vol. 505, Issue 7484 https://doi.org/10.1038/nature12820	journal	December 2013
Structure of a SusD Homologue, BT1043, Involved in Mucin O -Glycan Utilization in a Prominent Human Gut Symbiont ^† ^, ^‡ Koropatkin, Nicole; Martens, Eric C.; Gordon, Jeffrey I. Biochemistry, Vol. 48, Issue 7 https://doi.org/10.1021/bi801942a	journal	February 2009
Automated macromolecular model building for X-ray crystallography using ARP/wARP version 7 Langer, Gerrit; Cohen, Serge X.; Lamzin, Victor S. Nature Protocols, Vol. 3, Issue 7 https://doi.org/10.1038/nprot.2008.91	journal	June 2008
The Critical Roles of Polysaccharides in Gut Microbial Ecology and Physiology Porter, Nathan T.; Martens, Eric C. Annual Review of Microbiology, Vol. 71, Issue 1 https://doi.org/10.1146/annurev-micro-102215-095316	journal	September 2017
Data processing and analysis with the autoPROC toolbox Vonrhein, Clemens; Flensburg, Claus; Keller, Peter Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S0907444911007773	journal	March 2011
Dietary supplementation with β-glucan enriched oat bran increases faecal concentration of carboxylic acids in healthy subjects Nilsson, U.; Johansson, M.; Nilsson, Å European Journal of Clinical Nutrition, Vol. 62, Issue 8 https://doi.org/10.1038/sj.ejcn.1602816	journal	May 2007
Family 6 Carbohydrate Binding Modules Recognize the Non-reducing End of β-1,3-Linked Glucans by Presenting a Unique Ligand Binding Surface van Bueren, Alicia Lammerts; Morland, Carl; Gilbert, Harry J. Journal of Biological Chemistry, Vol. 280, Issue 1 https://doi.org/10.1074/jbc.M410113200	journal	October 2004
Differential Oligosaccharide Recognition by Evolutionarily-related β-1,4 and β-1,3 Glucan-binding Modules Boraston, Alisdair B.; Nurizzo, Didier; Notenboom, Valerie Journal of Molecular Biology, Vol. 319, Issue 5 https://doi.org/10.1016/S0022-2836(02)00374-1	journal	June 2002
SOLVE and RESOLVE: automated structure solution, density modification and model building Terwilliger, Thomas Journal of Synchrotron Radiation, Vol. 11, Issue 1 https://doi.org/10.1107/S0909049503023938	journal	November 2003
Gut Microbiota from Twins Discordant for Obesity Modulate Metabolism in Mice Ridaura, V. K.; Faith, J. J.; Rey, F. E. Science, Vol. 341, Issue 6150 https://doi.org/10.1126/science.1241214	journal	September 2013
Molecular Interactions of β-(1→3)-Glucans with Their Receptors Legentil, Laurent; Paris, Franck; Ballet, Caroline Molecules, Vol. 20, Issue 6 https://doi.org/10.3390/molecules20069745	journal	May 2015
Phaser crystallographic software McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D. Journal of Applied Crystallography, Vol. 40, Issue 4 https://doi.org/10.1107/S0021889807021206	journal	July 2007
Advances in understanding the molecular basis of plant cell wall polysaccharide recognition by carbohydrate-binding modules Gilbert, Harry J.; Knox, J. Paul; Boraston, Alisdair B. Current Opinion in Structural Biology, Vol. 23, Issue 5 https://doi.org/10.1016/j.sbi.2013.05.005	journal	October 2013

Similar Records

Surface glycan-binding proteins are essential for cereal beta-glucan utilization by the human gut symbiont Bacteroides ovatus

Journal Article · Mon May 06 00:00:00 EDT 2019 · Cellular and Molecular Life Sciences · OSTI ID:1832581

Tamura, Kazune; Foley, Matthew H.; Gardill, Bernd R.; +7 more

Molecular Dissection of Xyloglucan Recognition in a Prominent Human Gut Symbiont

Journal Article · Tue Apr 26 00:00:00 EDT 2016 · mBio (Online) · OSTI ID:1832581

Tauzin, Alexandra S.; Kwiatkowski, Kurt J.; Orlovsky, Nicole I.; +6 more

Molecular Dissection of Xyloglucan Recognition in a Prominent Human Gut Symbiont

Journal Article · Wed May 04 00:00:00 EDT 2016 · mBio · OSTI ID:1832581

Tauzin, Alexandra S.; Kwiatkowski, Kurt J.; Orlovsky, Nicole I.; +8 more

Related Subjects

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

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

Citation Formats

References (82)

Similar Records

Related Subjects