Mechanistic insights into glycoside 3-oxidases involved in C-glycoside metabolism in soil microorganisms

Bibliographic Details
Main Author: Taborda, André
Publication Date: 2023
Other Authors: Frazão, Tomás, Rodrigues, Miguel V., Fernández-Luengo, Xavier, Sancho, Ferran, Lucas, Maria Fátima, Frazão, Carlos, Melo, Eduardo P., Ventura, M. Rita, Masgrau, Laura, Borges, Patrícia T., Martins, Lígia O.
Format: Article
Language: eng
Source: Repositórios Científicos de Acesso Aberto de Portugal (RCAAP)
Download full: http://hdl.handle.net/10362/165733
Summary: Funding Information: We thank Diana Santos for preliminary data, Teresa Catarino with stopped-flow analysis, Tiago N. Cordeiro for help with Rosetta, Philippe Carpentier for support with krypton high-pressure experiments, Pedro Matias and Maximino Manzanera for valuable discussions. We thank the beamline staff at ESRF (Grenoble, France) and ALBA (Barcelona, Spain) for their support during the synchrotron data collection and Teresa Silva and Cristina Timóteo (Research Facilities, ITQB-NOVA) for technical assistance. The NMR data were acquired at CERMAX, ITQB-NOVA, Oeiras, Portugal, with equipment funded by FCT, project AAC 01/SAICT/2016. This work was supported by the Fundação para a Ciência e Tecnologia, Portugal, grants, 2022.02027.PTDC (L.O.M.), MOSTMICRO-ITQB (UIDB/04612/2020 and UIDP/04612/2020) (L.O.M. and M.R.V.), LS4FUTURE Associated Laboratory (LA/P/0087/2020) (L.O.M. and M.R.V.), PTDC/BII-BBF/29564/2017 (L.O.M.), UIDB/04326/2020, UIDP/043226/2020 and LA/P/0101/2020 (EPM) and FCT PhD fellowships 2020.07928 (A.T.), 2022.13872 (T.F.), and 2022.09426 (M.V.R.). B-Ligzymes (GA 824017) from the European Union’s Horizon 2020 Research and Innovation Program is also acknowledged for funding T.F. secondment at Zymvol and F.S. secondment at ITQB NOVA. L.M. and X.F.L. acknowledge PID2021-126897NB-I00 project and PRE2019-088412 fellowship, funded by MCIN/AEI/10.13039/501100011033/ FEDER, EU. Funding Information: We thank Diana Santos for preliminary data, Teresa Catarino with stopped-flow analysis, Tiago N. Cordeiro for help with Rosetta, Philippe Carpentier for support with krypton high-pressure experiments, Pedro Matias and Maximino Manzanera for valuable discussions. We thank the beamline staff at ESRF (Grenoble, France) and ALBA (Barcelona, Spain) for their support during the synchrotron data collection and Teresa Silva and Cristina Timóteo (Research Facilities, ITQB-NOVA) for technical assistance. The NMR data were acquired at CERMAX, ITQB-NOVA, Oeiras, Portugal, with equipment funded by FCT, project AAC 01/SAICT/2016. This work was supported by the Fundação para a Ciência e Tecnologia, Portugal, grants, 2022.02027.PTDC (L.O.M.), MOSTMICRO-ITQB (UIDB/04612/2020 and UIDP/04612/2020) (L.O.M. and M.R.V.), LS4FUTURE Associated Laboratory (LA/P/0087/2020) (L.O.M. and M.R.V.), PTDC/BII-BBF/29564/2017 (L.O.M.), UIDB/04326/2020, UIDP/043226/2020 and LA/P/0101/2020 (EPM) and FCT PhD fellowships 2020.07928 (A.T.), 2022.13872 (T.F.), and 2022.09426 (M.V.R.). B-Ligzymes (GA 824017) from the European Union’s Horizon 2020 Research and Innovation Program is also acknowledged for funding T.F. secondment at Zymvol and F.S. secondment at ITQB NOVA. L.M. and X.F.L. acknowledge PID2021-126897NB-I00 project and PRE2019-088412 fellowship, funded by MCIN/AEI/10.13039/501100011033/ FEDER, EU. Publisher Copyright: © 2023, The Author(s).
