Mapping Molecular Recognition of β1,3-1,4-Glucans by a Surface Glycan-Binding Protein from the Human Gut Symbiont Bacteroides ovatus
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| Publication Date: | 2021 |
| Other Authors: | , , , , , , , , , , , , |
| Format: | Article |
| Language: | eng |
| Source: | Repositórios Científicos de Acesso Aberto de Portugal (RCAAP) |
| Download full: | http://hdl.handle.net/10362/128612 |
Summary: | contract DL-57/2016 WT108430/Z/15/Z WT218304/Z/19/Z 22-FY18-821 |
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Mapping Molecular Recognition of β1,3-1,4-Glucans by a Surface Glycan-Binding Protein from the Human Gut Symbiont Bacteroides ovatusβ-glucanBacteroides ovatucarbohydrate microarrayspolysaccharide utilization lociprotein-carbohydrate interactionsSusD-like proteinsX-ray crystallographySDG 3 - Good Health and Well-beingcontract DL-57/2016 WT108430/Z/15/Z WT218304/Z/19/Z 22-FY18-821A multigene polysaccharide utilization locus (PUL) encoding enzymes and surface carbohydrate (glycan)-binding proteins (SGBPs) was recently identified in prominent members of Bacteroidetes in the human gut and characterized in Bacteroides ovatus. This PUL-encoded system specifically targets mixed-linkage β1,3-1,4-glucans, a group of diet-derived carbohydrates that promote a healthy microbiota and have potential as prebiotics. The BoSGBPMLG-A protein encoded by the BACOVA_2743 gene is a SusD-like protein that plays a key role in the PUL's specificity and functionality. Here, we perform a detailed analysis of the molecular determinants underlying carbohydrate binding by BoSGBPMLG-A, combining carbohydrate microarray technology with quantitative affinity studies and a high-resolution X-ray crystallography structure of the complex of BoSGBPMLG-A with a β1,3-1,4-nonasaccharide. We demonstrate its unique binding specificity toward β1,3-1,4-gluco-oligosaccharides, with increasing binding affinities up to the octasaccharide and dependency on the number and position of β1,3 linkages. The interaction is defined by a 41-Å-long extended binding site that accommodates the oligosaccharide in a mode distinct from that of previously described bacterial β1,3-1,4-glucan-binding proteins. In addition to the shape complementarity mediated by CH-π interactions, a complex hydrogen bonding network complemented by a high number of key ordered water molecules establishes additional specific interactions with the oligosaccharide. These support the twisted conformation of the β-glucan backbone imposed by the β1,3 linkages and explain the dependency on the oligosaccharide chain length. We propose that the specificity of the PUL conferred by BoSGBPMLG-A to import long β1,3-1,4-glucan oligosaccharides to the bacterial periplasm allows Bacteroidetes to outcompete bacteria that lack this PUL for utilization of β1,3-1,4-glucans. IMPORTANCE With the knowledge of bacterial gene systems encoding proteins that target dietary carbohydrates as a source of nutrients and their importance for human health, major efforts are being made to understand carbohydrate recognition by various commensal bacteria. Here, we describe an integrative strategy that combines carbohydrate microarray technology with structural studies to further elucidate the molecular determinants of carbohydrate recognition by BoSGBPMLG-A, a key protein expressed at the surface of Bacteroides ovatus for utilization of mixed-linkage β1,3-1,4-glucans. We have mapped at high resolution interactions that occur at the binding site of BoSGBPMLG-A and provide evidence for the role of key water-mediated interactions for fine specificity and affinity. Understanding at the molecular level how commensal bacteria, such as prominent members of Bacteroidetes, can differentially utilize dietary carbohydrates with potential prebiotic activities will shed light on possible ways to modulate the microbiome to promote human health.UCIBIO - Applied Molecular Biosciences UnitDQ - Departamento de QuímicaRUNCorreia, Viviana G.Trovão, FilipaPinheiro, Benedita A.Brás, Joana L. A.Silva, Lisete M.Nunes, CláudiaCoimbra, Manuel A.Liu, YanFeizi, TenFontes, Carlos M. G. A.Mulloy, BarbaraChai, WengangCarvalho, Ana LuísaPalma, Angelina S.2021-12-02T23:47:45Z2021-11-242021-11-24T00:00:00Zinfo:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articleapplication/pdfhttp://hdl.handle.net/10362/128612eng2165-0497PURE: 35125874https://doi.org/10.1128/Spectrum.01826-21info:eu-repo/semantics/openAccessreponame:Repositórios Científicos de Acesso Aberto de Portugal (RCAAP)instname:FCCN, serviços digitais da FCT – Fundação para a Ciência e a Tecnologiainstacron:RCAAP2024-05-22T17:57:24Zoai:run.unl.pt:10362/128612Portal AgregadorONGhttps://www.rcaap.pt/oai/openaireinfo@rcaap.ptopendoar:https://opendoar.ac.uk/repository/71602025-05-28T17:28:20.422217Repositórios Científicos de Acesso Aberto de Portugal (RCAAP) - FCCN, serviços digitais da FCT – Fundação para a Ciência e a Tecnologiafalse |
