Surface glycan-binding proteins are essential for cereal beta-glucan utilization by the human gut symbiont Bacteroides ovatus
Abstract
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 BoSGBPMLG-A are essential for growth on MLG, whereas the divergent, multi-domain BoSGBPMLG-B is dispensable but may assist in oligosaccharide scavenging from the environment. Overall, the synthesis of these data illuminates the critical rolemore »
- Authors:
-
[1]
- Univ. of British Columbia, Vancouver, BC (Canada)
- Univ. of Michigan, Ann Arbor, MI (United States)
- Publication Date:
- Research Org.:
- Argonne National Lab. (ANL), Argonne, IL (United States). Advanced Photon Source (APS)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER); National Institutes of Health (NIH)
- OSTI Identifier:
- 1573405
- Grant/Contract Number:
- AC02–06CH11357; AC02–76SF00515; P41GM103393
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Cellular and Molecular Life Sciences
- Additional Journal Information:
- Journal Volume: 76; Journal Issue: 21; Journal ID: ISSN 1420-682X
- Country of Publication:
- United States
- Language:
- ENGLISH
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Tamura, Kazune, Foley, Matthew H., Gardill, Bernd R., Dejean, Guillaume, Schnizlein, Matthew, Bahr, Constance E., Louise Creagh, A., van Petegem, Filip, Koropatkin, Nicole M., and Brumer, Harry. Surface glycan-binding proteins are essential for cereal beta-glucan utilization by the human gut symbiont Bacteroides ovatus. United States: N. p., 2019.
Web. doi:10.1007/s00018-019-03115-3.
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. Surface glycan-binding proteins are essential for cereal beta-glucan utilization by the human gut symbiont Bacteroides ovatus. United States. https://doi.org/10.1007/s00018-019-03115-3
Tamura, Kazune, Foley, Matthew H., Gardill, Bernd R., Dejean, Guillaume, Schnizlein, Matthew, Bahr, Constance E., Louise Creagh, A., van Petegem, Filip, Koropatkin, Nicole M., and Brumer, Harry. Mon .
"Surface glycan-binding proteins are essential for cereal beta-glucan utilization by the human gut symbiont Bacteroides ovatus". United States. https://doi.org/10.1007/s00018-019-03115-3. https://www.osti.gov/servlets/purl/1573405.
@article{osti_1573405,
title = {Surface glycan-binding proteins are essential for cereal beta-glucan utilization by the human gut symbiont Bacteroides ovatus},
author = {Tamura, Kazune and Foley, Matthew H. and Gardill, Bernd R. and Dejean, Guillaume and Schnizlein, Matthew and Bahr, Constance E. and Louise Creagh, A. and van Petegem, Filip and Koropatkin, Nicole M. and Brumer, Harry},
abstractNote = {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 BoSGBPMLG-A are essential for growth on MLG, whereas the divergent, multi-domain BoSGBPMLG-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.},
doi = {10.1007/s00018-019-03115-3},
journal = {Cellular and Molecular Life Sciences},
number = 21,
volume = 76,
place = {United States},
year = {Mon May 06 00:00:00 EDT 2019},
month = {Mon May 06 00:00:00 EDT 2019}
}
Free Publicly Available Full Text
Publisher's Version of Record
Other availability
Search WorldCat to find libraries that may hold this journal
Cited by: 25 works
Citation information provided by
Web of Science
Web of Science
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
Chemistry, physico-chemistry and applications linked to biological activities of β-glucans
journal, January 2011
- Barsanti, Laura; Passarelli, Vincenzo; Evangelista, Valtere
- Natural Product Reports, Vol. 28, Issue 3
SusE facilitates starch uptake independent of starch binding in B. thetaiotaomicron : SusE promotes starch uptake in
journal, April 2018
- Foley, Matthew H.; Martens, Eric C.; Koropatkin, Nicole M.
- Molecular Microbiology, Vol. 108, Issue 5
The microbiome and cancer
journal, October 2013
- Schwabe, Robert F.; Jobin, Christian
- Nature Reviews Cancer, Vol. 13, Issue 11
How members of the human gut microbiota overcome the sulfation problem posed by glycosaminoglycans
journal, June 2017
- Cartmell, Alan; Lowe, Elisabeth C.; Baslé, Arnaud
- Proceedings of the National Academy of Sciences, Vol. 114, Issue 27
A Polysaccharide Utilization Locus from an Uncultured Bacteroidetes Phylotype Suggests Ecological Adaptation and Substrate Versatility
journal, October 2014
- Mackenzie, A. K.; Naas, A. E.; Kracun, S. K.
