The structure of a Bacteroides thetaiotaomicron carbohydrate-binding module provides new insight into the recognition of complex pectic polysaccharides by the human microbiome

Detalhes bibliográficos
Autor(a) principal: Trovão, Filipa
Data de Publicação: 2023
Outros Autores: Correia, Viviana G., Lourenço, Frederico M., Ribeiro, Diana O., Carvalho, Ana Luísa, Palma, Angelina S., Pinheiro, Benedita A.
Tipo de documento: Artigo
Idioma: eng
Título da fonte: Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)
Texto Completo: http://hdl.handle.net/10362/152341
Resumo: Funding Information: We thank Prof. Carlos Fontes and Dr Joana Bras (NZYTech, Portugal) for their assistance in obtaining the initial BT0996-C clone. We are grateful to Prof Ten Feizi, Dr Yan Liu and Dr Lisete Silva from the Glycosciences Laboratory (Imperial College London, UK) for their support and assistance on robotic microarray printing. This work was supported by the FCT - Fundação para a Ciência e a Tecnologia, I.P., through the DL-57/2016 Program Contract (BP). This work is financed by national funds from FCT - Fundação para a Ciência e a Tecnologia, I.P., in the scope of the project LA/P/0140/2020 of the Associate Laboratory Institute for Health and Bioeconomy - i4HB. The authors acknowledge the European Synchrotron Radiation Facility (Grenoble, France) and ALBA (Barcelona, Spain) for access to beamlines ID30B and BL-13 XALOC, respectively. Publisher Copyright: © 2022
id RCAP_55f58486bf145473a772098138066256
oai_identifier_str oai:run.unl.pt:10362/152341
network_acronym_str RCAP
network_name_str Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)
repository_id_str 7160
spelling The structure of a Bacteroides thetaiotaomicron carbohydrate-binding module provides new insight into the recognition of complex pectic polysaccharides by the human microbiomeBacteroides thetaiotaomicronCarbohydrate binding moduleCarbohydratesHuman gut microbiotaRhamnogalacturonan IIStructural BiologyFunding Information: We thank Prof. Carlos Fontes and Dr Joana Bras (NZYTech, Portugal) for their assistance in obtaining the initial BT0996-C clone. We are grateful to Prof Ten Feizi, Dr Yan Liu and Dr Lisete Silva from the Glycosciences Laboratory (Imperial College London, UK) for their support and assistance on robotic microarray printing. This work was supported by the FCT - Fundação para a Ciência e a Tecnologia, I.P., through the DL-57/2016 Program Contract (BP). This work is financed by national funds from FCT - Fundação para a Ciência e a Tecnologia, I.P., in the scope of the project LA/P/0140/2020 of the Associate Laboratory Institute for Health and Bioeconomy - i4HB. The authors acknowledge the European Synchrotron Radiation Facility (Grenoble, France) and ALBA (Barcelona, Spain) for access to beamlines ID30B and BL-13 XALOC, respectively. Publisher Copyright: © 2022The Bacteroides thetaiotaomicron has developed a consortium of enzymes capable of overcoming steric constraints and degrading, in a sequential manner, the complex rhamnogalacturonan II (RG-II) polysaccharide. BT0996 protein acts in the initial stages of the RG-II depolymerisation, where its two catalytic modules remove the terminal monosaccharides from RG-II side chains A and B. BT0996 is modular and has three putative carbohydrate-binding modules (CBMs) for which the roles in the RG-II degradation are unknown. Here, we present the characterisation of the module at the C-terminal domain, which we designated BT0996-C. The high-resolution structure obtained by X-ray crystallography reveals that the protein displays a typical β-sandwich fold with structural similarity to CBMs assigned to families 6 and 35. The distinctive features are: 1) the presence of several charged residues at the BT0996-C surface creating a large, broad positive lysine-rich patch that encompasses the putative binding site; and 2) the absence of the highly conserved binding-site signatures observed in CBMs from families 6 and 35, such as region A tryptophan and region C asparagine. These findings hint at a binding mode of BT0996-C not yet observed in its homologues. In line with this, carbohydrate microarrays and microscale thermophoresis show the ability of BT0996-C to bind α1-4-linked polygalacturonic acid, and that electrostatic interactions are essential for the recognition of the anionic polysaccharide. The results support the hypothesis that BT0996-C may have evolved to potentiate the action of BT0996 catalytic modules on the complex structure of RG-II by binding to the polygalacturonic acid backbone sequence.UCIBIO - Applied Molecular Biosciences UnitDQ - Departamento de QuímicaRUNTrovão, FilipaCorreia, Viviana G.Lourenço, Frederico M.Ribeiro, Diana O.Carvalho, Ana LuísaPalma, Angelina S.Pinheiro, Benedita A.2023-05-02T22:10:55Z20232023-01-01T00:00:00Zinfo:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/article10application/pdfhttp://hdl.handle.net/10362/152341eng2590-1524PURE: 52152582https://doi.org/10.1016/j.yjsbx.2022.100084info:eu-repo/semantics/openAccessreponame:Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)instname:Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informaçãoinstacron:RCAAP2024-03-11T05:34:39Zoai:run.unl.pt:10362/152341Portal AgregadorONGhttps://www.rcaap.pt/oai/openaireopendoar:71602024-03-20T03:54:52.062074Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) - Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informaçãofalse
