Structure–function characterization of two enzymes from novel subfamilies of manganese peroxidases secreted by the lignocellulose-degrading Agaricales fungi Agrocybe pediades and Cyathus striatus

21 p.-7 fig.-3 tab.

Detalles Bibliográficos
Autores: Sánchez-Ruiz, María I., Santillana, Elena, Linde, Dolores, Romero, Antonio, Martínez, Ángel T., Ruiz-Dueñas, F. J.
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2024
País:España
Institución:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/381932
Acceso en línea:http://hdl.handle.net/10261/381932
Access Level:acceso abierto
Palabra clave:Agrocybe pediades
Cyathus striatus
Agaricales fungi
Lignin
Manganese peroxidase
Novel enzymatic subfamilies
Enzyme catalysis
Crystal structure
Manganese oxidation site
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oai_identifier_str oai:digital.csic.es:10261/381932
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network_name_str España
repository_id_str
dc.title.none.fl_str_mv Structure–function characterization of two enzymes from novel subfamilies of manganese peroxidases secreted by the lignocellulose-degrading Agaricales fungi Agrocybe pediades and Cyathus striatus
title Structure–function characterization of two enzymes from novel subfamilies of manganese peroxidases secreted by the lignocellulose-degrading Agaricales fungi Agrocybe pediades and Cyathus striatus
spellingShingle Structure–function characterization of two enzymes from novel subfamilies of manganese peroxidases secreted by the lignocellulose-degrading Agaricales fungi Agrocybe pediades and Cyathus striatus
Sánchez-Ruiz, María I.
Agrocybe pediades
Cyathus striatus
Agaricales fungi
Lignin
Manganese peroxidase
Novel enzymatic subfamilies
Enzyme catalysis
Crystal structure
Manganese oxidation site
title_short Structure–function characterization of two enzymes from novel subfamilies of manganese peroxidases secreted by the lignocellulose-degrading Agaricales fungi Agrocybe pediades and Cyathus striatus
title_full Structure–function characterization of two enzymes from novel subfamilies of manganese peroxidases secreted by the lignocellulose-degrading Agaricales fungi Agrocybe pediades and Cyathus striatus
title_fullStr Structure–function characterization of two enzymes from novel subfamilies of manganese peroxidases secreted by the lignocellulose-degrading Agaricales fungi Agrocybe pediades and Cyathus striatus
title_full_unstemmed Structure–function characterization of two enzymes from novel subfamilies of manganese peroxidases secreted by the lignocellulose-degrading Agaricales fungi Agrocybe pediades and Cyathus striatus
title_sort Structure–function characterization of two enzymes from novel subfamilies of manganese peroxidases secreted by the lignocellulose-degrading Agaricales fungi Agrocybe pediades and Cyathus striatus
dc.creator.none.fl_str_mv Sánchez-Ruiz, María I.
Santillana, Elena
Linde, Dolores
Romero, Antonio
Martínez, Ángel T.
Ruiz-Dueñas, F. J.
author Sánchez-Ruiz, María I.
author_facet Sánchez-Ruiz, María I.
Santillana, Elena
Linde, Dolores
Romero, Antonio
Martínez, Ángel T.
Ruiz-Dueñas, F. J.
author_role author
author2 Santillana, Elena
Linde, Dolores
Romero, Antonio
Martínez, Ángel T.
Ruiz-Dueñas, F. J.
author2_role author
author
author
author
author
dc.contributor.none.fl_str_mv Consejo Superior de Investigaciones Científicas (España)
Ministerio de Ciencia, Innovación y Universidades (España)
Santillana, Elena [0000-0002-6227-1725]
Linde, Dolores [0000-0002-0359-0566]
Romero, Antonio [0000-0002-6990-6973]
Martínez, Ángel T. [0000-0002-1584-2863]
Ruiz-Dueñas, F. J. [0000-0002-9837-5665]
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv Agrocybe pediades
Cyathus striatus
Agaricales fungi
Lignin
Manganese peroxidase
Novel enzymatic subfamilies
Enzyme catalysis
Crystal structure
Manganese oxidation site
topic Agrocybe pediades
Cyathus striatus
Agaricales fungi
Lignin
Manganese peroxidase
Novel enzymatic subfamilies
Enzyme catalysis
Crystal structure
Manganese oxidation site
description 21 p.-7 fig.-3 tab.