- Applied and Environmental Microbiology, Vol. 81, Issue 1
Early infancy microbial and metabolic alterations affect risk of childhood asthma
journal, September 2015
- Arrieta, Marie-Claire; Stiemsma, Leah T.; Dimitriu, Pedro A.
- Science Translational Medicine, Vol. 7, Issue 307
Multifunctional Nutrient-Binding Proteins Adapt Human Symbiotic Bacteria for Glycan Competition in the Gut by Separately Promoting Enhanced Sensing and Catalysis
journal, September 2014
- Cameron, Elizabeth A.; Kwiatkowski, Kurt J.; Lee, Byung-Hoo
- mBio, Vol. 5, Issue 5
Dali server update
journal, April 2016
- Holm, Liisa; Laakso, Laura M.
- Nucleic Acids Research, Vol. 44, Issue W1
Dali server: conservation mapping in 3D
journal, May 2010
- Holm, Liisa; Rosenstr�m, P�ivi
- Nucleic Acids Research, Vol. 38, Issue suppl_2
Multidomain Carbohydrate-binding Proteins Involved in Bacteroides thetaiotaomicron Starch Metabolism
journal, August 2012
- Cameron, Elizabeth A.; Maynard, Mallory A.; Smith, Christopher J.
- Journal of Biological Chemistry, Vol. 287, Issue 41
The Host Microbiome Regulates and Maintains Human Health: A Primer and Perspective for Non-Microbiologists
journal, March 2017
- Thomas, Sunil; Izard, Jacques; Walsh, Emily
- Cancer Research, Vol. 77, Issue 8
Cholesterol-lowering effects of oat β-glucan: Nutrition Reviews©, Vol. ••(••): ••-••
journal, June 2011
- Othman, Rgia A.; Moghadasian, Mohammed H.; Jones, Peter JH
- Nutrition Reviews, Vol. 69, Issue 6
SignalP 4.0: discriminating signal peptides from transmembrane regions
journal, September 2011
- Petersen, Thomas Nordahl; Brunak, Søren; von Heijne, Gunnar
- Nature Methods, Vol. 8, Issue 10
Engineering of the gut commensal bacterium Bacteroides ovatus to produce and secrete biologically active murine interleukin-2 in response to xylan
journal, May 2005
- Farrar, M. D.; Whitehead, T. R.; Lan, J.
- Journal of Applied Microbiology, Vol. 98, Issue 5
An exclusive metabolic niche enables strain engraftment in the gut microbiota
journal, May 2018
- Shepherd, Elizabeth Stanley; DeLoache, William C.; Pruss, Kali M.
- Nature, Vol. 557, Issue 7705
Gut microbiota composition correlates with diet and health in the elderly
journal, July 2012
- Claesson, Marcus J.; Jeffery, Ian B.; Conde, Susana
- Nature, Vol. 488, Issue 7410
Microbiota in Allergy and Asthma and the Emerging Relationship with the Gut Microbiome
journal, May 2015
- Fujimura, Kei E.; Lynch, Susan V.
- Cell Host & Microbe, Vol. 17, Issue 5
Structural basis for nutrient acquisition by dominant members of the human gut microbiota
journal, January 2017
- Glenwright, Amy J.; Pothula, Karunakar R.; Bhamidimarri, Satya P.
- Nature, Vol. 541, Issue 7637
Revised Estimates for the Number of Human and Bacteria Cells in the Body
journal, August 2016
- Sender, Ron; Fuchs, Shai; Milo, Ron
- PLOS Biology, Vol. 14, Issue 8
Glycan recognition by the Bacteroidetes Sus-like systems
journal, October 2012
- Bolam, David N.; Koropatkin, Nicole M.
- Current Opinion in Structural Biology, Vol. 22, Issue 5
Prediction of lipoprotein signal peptides in Gram-negative bacteria
journal, August 2003
- Juncker, Agnieszka S.; Willenbrock, Hanni; von Heijne, Gunnar
- Protein Science, Vol. 12, Issue 8
Dynamics and associations of microbial community types across the human body
journal, April 2014
- Ding, Tao; Schloss, Patrick D.
- Nature, Vol. 509, Issue 7500
Molecular recognition of the beta‐glucans laminarin and pustulan by a SusD‐like glycan‐binding protein of a marine Bacteroidetes
journal, October 2018
- Mystkowska, Agata Anna; Robb, Craig; Vidal‐Melgosa, Silvia
- The FEBS Journal, Vol. 285, Issue 23
The abundance and variety of carbohydrate-active enzymes in the human gut microbiota
journal, June 2013
- Kaoutari, Abdessamad El; Armougom, Fabrice; Gordon, Jeffrey I.