dc.title.none.fl_str_mv The structure of a Bacteroides thetaiotaomicron carbohydrate-binding module provides new insight into the recognition of complex pectic polysaccharides by the human microbiome
title The structure of a Bacteroides thetaiotaomicron carbohydrate-binding module provides new insight into the recognition of complex pectic polysaccharides by the human microbiome
spellingShingle The structure of a Bacteroides thetaiotaomicron carbohydrate-binding module provides new insight into the recognition of complex pectic polysaccharides by the human microbiome
Trovão, Filipa
Bacteroides thetaiotaomicron
Carbohydrate binding module
Carbohydrates
Human gut microbiota
Rhamnogalacturonan II
Structural Biology
title_short The structure of a Bacteroides thetaiotaomicron carbohydrate-binding module provides new insight into the recognition of complex pectic polysaccharides by the human microbiome
title_full The structure of a Bacteroides thetaiotaomicron carbohydrate-binding module provides new insight into the recognition of complex pectic polysaccharides by the human microbiome
title_fullStr The structure of a Bacteroides thetaiotaomicron carbohydrate-binding module provides new insight into the recognition of complex pectic polysaccharides by the human microbiome
title_full_unstemmed The structure of a Bacteroides thetaiotaomicron carbohydrate-binding module provides new insight into the recognition of complex pectic polysaccharides by the human microbiome
title_sort The structure of a Bacteroides thetaiotaomicron carbohydrate-binding module provides new insight into the recognition of complex pectic polysaccharides by the human microbiome
author Trovão, Filipa
author_facet Trovão, Filipa
Correia, Viviana G.
Lourenço, Frederico M.
Ribeiro, Diana O.
Carvalho, Ana Luísa
Palma, Angelina S.
Pinheiro, Benedita A.
author_role author
author2 Correia, Viviana G.
Lourenço, Frederico M.
Ribeiro, Diana O.
Carvalho, Ana Luísa
Palma, Angelina S.
Pinheiro, Benedita A.
author2_role 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 Trovão, Filipa
Correia, Viviana G.
Lourenço, Frederico M.
Ribeiro, Diana O.
Carvalho, Ana Luísa
Palma, Angelina S.
Pinheiro, Benedita A.
dc.subject.por.fl_str_mv Bacteroides thetaiotaomicron
Carbohydrate binding module
Carbohydrates
Human gut microbiota
Rhamnogalacturonan II
Structural Biology
topic Bacteroides thetaiotaomicron
Carbohydrate binding module
Carbohydrates
Human gut microbiota
Rhamnogalacturonan II
Structural Biology
description Funding Information: We thank Prof. Carlos Fontes and Dr Joana Bras (NZYTech, Portugal) for their assistance in obtaining the initial BT0996-C clone. We are grateful to Prof Ten Feizi, Dr Yan Liu and Dr Lisete Silva from the Glycosciences Laboratory (Imperial College London, UK) for their support and assistance on robotic microarray printing. This work was supported by the FCT - Fundação para a Ciência e a Tecnologia, I.P., through the DL-57/2016 Program Contract (BP). This work is financed by national funds from FCT - Fundação para a Ciência e a Tecnologia, I.P., in the scope of the project LA/P/0140/2020 of the Associate Laboratory Institute for Health and Bioeconomy - i4HB. The authors acknowledge the European Synchrotron Radiation Facility (Grenoble, France) and ALBA (Barcelona, Spain) for access to beamlines ID30B and BL-13 XALOC, respectively. Publisher Copyright: © 2022
publishDate 2023
dc.date.none.fl_str_mv 2023-05-02T22:10:55Z
2023
2023-01-01T00:00:00Z
dc.type.status.fl_str_mv info:eu-repo/semantics/publishedVersion
dc.type.driver.fl_str_mv info:eu-repo/semantics/article
format article
status_str publishedVersion
dc.identifier.uri.fl_str_mv http://hdl.handle.net/10362/152341
url http://hdl.handle.net/10362/152341
dc.language.iso.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv 2590-1524
PURE: 52152582
https://doi.org/10.1016/j.yjsbx.2022.100084
dc.rights.driver.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv 10
application/pdf
dc.source.none.fl_str_mv reponame:Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)
instname:Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação
instacron:RCAAP
instname_str Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação
instacron_str RCAAP
institution RCAAP
reponame_str Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)
collection Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)
repository.name.fl_str_mv Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) - Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação
repository.mail.fl_str_mv
_version_ 1799138136665620480

Registros relacionados