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spelling Mechanistic insights into glycoside 3-oxidases involved in C-glycoside metabolism in soil microorganismsChemistry(all)Biochemistry, Genetics and Molecular Biology(all)Physics and Astronomy(all)Funding Information: We thank Diana Santos for preliminary data, Teresa Catarino with stopped-flow analysis, Tiago N. Cordeiro for help with Rosetta, Philippe Carpentier for support with krypton high-pressure experiments, Pedro Matias and Maximino Manzanera for valuable discussions. We thank the beamline staff at ESRF (Grenoble, France) and ALBA (Barcelona, Spain) for their support during the synchrotron data collection and Teresa Silva and Cristina Timóteo (Research Facilities, ITQB-NOVA) for technical assistance. The NMR data were acquired at CERMAX, ITQB-NOVA, Oeiras, Portugal, with equipment funded by FCT, project AAC 01/SAICT/2016. This work was supported by the Fundação para a Ciência e Tecnologia, Portugal, grants, 2022.02027.PTDC (L.O.M.), MOSTMICRO-ITQB (UIDB/04612/2020 and UIDP/04612/2020) (L.O.M. and M.R.V.), LS4FUTURE Associated Laboratory (LA/P/0087/2020) (L.O.M. and M.R.V.), PTDC/BII-BBF/29564/2017 (L.O.M.), UIDB/04326/2020, UIDP/043226/2020 and LA/P/0101/2020 (EPM) and FCT PhD fellowships 2020.07928 (A.T.), 2022.13872 (T.F.), and 2022.09426 (M.V.R.). B-Ligzymes (GA 824017) from the European Union’s Horizon 2020 Research and Innovation Program is also acknowledged for funding T.F. secondment at Zymvol and F.S. secondment at ITQB NOVA. L.M. and X.F.L. acknowledge PID2021-126897NB-I00 project and PRE2019-088412 fellowship, funded by MCIN/AEI/10.13039/501100011033/ FEDER, EU. Funding Information: We thank Diana Santos for preliminary data, Teresa Catarino with stopped-flow analysis, Tiago N. Cordeiro for help with Rosetta, Philippe Carpentier for support with krypton high-pressure experiments, Pedro Matias and Maximino Manzanera for valuable discussions. We thank the beamline staff at ESRF (Grenoble, France) and ALBA (Barcelona, Spain) for their support during the synchrotron data collection and Teresa Silva and Cristina Timóteo (Research Facilities, ITQB-NOVA) for technical assistance. The NMR data were acquired at CERMAX, ITQB-NOVA, Oeiras, Portugal, with equipment funded by FCT, project AAC 01/SAICT/2016. This work was supported by the Fundação para a Ciência e Tecnologia, Portugal, grants, 2022.02027.PTDC (L.O.M.), MOSTMICRO-ITQB (UIDB/04612/2020 and UIDP/04612/2020) (L.O.M. and M.R.V.), LS4FUTURE Associated Laboratory (LA/P/0087/2020) (L.O.M. and M.R.V.), PTDC/BII-BBF/29564/2017 (L.O.M.), UIDB/04326/2020, UIDP/043226/2020 and LA/P/0101/2020 (EPM) and FCT PhD fellowships 2020.07928 (A.T.), 2022.13872 (T.F.), and 2022.09426 (M.V.R.). B-Ligzymes (GA 824017) from the European Union’s Horizon 2020 Research and Innovation Program is also acknowledged for funding T.F. secondment at Zymvol and F.S. secondment at ITQB NOVA. L.M. and X.F.L. acknowledge PID2021-126897NB-I00 project and PRE2019-088412 fellowship, funded by MCIN/AEI/10.13039/501100011033/ FEDER, EU. Publisher Copyright: © 2023, The Author(s).C-glycosides are natural products with important biological activities but are recalcitrant to degradation. Glycoside 3-oxidases (G3Oxs) are recently identified bacterial flavo-oxidases from the glucose-methanol-coline (GMC) superfamily that catalyze the oxidation of C-glycosides with the concomitant reduction of O2 to H2O2. This oxidation is followed by C-C acid/base-assisted bond cleavage in two-step