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.; Dejean, Guillaume; Schnizlein, Matthew; Bahr, Constance E.; Louise Creagh, A.; van Petegem, Filip; Koropatkin, Nicole M.; Brumer, Harry

doi:10.1007/s00018-019-03115-3

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

DOI:https://doi.org/10.1007/s00018-019-03115-3· OSTI ID:1573405

Tamura, Kazune ^[1]; Foley, Matthew H. ^[2]; Gardill, Bernd R. ^[1]; Dejean, Guillaume ^[1]; Schnizlein, Matthew ^[2]; Bahr, Constance E. ^[2]; Louise Creagh, A. ^[1]; van Petegem, Filip ^[1]; Koropatkin, Nicole M. ^[2]; ^[1]

Univ. of British Columbia, Vancouver, BC (Canada)
Univ. of Michigan, Ann Arbor, MI (United States)

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_MLG-A are essential for growth on MLG, whereas the divergent, multi-domain BoSGBP_MLG-B is dispensable but may assist in oligosaccharide scavenging from the environment. Overall, 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.

View Accepted Manuscript (DOE)

Research Organization:: Advanced Photon Source (APS), Argonne National Laboratory (ANL), Argonne, IL (US)

Sponsoring Organization:: National Institutes of Health (NIH); USDOE Office of Science (SC), Biological and Environmental Research (BER)

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

OSTI ID:: 1573405

Journal Information:: Cellular and Molecular Life Sciences, Journal Name: Cellular and Molecular Life Sciences Journal Issue: 21 Vol. 76; ISSN 1420-682X

Country of Publication:: United States

Language:: ENGLISH

References (93)