- Nature Reviews Microbiology, Vol. 11, Issue 7
Beta Glucan: Health Benefits in Obesity and Metabolic Syndrome
journal, January 2012
- El Khoury, D.; Cuda, C.; Luhovyy, B. L.
- Journal of Nutrition and Metabolism, Vol. 2012
Molecular Dissection of Xyloglucan Recognition in a Prominent Human Gut Symbiont
journal, April 2016
- Tauzin, Alexandra S.; Kwiatkowski, Kurt J.; Orlovsky, Nicole I.
- mBio, Vol. 7, Issue 2
PULDB: the expanded database of Polysaccharide Utilization Loci
journal, October 2017
- Terrapon, Nicolas; Lombard, Vincent; Drula, Élodie
- Nucleic Acids Research, Vol. 46, Issue D1
An Ecological Network of Polysaccharide Utilization among Human Intestinal Symbionts
journal, January 2014
- Rakoff-Nahoum, Seth; Coyne, Michael J.; Comstock, Laurie E.
- Current Biology, Vol. 24, Issue 1
A comparative study on structure–function relations of mixed-linkage (1→3), (1→4) linear β-d-glucans
journal, September 2004
- Lazaridou, A.; Biliaderis, C. G.; Micha-Screttas, M.
- Food Hydrocolloids, Vol. 18, Issue 5
Metagenomics reveals functional synergy and novel polysaccharide utilization loci in the Castor canadensis fecal microbiome
journal, July 2018
- Armstrong, Zachary; Mewis, Keith; Liu, Feng
- The ISME Journal, Vol. 12, Issue 11
Two SusD-Like Proteins Encoded within a Polysaccharide Utilization Locus of an Uncultured Ruminant Bacteroidetes Phylotype Bind Strongly to Cellulose
journal, June 2012
- Mackenzie, A. K.; Pope, P. B.; Pedersen, H. L.
- Applied and Environmental Microbiology, Vol. 78, Issue 16
A general, robust method for the quality control of intact proteins using LC–ESI-MS
journal, June 2007
- Sundqvist, Gustav; Stenvall, Maria; Berglund, Helena
- Journal of Chromatography B, Vol. 852, Issue 1-2
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
journal, December 2016
- Gunness, Purnima; Michiels, Joris; Vanhaecke, Lynn
- The FASEB Journal, Vol. 30, Issue 12
Privateer: software for the conformational validation of carbohydrate structures
journal, November 2015
- Agirre, Jon; Iglesias-Fernández, Javier; Rovira, Carme
- Nature Structural & Molecular Biology, Vol. 22, Issue 11
A Dietary Fiber-Deprived Gut Microbiota Degrades the Colonic Mucus Barrier and Enhances Pathogen Susceptibility
journal, November 2016
- Desai, Mahesh S.; Seekatz, Anna M.; Koropatkin, Nicole M.
- Cell, Vol. 167, Issue 5
In Vitro Fermentation of Selected Prebiotics and Their Effects on the Composition and Activity of the Adult Gut Microbiota
journal, October 2018
- Fehlbaum, Sophie; Prudence, Kevin; Kieboom, Jasper
- International Journal of Molecular Sciences, Vol. 19, Issue 10
Do Rumen Bacteroidetes Utilize an Alternative Mechanism for Cellulose Degradation?
journal, August 2014
- Naas, A. E.; Mackenzie, A. K.; Mravec, J.
- mBio, Vol. 5, Issue 4
Effects of Diet on Resource Utilization by a Model Human Gut Microbiota Containing Bacteroides cellulosilyticus WH2, a Symbiont with an Extensive Glycobiome
journal, August 2013
- McNulty, Nathan P.; Wu, Meng; Erickson, Alison R.
- PLoS Biology, Vol. 11, Issue 8
Starch Catabolism by a Prominent Human Gut Symbiont Is Directed by the Recognition of Amylose Helices
journal, July 2008
- Koropatkin, Nicole M.; Martens, Eric C.; Gordon, Jeffrey I.
- Structure, Vol. 16, Issue 7
Role of the gut microbiota in defining human health
journal, April 2010
- Fujimura, Kei E.; Slusher, Nicole A.; Cabana, Michael D.
- Expert Review of Anti-infective Therapy, Vol. 8, Issue 4
Molecular Mechanism by which Prominent Human Gut Bacteroidetes Utilize Mixed-Linkage Beta-Glucans, Major Health-Promoting Cereal Polysaccharides
journal, October 2017
- Tamura, Kazune; Hemsworth, Glyn R.; Déjean, Guillaume
- Cell Reports, Vol. 21, Issue 2
Signal Peptidases
journal, December 2002
- Paetzel, Mark; Karla, Andrew; Strynadka, Natalie C. J.