C-deglycosylation pathways. Soil and gut microorganisms have different oxidative enzymes, but the details of their catalytic mechanisms are largely unknown. Here, we report that PsG3Ox oxidizes at 50,000-fold higher specificity (k cat/Km) the glucose moiety of mangiferin to 3-keto-mangiferin than free D-glucose to 2-keto-glucose. Analysis of PsG3Ox X-ray crystal structures and PsG3Ox in complex with glucose and mangiferin, combined with mutagenesis and molecular dynamics simulations, reveal distinctive features in the topology surrounding the active site that favor catalytically competent conformational states suitable for recognition, stabilization, and oxidation of the glucose moiety of mangiferin. Furthermore, their distinction to pyranose 2-oxidases (P2Oxs) involved in wood decay and recycling is discussed from an evolutionary, structural, and functional viewpoint.Instituto de Tecnologia Química e Biológica António Xavier (ITQB)RUNTaborda, AndréFrazão, TomásRodrigues, Miguel V.Fernández-Luengo, XavierSancho, FerranLucas, Maria FátimaFrazão, CarlosMelo, Eduardo P.Ventura, M. RitaMasgrau, LauraBorges, Patrícia T.Martins, Lígia O.2024-04-02T23:47:37Z2023-122023-12-01T00:00:00Zinfo:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articleapplication/pdfhttp://hdl.handle.net/10362/165733eng2041-1723PURE: 83670875https://doi.org/10.1038/s41467-023-42000-3info: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:RCAAP2024-05-22T18:20:08Zoai:run.unl.pt:10362/165733Portal AgregadorONGhttps://www.rcaap.pt/oai/openaireinfo@rcaap.ptopendoar:https://opendoar.ac.uk/repository/71602025-05-28T17:50:52.877295Repositórios 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 Mechanistic insights into glycoside 3-oxidases involved in C-glycoside metabolism in soil microorganisms
title Mechanistic insights into glycoside 3-oxidases involved in C-glycoside metabolism in soil microorganisms
spellingShingle Mechanistic insights into glycoside 3-oxidases involved in C-glycoside metabolism in soil microorganisms
Taborda, André
Chemistry(all)
Biochemistry, Genetics and Molecular Biology(all)
Physics and Astronomy(all)
title_short Mechanistic insights into glycoside 3-oxidases involved in C-glycoside metabolism in soil microorganisms
title_full Mechanistic insights into glycoside 3-oxidases involved in C-glycoside metabolism in soil microorganisms
title_fullStr Mechanistic insights into glycoside 3-oxidases involved in C-glycoside metabolism in soil microorganisms
title_full_unstemmed Mechanistic insights into glycoside 3-oxidases involved in C-glycoside metabolism in soil microorganisms
title_sort Mechanistic insights into glycoside 3-oxidases involved in C-glycoside metabolism in soil microorganisms
author Taborda, André
author_facet Taborda, André
Frazão, Tomás
Rodrigues, Miguel V.
Fernández-Luengo, Xavier
Sancho, Ferran
Lucas, Maria Fátima
Frazão, Carlos
Melo, Eduardo P.
Ventura, M. Rita
Masgrau, Laura
Borges, Patrícia T.
Martins, Lígia O.
author_role author
author2 Frazão, Tomás
Rodrigues, Miguel V.
Fernández-Luengo, Xavier
Sancho, Ferran
Lucas, Maria Fátima
Frazão, Carlos
Melo, Eduardo P.
Ventura, M. Rita
Masgrau, Laura
Borges, Patrícia T.
Martins, Lígia O.
author2_role author
author
author
author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Instituto de Tecnologia Química e Biológica António Xavier (ITQB)
RUN
dc.contributor.author.fl_str_mv Taborda, André
Frazão, Tomás
Rodrigues, Miguel V.
Fernández-Luengo, Xavier
Sancho, Ferran
Lucas, Maria Fátima
Frazão, Carlos
Melo, Eduardo P.