Signal Peptidases Paetzel, Mark; Karla, Andrew; Strynadka, Natalie C. J. ChemInform, Vol. 34, Issue 6 https://doi.org/10.1002/chin.200306271	journal	February 2003
The microbiome and cancer: The microbiome and cancer Goodman, Brian; Gardner, Humphrey The Journal of Pathology, Vol. 244, Issue 5 https://doi.org/10.1002/path.5047	journal	March 2018
Predicting Secretory Proteins with SignalP Nielsen, Henrik Methods in Molecular Biology https://doi.org/10.1007/978-1-4939-7015-5_6	book	January 2017
Production of Selenomethionyl Proteins in Prokaryotic and Eukaryotic Expression Systems Doublié, Sylvie Methods in Molecular Biology https://doi.org/10.1007/978-1-59745-209-0_5	book	January 2007
Addition of arabinoxylan and mixed linkage glucans in porcine diets affects the large intestinal bacterial populations Gorham, John B.; Kang, Seungha; Williams, Barbara A. European Journal of Nutrition, Vol. 56, Issue 6 https://doi.org/10.1007/s00394-016-1263-4	journal	July 2016
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
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
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 7 https://doi.org/10.1016/j.celrep.2017.11.013	journal	November 2017
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
Starving our Microbial Self: The Deleterious Consequences of a Diet Deficient in Microbiota-Accessible Carbohydrates Sonnenburg, Erica D.; Sonnenburg, Justin L. Cell Metabolism, Vol. 20, Issue 5 https://doi.org/10.1016/j.cmet.2014.07.003	journal	November 2014
An Ecological Network of Polysaccharide Utilization among Human Intestinal Symbionts Rakoff-Nahoum, Seth; Coyne, Michael J.; Comstock, Laurie E. Current Biology, Vol. 24, Issue 1 https://doi.org/10.1016/j.cub.2013.10.077	journal	January 2014
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
A general, robust method for the quality control of intact proteins using LC–ESI-MS Sundqvist, Gustav; Stenvall, Maria; Berglund, Helena Journal of Chromatography B, Vol. 852, Issue 1-2 https://doi.org/10.1016/j.jchromb.2007.01.011	journal	June 2007
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
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
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
[20] Processing of X-ray diffraction data collected in oscillation mode Otwinowski, Zbyszek; Minor, Wladek Macromolecular Crystallography Part A, 307-326 https://doi.org/10.1016/s0076-6879(97)76066-x	book	January 1997
Carbohydrate–Aromatic Interactions Asensio, Juan Luis; Ardá, Ana; Cañada, Francisco Javier Accounts of Chemical Research, Vol. 46, Issue 4 https://doi.org/10.1021/ar300024d	journal	June 2012
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
Role of (1,3)(1,4)-β-Glucan in Cell Walls: Interaction with Cellulose Kiemle, Sarah N.; Zhang, Xiao; Esker, Alan R. Biomacromolecules, Vol. 15, Issue 5 https://doi.org/10.1021/bm5001247	journal	April 2014
Signal Peptidases Paetzel, Mark; Karla, Andrew; Strynadka, Natalie C. J. Chemical Reviews, Vol. 102, Issue 12 https://doi.org/10.1021/cr010166y	journal	December 2002
Carbohydrate–Aromatic Interactions in Proteins Hudson, Kieran L.; Bartlett, Gail J.; Diehl, Roger C. Journal of the American Chemical Society, Vol. 137, Issue 48 https://doi.org/10.1021/jacs.5b08424	journal	November 2015
An obesity-associated gut microbiome with increased capacity for energy harvest Turnbaugh, Peter J.; Ley, Ruth E.; Mahowald, Michael A. Nature, Vol. 444, Issue 7122 https://doi.org/10.1038/nature05414	journal	December 2006
Gut microbiota composition correlates with diet and health in the elderly Claesson, Marcus J.; Jeffery, Ian B.; Conde, Susana Nature, Vol. 488, Issue 7410 https://doi.org/10.1038/nature11319	journal	July 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
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
Dynamics and associations of microbial community types across the human body Ding, Tao; Schloss, Patrick D. Nature, Vol. 509, Issue 7500 https://doi.org/10.1038/nature13178	journal	April 2014
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
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
SignalP 4.0: discriminating signal peptides from transmembrane regions Petersen, Thomas Nordahl; Brunak, Søren; von Heijne, Gunnar Nature Methods, Vol. 8, Issue 10 https://doi.org/10.1038/nmeth.1701	journal	September 2011
The microbiome and cancer Schwabe, Robert F.; Jobin, Christian Nature Reviews Cancer, Vol. 13, Issue 11 https://doi.org/10.1038/nrc3610	journal	October 2013
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
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
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
Prenatal food insecurity post Hurricane Maria is associated with decreased Veillonella in the infant gut Wang, Leyao; de Ángel Solá, David; Acevedo Flores, Midnela Pediatric Research, Vol. 88, Issue 6 https://doi.org/10.1038/s41390-020-0839-0	journal	March 2020
Metagenomics reveals functional synergy and novel polysaccharide utilization loci in the Castor canadensis fecal microbiome Armstrong, Zachary; Mewis, Keith; Liu, Feng The ISME Journal, Vol. 12, Issue 11 https://doi.org/10.1038/s41396-018-0215-9	journal	July 2018