- Chemical Reviews, Vol. 102, Issue 12
Dietary pectic glycans are degraded by coordinated enzyme pathways in human colonic Bacteroides
journal, December 2017
- Luis, Ana S.; Briggs, Jonathon; Zhang, Xiaoyang
- Nature Microbiology, Vol. 3, Issue 2
An Examination of Diet for the Maintenance of Remission in Inflammatory Bowel Disease
journal, March 2017
- Haskey, Natasha; Gibson, Deanna
- Nutrients, Vol. 9, Issue 3
Glycan complexity dictates microbial resource allocation in the large intestine
journal, June 2015
- Rogowski, Artur; Briggs, Jonathon A.; Mortimer, Jennifer C.
- Nature Communications, Vol. 6, Issue 1
Starving our Microbial Self: The Deleterious Consequences of a Diet Deficient in Microbiota-Accessible Carbohydrates
journal, November 2014
- Sonnenburg, Erica D.; Sonnenburg, Justin L.
- Cell Metabolism, Vol. 20, Issue 5
Carbohydrate–Aromatic Interactions in Proteins
journal, November 2015
- Hudson, Kieran L.; Bartlett, Gail J.; Diehl, Roger C.
- Journal of the American Chemical Society, Vol. 137, Issue 48
Structure-Function Analysis of a Mixed-linkage β-Glucanase/Xyloglucanase from the Key Ruminal Bacteroidetes Prevotella bryantii B 1 4
journal, October 2015
- McGregor, Nicholas; Morar, Mariya; Fenger, Thomas Hauch
- Journal of Biological Chemistry, Vol. 291, Issue 3
A discrete genetic locus confers xyloglucan metabolism in select human gut Bacteroidetes
journal, January 2014
- Larsbrink, Johan; Rogers, Theresa E.; Hemsworth, Glyn R.
- Nature, Vol. 506, Issue 7489
An obesity-associated gut microbiome with increased capacity for energy harvest
journal, December 2006
- Turnbaugh, Peter J.; Ley, Ruth E.; Mahowald, Michael A.
- Nature, Vol. 444, Issue 7122
How glycan metabolism shapes the human gut microbiota
journal, April 2012
- Koropatkin, Nicole M.; Cameron, Elizabeth A.; Martens, Eric C.
- Nature Reviews Microbiology, Vol. 10, Issue 5
Recognition and Degradation of Plant Cell Wall Polysaccharides by Two Human Gut Symbionts
journal, December 2011
- Martens, Eric C.; Lowe, Elisabeth C.; Chiang, Herbert
- PLoS Biology, Vol. 9, Issue 12
Diet rapidly and reproducibly alters the human gut microbiome
journal, December 2013
- David, Lawrence A.; Maurice, Corinne F.; Carmody, Rachel N.
- Nature, Vol. 505, Issue 7484
Gut Fermentation of Dietary Fibres: Physico-Chemistry of Plant Cell Walls and Implications for Health
journal, October 2017
- Williams, Barbara; Grant, Lucas; Gidley, Michael
- International Journal of Molecular Sciences, Vol. 18, Issue 10
Structure of a SusD Homologue, BT1043, Involved in Mucin O -Glycan Utilization in a Prominent Human Gut Symbiont † , ‡
journal, February 2009
- Koropatkin, Nicole; Martens, Eric C.; Gordon, Jeffrey I.
- Biochemistry, Vol. 48, Issue 7
Dietary supplementation with β-glucan enriched oat bran increases faecal concentration of carboxylic acids in healthy subjects
journal, May 2007
- Nilsson, U.; Johansson, M.; Nilsson, Å
- European Journal of Clinical Nutrition, Vol. 62, Issue 8
Genetic Variation of the SusC/SusD Homologs from a Polysaccharide Utilization Locus Underlies Divergent Fructan Specificities and Functional Adaptation in Bacteroides thetaiotaomicron Strains
journal, May 2018
- Joglekar, Payal; Sonnenburg, Erica D.; Higginbottom, Steven K.
- mSphere, Vol. 3, Issue 3
Structural and functional characterization of NanU, a novel high-affinity sialic acid-inducible binding protein of oral and gut-dwelling Bacteroidetes species
journal, February 2014
- Phansopa, Chatchawal; Roy, Sumita; Rafferty, John B.
- Biochemical Journal, Vol. 458, Issue 3
A polysaccharide utilization locus from Flavobacterium johnsoniae enables conversion of recalcitrant chitin
journal, November 2016
- Larsbrink, Johan; Zhu, Yongtao; Kharade, Sampada S.