Ventura, M. Rita
Masgrau, Laura
Borges, Patrícia T.
Martins, Lígia O.
dc.subject.por.fl_str_mv Chemistry(all)
Biochemistry, Genetics and Molecular Biology(all)
Physics and Astronomy(all)
topic Chemistry(all)
Biochemistry, Genetics and Molecular Biology(all)
Physics and Astronomy(all)
description Funding Information: We thank Diana Santos for preliminary data, Teresa Catarino with stopped-flow analysis, Tiago N. Cordeiro for help with Rosetta, Philippe Carpentier for support with krypton high-pressure experiments, Pedro Matias and Maximino Manzanera for valuable discussions. We thank the beamline staff at ESRF (Grenoble, France) and ALBA (Barcelona, Spain) for their support during the synchrotron data collection and Teresa Silva and Cristina Timóteo (Research Facilities, ITQB-NOVA) for technical assistance. The NMR data were acquired at CERMAX, ITQB-NOVA, Oeiras, Portugal, with equipment funded by FCT, project AAC 01/SAICT/2016. This work was supported by the Fundação para a Ciência e Tecnologia, Portugal, grants, 2022.02027.PTDC (L.O.M.), MOSTMICRO-ITQB (UIDB/04612/2020 and UIDP/04612/2020) (L.O.M. and M.R.V.), LS4FUTURE Associated Laboratory (LA/P/0087/2020) (L.O.M. and M.R.V.), PTDC/BII-BBF/29564/2017 (L.O.M.), UIDB/04326/2020, UIDP/043226/2020 and LA/P/0101/2020 (EPM) and FCT PhD fellowships 2020.07928 (A.T.), 2022.13872 (T.F.), and 2022.09426 (M.V.R.). B-Ligzymes (GA 824017) from the European Union’s Horizon 2020 Research and Innovation Program is also acknowledged for funding T.F. secondment at Zymvol and F.S. secondment at ITQB NOVA. L.M. and X.F.L. acknowledge PID2021-126897NB-I00 project and PRE2019-088412 fellowship, funded by MCIN/AEI/10.13039/501100011033/ FEDER, EU. Funding Information: We thank Diana Santos for preliminary data, Teresa Catarino with stopped-flow analysis, Tiago N. Cordeiro for help with Rosetta, Philippe Carpentier for support with krypton high-pressure experiments, Pedro Matias and Maximino Manzanera for valuable discussions. We thank the beamline staff at ESRF (Grenoble, France) and ALBA (Barcelona, Spain) for their support during the synchrotron data collection and Teresa Silva and Cristina Timóteo (Research Facilities, ITQB-NOVA) for technical assistance. The NMR data were acquired at CERMAX, ITQB-NOVA, Oeiras, Portugal, with equipment funded by FCT, project AAC 01/SAICT/2016. This work was supported by the Fundação para a Ciência e Tecnologia, Portugal, grants, 2022.02027.PTDC (L.O.M.), MOSTMICRO-ITQB (UIDB/04612/2020 and UIDP/04612/2020) (L.O.M. and M.R.V.), LS4FUTURE Associated Laboratory (LA/P/0087/2020) (L.O.M. and M.R.V.), PTDC/BII-BBF/29564/2017 (L.O.M.), UIDB/04326/2020, UIDP/043226/2020 and LA/P/0101/2020 (EPM) and FCT PhD fellowships 2020.07928 (A.T.), 2022.13872 (T.F.), and 2022.09426 (M.V.R.). B-Ligzymes (GA 824017) from the European Union’s Horizon 2020 Research and Innovation Program is also acknowledged for funding T.F. secondment at Zymvol and F.S. secondment at ITQB NOVA. L.M. and X.F.L. acknowledge PID2021-126897NB-I00 project and PRE2019-088412 fellowship, funded by MCIN/AEI/10.13039/501100011033/ FEDER, EU. Publisher Copyright: © 2023, The Author(s).
publishDate 2023
dc.date.none.fl_str_mv 2023-12
2023-12-01T00:00:00Z
2024-04-02T23:47:37Z
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