Cavin1 intrinsically disordered domains are essential for fuzzy electrostatic interactions and caveola formation Tillu, Vikas A.; Rae, James; Gao, Ya Nature Communications, Vol. 12, Issue 1 https://doi.org/10.1038/s41467-021-21035-4	journal	February 2021
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
An exclusive metabolic niche enables strain engraftment in the gut microbiota Shepherd, Elizabeth Stanley; DeLoache, William C.; Pruss, Kali M. Nature, Vol. 557, Issue 7705 https://doi.org/10.1038/s41586-018-0092-4	journal	May 2018
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
Chemistry, physico-chemistry and applications linked to biological activities of β-glucans Barsanti, Laura; Passarelli, Vincenzo; Evangelista, Valtere Natural Product Reports, Vol. 28, Issue 3 https://doi.org/10.1039/c0np00018c	journal	January 2011
Structural and functional characterization of NanU, a novel high-affinity sialic acid-inducible binding protein of oral and gut-dwelling Bacteroidetes species Phansopa, Chatchawal; Roy, Sumita; Rafferty, John B. Biochemical Journal, Vol. 458, Issue 3 https://doi.org/10.1042/bj20131415	journal	February 2014
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
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
Structure-Function Analysis of a Mixed-linkage β-Glucanase/Xyloglucanase from the Key Ruminal Bacteroidetes Prevotella bryantii B ₁ 4 McGregor, Nicholas; Morar, Mariya; Fenger, Thomas Hauch Journal of Biological Chemistry, Vol. 291, Issue 3 https://doi.org/10.1074/jbc.M115.691659	journal	October 2015
Dali server: conservation mapping in 3D Holm, Liisa; Rosenstrï¿½m, Pï¿½ivi Nucleic Acids Research, Vol. 38, Issue suppl_2 https://doi.org/10.1093/nar/gkq366	journal	May 2010
Dali server update Holm, Liisa; Laakso, Laura M. Nucleic Acids Research, Vol. 44, Issue W1 https://doi.org/10.1093/nar/gkw357	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
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
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
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
Refinement of severely incomplete structures with maximum likelihood in BUSTER–TNT Blanc, E.; Roversi, P.; Vonrhein, C. Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12 https://doi.org/10.1107/s0907444904016427	journal	November 2004
Coot model-building tools for molecular graphics Emsley, Paul; Cowtan, Kevin Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12, p. 2126-2132 https://doi.org/10.1107/s0907444904019158	journal	November 2004
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
Molecular replacement with MOLREP Vagin, Alexei; Teplyakov, Alexei Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 1 https://doi.org/10.1107/s0907444909042589	journal	December 2009
XDS Kabsch, Wolfgang Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2 https://doi.org/10.1107/s0907444909047337	journal	January 2010
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
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
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
Towards automated crystallographic structure refinement with phenix.refine Afonine, Pavel V.; Grosse-Kunstleve, Ralf W.; Echols, Nathaniel Acta Crystallographica Section D Biological Crystallography, Vol. 68, Issue 4 https://doi.org/10.1107/s0907444912001308	journal	March 2012
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
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
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
Cellulose degradation in the human gut: Ruminococcus champanellensis expands the cellulosome paradigm Cann, Isaac; Bernardi, Rafael C.; Mackie, Roderick I. Environmental Microbiology, Vol. 18, Issue 2 https://doi.org/10.1111/1462-2920.13152	journal	January 2016
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
Engineering of the gut commensal bacterium Bacteroides ovatus to produce and secrete biologically active murine interleukin-2 in response to xylan Farrar, M. D.; Whitehead, T. R.; Lan, J. Journal of Applied Microbiology, Vol. 98, Issue 5 https://doi.org/10.1111/j.1365-2672.2005.02565.x	journal	May 2005
Cholesterol-lowering effects of oat β-glucan: Nutrition Reviews©, Vol. ••(••): ••-•• Othman, Rgia A.; Moghadasian, Mohammed H.; Jones, Peter JH Nutrition Reviews, Vol. 69, Issue 6 https://doi.org/10.1111/j.1753-4887.2011.00401.x	journal	June 2011
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
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
Early infancy microbial and metabolic alterations affect risk of childhood asthma Arrieta, Marie-Claire; Stiemsma, Leah T.; Dimitriu, Pedro A. Science Translational Medicine, Vol. 7, Issue 307 https://doi.org/10.1126/scitranslmed.aab2271	journal	September 2015
Two SusD-Like Proteins Encoded within a Polysaccharide Utilization Locus of an Uncultured Ruminant Bacteroidetes Phylotype Bind Strongly to Cellulose Mackenzie, A. K.; Pope, P. B.; Pedersen, H. L. Applied and Environmental Microbiology, Vol. 78, Issue 16 https://doi.org/10.1128/AEM.01164-12	journal	June 2012
A Polysaccharide Utilization Locus from an Uncultured Bacteroidetes Phylotype Suggests Ecological Adaptation and Substrate Versatility Mackenzie, A. K.; Naas, A. E.; Kracun, S. K. Applied and Environmental Microbiology, Vol. 81, Issue 1 https://doi.org/10.1128/AEM.02858-14	journal	October 2014