| dc.title.none.fl_str_mv |
Mapping Molecular Recognition of β1,3-1,4-Glucans by a Surface Glycan-Binding Protein from the Human Gut Symbiont Bacteroides ovatus |
| title |
Mapping Molecular Recognition of β1,3-1,4-Glucans by a Surface Glycan-Binding Protein from the Human Gut Symbiont Bacteroides ovatus |
| spellingShingle |
Mapping Molecular Recognition of β1,3-1,4-Glucans by a Surface Glycan-Binding Protein from the Human Gut Symbiont Bacteroides ovatus Correia, Viviana G. β-glucan Bacteroides ovatu carbohydrate microarrays polysaccharide utilization loci protein-carbohydrate interactions SusD-like proteins X-ray crystallography SDG 3 - Good Health and Well-being |
| title_short |
Mapping Molecular Recognition of β1,3-1,4-Glucans by a Surface Glycan-Binding Protein from the Human Gut Symbiont Bacteroides ovatus |
| title_full |
Mapping Molecular Recognition of β1,3-1,4-Glucans by a Surface Glycan-Binding Protein from the Human Gut Symbiont Bacteroides ovatus |
| title_fullStr |
Mapping Molecular Recognition of β1,3-1,4-Glucans by a Surface Glycan-Binding Protein from the Human Gut Symbiont Bacteroides ovatus |
| title_full_unstemmed |
Mapping Molecular Recognition of β1,3-1,4-Glucans by a Surface Glycan-Binding Protein from the Human Gut Symbiont Bacteroides ovatus |
| title_sort |
Mapping Molecular Recognition of β1,3-1,4-Glucans by a Surface Glycan-Binding Protein from the Human Gut Symbiont Bacteroides ovatus |
| author |
Correia, Viviana G. |
| author_facet |
Correia, Viviana G. Trovão, Filipa Pinheiro, Benedita A. Brás, Joana L. A. Silva, Lisete M. Nunes, Cláudia Coimbra, Manuel A. Liu, Yan Feizi, Ten Fontes, Carlos M. G. A. Mulloy, Barbara Chai, Wengang Carvalho, Ana Luísa Palma, Angelina S. |
| author_role |
author |
| author2 |
Trovão, Filipa Pinheiro, Benedita A. Brás, Joana L. A. Silva, Lisete M. Nunes, Cláudia Coimbra, Manuel A. Liu, Yan Feizi, Ten Fontes, Carlos M. G. A. Mulloy, Barbara Chai, Wengang Carvalho, Ana Luísa Palma, Angelina S. |
| author2_role |
author author author author author author author author author author author author author |
| dc.contributor.none.fl_str_mv |
UCIBIO - Applied Molecular Biosciences Unit DQ - Departamento de Química RUN |
| dc.contributor.author.fl_str_mv |
Correia, Viviana G. Trovão, Filipa Pinheiro, Benedita A. Brás, Joana L. A. Silva, Lisete M. Nunes, Cláudia Coimbra, Manuel A. Liu, Yan Feizi, Ten Fontes, Carlos M. G. A. Mulloy, Barbara Chai, Wengang Carvalho, Ana Luísa Palma, Angelina S. |
| dc.subject.por.fl_str_mv |
β-glucan Bacteroides ovatu carbohydrate microarrays polysaccharide utilization loci protein-carbohydrate interactions SusD-like proteins X-ray crystallography SDG 3 - Good Health and Well-being |
| topic |
β-glucan Bacteroides ovatu carbohydrate microarrays polysaccharide utilization loci protein-carbohydrate interactions SusD-like proteins X-ray crystallography SDG 3 - Good Health and Well-being |
| description |
contract DL-57/2016 WT108430/Z/15/Z WT218304/Z/19/Z 22-FY18-821 |
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2021 |
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2021-12-02T23:47:45Z 2021-11-24 2021-11-24T00:00:00Z |
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info:eu-repo/semantics/publishedVersion |
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info:eu-repo/semantics/article |
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http://hdl.handle.net/10362/128612 |
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eng |
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eng |
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2165-0497 PURE: 35125874 https://doi.org/10.1128/Spectrum.01826-21 |
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