publishDate 2024
dc.date.none.fl_str_mv 2024
2025
2025
dc.type.none.fl_str_mv info:eu-repo/semantics/article
http://purl.org/coar/resource_type/c_6501
Publisher's version
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/381932
url http://hdl.handle.net/10261/381932
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv #PLACEHOLDER_PARENT_METADATA_VALUE#
#PLACEHOLDER_PARENT_METADATA_VALUE#
info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016/BIO2017-86559-R
info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2021-2023/PID2021-126384OB-I00
https://doi.org/10.1186/s13068-024-02517-1
Sí
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.publisher.none.fl_str_mv BioMed Central
publisher.none.fl_str_mv BioMed Central
dc.source.none.fl_str_mv reponame:DIGITAL.CSIC. Repositorio Institucional del CSIC
instname:Consejo Superior de Investigaciones Científicas (CSIC)
instname_str Consejo Superior de Investigaciones Científicas (CSIC)
reponame_str DIGITAL.CSIC. Repositorio Institucional del CSIC
collection DIGITAL.CSIC. Repositorio Institucional del CSIC
repository.name.fl_str_mv
repository.mail.fl_str_mv
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spelling Structure–function characterization of two enzymes from novel subfamilies of manganese peroxidases secreted by the lignocellulose-degrading Agaricales fungi Agrocybe pediades and Cyathus striatusSánchez-Ruiz, María I.Santillana, ElenaLinde, DoloresRomero, AntonioMartínez, Ángel T.Ruiz-Dueñas, F. J.Agrocybe pediadesCyathus striatusAgaricales fungiLigninManganese peroxidaseNovel enzymatic subfamiliesEnzyme catalysisCrystal structureManganese oxidation site21 p.-7 fig.-3 tab.Background: Manganese peroxidases (MnPs) are, together with lignin peroxidases and versatile peroxidases, key elements of the enzymatic machineries secreted by white-rot fungi to degrade lignin, thus providing access to cellulose and hemicellulose in plant cell walls. A recent genomic analysis of 52 Agaricomycetes species revealed the existence of novel MnP subfamilies differing in the amino-acid residues that constitute the manganese oxidation site. Following this in silico analysis, a comprehensive structure–function study is needed to understand how these enzymes work and contribute to transform the lignin macromoleculeResults: Two MnPs belonging to the subfamilies recently classified as MnP-DGD and MnP-ESD—referred to as Ape-MnP1 and Cst-MnP1, respectively—were identified as the primary peroxidases secreted by the Agaricales species Agrocybe pediades and Cyathus striatus when growing on lignocellulosic substrates. Following heterologous expression and in vitro activation, their biochemical characterization confirmed that these enzymes are active MnPs. However, crystal structure and mutagenesis studies revealed manganese coordination spheres different from those expected after their initial classification. Specifically, a glutamine residue (Gln333) in the C-terminal tail of Ape-MnP1 was found to be involved in manganese binding, along with Asp35 and Asp177, while Cst-MnP1 counts only two amino acids (Glu36 and Asp176), instead of three, to function as a MnP. These findings led to the renaming of these subfamilies as MnP-DDQ and MnP-ED and to re-evaluate their evolutionary origin. Both enzymes were also able to directly oxidize lignin-derived phenolic compounds, as seen for other short MnPs. Importantly, size-exclusion chromatography analyses showed that both enzymes cause changes in polymeric lignin in the presence of manganese, suggesting their relevance in lignocellulose transformation.Conclusions: Understanding the mechanisms used by basidiomycetes to degrade lignin is of particular relevance to comprehend carbon cycle in nature and to design biotechnological tools for the industrial use of plant biomass. Here, we provide the first structure–function characterization of two novel MnP subfamilies present in Agaricales mushrooms, elucidating the main residues involved in catalysis and demonstrating their ability to modify the lignin macromolecule.Open Access funding provided thanks to the CRUE-CSIC agreement with Springer Nature. This work has been funded by the projects GENOBIOREF (BIO2017-86559-R) and LIGT2PLAST (project PID2021-126384OB-I00 funded by MICIU/AEI/10.13039/501100011033/ and by ERDF A way of making Europe) to FJR-D and ATM; and by the Consejo Superior de Investigaciones Científicas PIE-202120E019 to ATM and PIE-202020E224 to AR, and the SusPlast platform to FJR-D.Peer reviewedBioMed CentralConsejo Superior de Investigaciones Científicas (España)Ministerio de Ciencia, Innovación y Universidades (España)Santillana, Elena [0000-0002-6227-1725]Linde, Dolores [0000-0002-0359-0566]Romero, Antonio [0000-0002-6990-6973]Martínez, Ángel T. [0000-0002-1584-2863]Ruiz-Dueñas, F. J. [0000-0002-9837-5665]Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]202520252024info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionhttp://hdl.handle.net/10261/381932reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)Inglés#PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE#info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016/BIO2017-86559-Rinfo:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2021-2023/PID2021-126384OB-I00https://doi.org/10.1186/s13068-024-02517-1Síinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/3819322026-05-22T06:33:51Z
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