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
Do Rumen Bacteroidetes Utilize an Alternative Mechanism for Cellulose Degradation? Naas, A. E.; Mackenzie, A. K.; Mravec, J. mBio, Vol. 5, Issue 4 https://doi.org/10.1128/mBio.01401-14	journal	August 2014
Multifunctional Nutrient-Binding Proteins Adapt Human Symbiotic Bacteria for Glycan Competition in the Gut by Separately Promoting Enhanced Sensing and Catalysis Cameron, Elizabeth A.; Kwiatkowski, Kurt J.; Lee, Byung-Hoo mBio, Vol. 5, Issue 5 https://doi.org/10.1128/mBio.01441-14	journal	September 2014
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
Genetic Variation of the SusC/SusD Homologs from a Polysaccharide Utilization Locus Underlies Divergent Fructan Specificities and Functional Adaptation in Bacteroides thetaiotaomicron Strains Joglekar, Payal; Sonnenburg, Erica D.; Higginbottom, Steven K. mSphere, Vol. 3, Issue 3 https://doi.org/10.1128/mspheredirect.00185-18	journal	May 2018
Beta Glucan: Health Benefits in Obesity and Metabolic Syndrome El Khoury, D.; Cuda, C.; Luhovyy, B. L. Journal of Nutrition and Metabolism, Vol. 2012 https://doi.org/10.1155/2012/851362	journal	January 2012
The Host Microbiome Regulates and Maintains Human Health: A Primer and Perspective for Non-Microbiologists Thomas, Sunil; Izard, Jacques; Walsh, Emily Cancer Research, Vol. 77, Issue 8 https://doi.org/10.1158/0008-5472.can-16-2929	journal	March 2017
A polysaccharide utilization locus from Flavobacterium johnsoniae enables conversion of recalcitrant chitin Larsbrink, Johan; Zhu, Yongtao; Kharade, Sampada S. Biotechnology for Biofuels, Vol. 9, Issue 1 https://doi.org/10.1186/s13068-016-0674-z	journal	November 2016
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
Effects of Diet on Resource Utilization by a Model Human Gut Microbiota Containing Bacteroides cellulosilyticus WH2, a Symbiont with an Extensive Glycobiome McNulty, Nathan P.; Wu, Meng; Erickson, Alison R. PLoS Biology, Vol. 11, Issue 8 https://doi.org/10.1371/journal.pbio.1001637	journal	August 2013
Revised Estimates for the Number of Human and Bacteria Cells in the Body Sender, Ron; Fuchs, Shai; Milo, Ron PLOS Biology, Vol. 14, Issue 8 https://doi.org/10.1371/journal.pbio.1002533	journal	August 2016
An Examination of Diet for the Maintenance of Remission in Inflammatory Bowel Disease Haskey, Natasha; Gibson, Deanna L. Multidisciplinary Digital Publishing Institute https://doi.org/10.14288/1.0379250	text	January 2019
Role of the gut microbiota in defining human health Fujimura, Kei E.; Slusher, Nicole A.; Cabana, Michael D. Expert Review of Anti-infective Therapy, Vol. 8, Issue 4 https://doi.org/10.1586/eri.10.14	journal	April 2010
Dietary pectic glycans are degraded by coordinated enzyme pathways in human colonic Bacteroides. Luis, Ana S.; Briggs, Jonathon; Zhang, Xiaoyang Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.27636	text	January 2018
PHENIX: a comprehensive Python-based system for macromolecular structure solution. Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.45787	text	January 2010
Decision-making in structure solution using Bayesian estimates of map quality: the PHENIX AutoSol wizard. Terwilliger, Thomas C.; Adams, Paul D.; Read, Randy Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.49142	text	January 2009
Overview of the CCP4 suite and current developments. Winn, Martyn D.; Ballard, Charles C.; Cowtan, Kevin D. Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.52322	text	January 2011
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 Deutsches Elektronen-Synchrotron, DESY, Hamburg https://doi.org/10.3204/pubdb-2019-00024	text	January 2018
Gut Fermentation of Dietary Fibres: Physico-Chemistry of Plant Cell Walls and Implications for Health Williams, Barbara; Grant, Lucas; Gidley, Michael International Journal of Molecular Sciences, Vol. 18, Issue 10 https://doi.org/10.3390/ijms18102203	journal	October 2017
In Vitro Fermentation of Selected Prebiotics and Their Effects on the Composition and Activity of the Adult Gut Microbiota Fehlbaum, Sophie; Prudence, Kevin; Kieboom, Jasper International Journal of Molecular Sciences, Vol. 19, Issue 10 https://doi.org/10.3390/ijms19103097	journal	October 2018
An Examination of Diet for the Maintenance of Remission in Inflammatory Bowel Disease Haskey, Natasha; Gibson, Deanna Nutrients, Vol. 9, Issue 3 https://doi.org/10.3390/nu9030259	journal	March 2017

Cited By (1)

Adaptation of Syntenic Xyloglucan Utilization Loci of Human Gut Bacteroidetes to Polysaccharide Side Chain Diversity Déjean, Guillaume; Tauzin, Alexandra S.; Bennett, Stuart W. Applied and Environmental Microbiology, Vol. 85, Issue 20 https://doi.org/10.1128/aem.01491-19	journal	August 2019

Similar Records

A Cell-Surface GH9 Endo-Glucanase Coordinates with Surface Glycan-Binding Proteins to Mediate Xyloglucan Uptake in the Gut Symbiont Bacteroides ovatus

Journal Article · Fri Jan 18 19:00:00 EST 2019 · Journal of Molecular Biology · OSTI ID:1544856

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:1498418

Related Subjects

59 BASIC BIOLOGICAL SCIENCES

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

Citation Formats

References (93)

Cited By (1)

Similar Records

Related Subjects