- Biotechnology for Biofuels, Vol. 9, Issue 1
Carbohydrate–Aromatic Interactions
journal, June 2012
- Asensio, Juan Luis; Ardá, Ana; Cañada, Francisco Javier
- Accounts of Chemical Research, Vol. 46, Issue 4
Cellulose degradation in the human gut: Ruminococcus champanellensis expands the cellulosome paradigm
journal, January 2016
- Cann, Isaac; Bernardi, Rafael C.; Mackie, Roderick I.
- Environmental Microbiology, Vol. 18, Issue 2
Addition of arabinoxylan and mixed linkage glucans in porcine diets affects the large intestinal bacterial populations
journal, July 2016
- Gorham, John B.; Kang, Seungha; Williams, Barbara A.
- European Journal of Nutrition, Vol. 56, Issue 6
Gut Microbiota from Twins Discordant for Obesity Modulate Metabolism in Mice
journal, September 2013
- Ridaura, V. K.; Faith, J. J.; Rey, F. E.
- Science, Vol. 341, Issue 6150
Advances in understanding the molecular basis of plant cell wall polysaccharide recognition by carbohydrate-binding modules
journal, October 2013
- Gilbert, Harry J.; Knox, J. Paul; Boraston, Alisdair B.
- Current Opinion in Structural Biology, Vol. 23, Issue 5
Role of (1,3)(1,4)-β-Glucan in Cell Walls: Interaction with Cellulose
journal, April 2014
- Kiemle, Sarah N.; Zhang, Xiao; Esker, Alan R.
- Biomacromolecules, Vol. 15, Issue 5
The microbiome and cancer: The microbiome and cancer
journal, March 2018
- Goodman, Brian; Gardner, Humphrey
- The Journal of Pathology, Vol. 244, Issue 5
Prenatal food insecurity post Hurricane Maria is associated with decreased Veillonella in the infant gut
journal, March 2020
- Wang, Leyao; de Ángel Solá, David; Acevedo Flores, Midnela
- Pediatric Research, Vol. 88, Issue 6
Cavin1 intrinsically disordered domains are essential for fuzzy electrostatic interactions and caveola formation
journal, February 2021
- Tillu, Vikas A.; Rae, James; Gao, Ya
- Nature Communications, Vol. 12, Issue 1
Dietary pectic glycans are degraded by coordinated enzyme pathways in human colonic Bacteroides.
text, January 2018
- Luis, Ana S.; Briggs, Jonathon; Zhang, Xiaoyang
- Apollo - University of Cambridge Repository
Decision-making in structure solution using Bayesian estimates of map quality: the PHENIX AutoSol wizard.
text, January 2009
- Terwilliger, Thomas C.; Adams, Paul D.; Read, Randy
- Apollo - University of Cambridge Repository
Overview of the CCP4 suite and current developments.
text, January 2011
- Winn, Martyn D.; Ballard, Charles C.; Cowtan, Kevin D.
- Apollo - University of Cambridge Repository
Molecular Mechanism by which Prominent Human Gut Bacteroidetes Utilize Mixed-Linkage Beta-Glucans, Major Health-Promoting Cereal Polysaccharides
journal, November 2017
- Tamura, Kazune; Hemsworth, Glyn R.; Déjean, Guillaume
- Cell Reports, Vol. 21, Issue 7
An Examination of Diet for the Maintenance of Remission in Inflammatory Bowel Disease
text, January 2019
- Haskey, Natasha; Gibson, Deanna L.
- Multidisciplinary Digital Publishing Institute
PHENIX: a comprehensive Python-based system for macromolecular structure solution.
text, January 2010
- Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor
- Apollo - University of Cambridge Repository
Molecular recognition of the beta-glucans laminarin and pustulan by a SusD-like glycan-binding protein of a marine Bacteroidetes
text, January 2018
- Mystkowska, Agata Anna; Robb, Craig; Vidal-Melgosa, Silvia
- Deutsches Elektronen-Synchrotron, DESY, Hamburg
Signal Peptidases
journal, February 2003
- Paetzel, Mark; Karla, Andrew; Strynadka, Natalie C. J.
- ChemInform, Vol. 34, Issue 6
Works referencing / citing this record:
Adaptation of Syntenic Xyloglucan Utilization Loci of Human Gut Bacteroidetes to Polysaccharide Side Chain Diversity
journal, August 2019
- Déjean, Guillaume; Tauzin, Alexandra S.; Bennett, Stuart W.
- Applied and Environmental Microbiology, Vol. 85, Issue 20