The white rot basidiomycete Gelatoporia subvermispora produces fatty aldehydes that enable fungal manganese peroxidases to degrade recalcitrant lignin structures

35 p.-6 fig.-2 tab.

Detalles Bibliográficos
Autores: Kapich, Alexander N., Suzuki, Hideki, Hirth, Kolby C., Fernández-Fueyo, Elena, Martínez, Ángel T., Houtman, Carl J., Hammel, Kenneth E.
Tipo de recurso: artículo
Estado:Versión aceptada para publicación
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:10261/356856
Acceso en línea:http://hdl.handle.net/10261/356856
Access Level:acceso abierto
Palabra clave:Fatty aldehydes
Free radicals
Ligninolysis
Manganese peroxidase
White rot fungus
id ES_5eefd4e3d8ff45b14f3f8749078e05a2
oai_identifier_str oai:digital.csic.es:10261/356856
network_acronym_str ES
network_name_str España
repository_id_str
spelling The white rot basidiomycete Gelatoporia subvermispora produces fatty aldehydes that enable fungal manganese peroxidases to degrade recalcitrant lignin structuresKapich, Alexander N.Suzuki, HidekiHirth, Kolby C.Fernández-Fueyo, ElenaMartínez, Ángel T.Houtman, Carl J.Hammel, Kenneth E.Fatty aldehydesFree radicalsLigninolysisManganese peroxidaseWhite rot fungus35 p.-6 fig.-2 tab.The ability of some white rot basidiomycetes to remove lignin selectively from wood indicates that low molecular weight oxidants have a role in ligninolysis. These oxidants are likely free radicals generated by fungal peroxidases from compounds in the biodegrading wood. Past work supports a role for manganese peroxidases (MnPs) in the production of ligninolytic oxidants from fungal membrane lipids. However, the fatty acid alkylperoxyl radicals initially formed during this process are not reactive enough to attack the major structures in lignin. Here, we evaluate the hypothesis that the peroxidation of fatty aldehydes might provide a source of more reactive acylperoxyl radicals. We found that Gelatoporia subvermispora produced trans-2-nonenal, trans-2-octenal, and n-hexanal (a likely metabolite of trans-2,4-decadienal) during the incipient decay of aspen wood. Fungal fatty aldehydes supported the in vitro oxidation by MnPs of a nonphenolic lignin model dimer, and also of the monomeric model veratryl alcohol. Experiments with the latter compound showed that the reactions were partially inhibited by oxalate, the chelator that white rot fungi employ to detach Mn3+ from the MnP active site, but nevertheless proceeded at its physiological concentration of 1 mM. The addition of catalase was inhibitory, which suggests that the standard MnP catalytic cycle is involved in the oxidation of aldehydes. MnP oxidized trans-2-nonenal quantitatively to trans-2-nonenoic acid with the consumption of one O2 equivalent. The data suggest that when Mn3+ remains associated with MnP, it can oxidize aldehydes to their acyl radicals, and the latter subsequently add O2 to become ligninolytic acylperoxyl radicals.IMPORTANCEThe biodegradation of lignin by white rot fungi is essential for the natural recycling of plant biomass and has useful applications in lignocellulose bioprocessing. Although fungal peroxidases have a key role in ligninolysis, past work indicates that biodegradation is initiated by smaller, as yet unidentified oxidants that can infiltrate the substrate. Here, we present evidence that the peroxidase-catalyzed oxidation of naturally occurring fungal aldehydes may provide a source of ligninolytic free radical oxidants.This work was supported by grant DE-SC0006929 from the U.S. Department of Energy, Office of Biological and Environmental Research to KEH and CJH.Peer reviewedAmerican Society for MicrobiologyDepartment of Energy (US)Fernández-Fueyo, Elena [0000-0002-5079-2240]Martínez, Ángel T. [0000-0002-1584-2863]Houtman, Carl J. [0000-0001-8139-6673]Hammel, Kenneth E. [0000-0002-2935-5847]Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]202420242024info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Postprintinfo:eu-repo/semantics/acceptedVersionhttp://hdl.handle.net/10261/356856reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)Ingléshttps://doi.org/10.1128/aem.02044-23Síinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/3568562026-05-22T06:33:51Z
dc.title.none.fl_str_mv The white rot basidiomycete Gelatoporia subvermispora produces fatty aldehydes that enable fungal manganese peroxidases to degrade recalcitrant lignin structures
title The white rot basidiomycete Gelatoporia subvermispora produces fatty aldehydes that enable fungal manganese peroxidases to degrade recalcitrant lignin structures
spellingShingle The white rot basidiomycete Gelatoporia subvermispora produces fatty aldehydes that enable fungal manganese peroxidases to degrade recalcitrant lignin structures
Kapich, Alexander N.
Fatty aldehydes
Free radicals
Ligninolysis
Manganese peroxidase
White rot fungus
title_short The white rot basidiomycete Gelatoporia subvermispora produces fatty aldehydes that enable fungal manganese peroxidases to degrade recalcitrant lignin structures
title_full The white rot basidiomycete Gelatoporia subvermispora produces fatty aldehydes that enable fungal manganese peroxidases to degrade recalcitrant lignin structures
title_fullStr The white rot basidiomycete Gelatoporia subvermispora produces fatty aldehydes that enable fungal manganese peroxidases to degrade recalcitrant lignin structures
title_full_unstemmed The white rot basidiomycete Gelatoporia subvermispora produces fatty aldehydes that enable fungal manganese peroxidases to degrade recalcitrant lignin structures
title_sort The white rot basidiomycete Gelatoporia subvermispora produces fatty aldehydes that enable fungal manganese peroxidases to degrade recalcitrant lignin structures
dc.creator.none.fl_str_mv Kapich, Alexander N.
Suzuki, Hideki
Hirth, Kolby C.
Fernández-Fueyo, Elena
Martínez, Ángel T.
Houtman, Carl J.
Hammel, Kenneth E.
author Kapich, Alexander N.
author_facet Kapich, Alexander N.
Suzuki, Hideki
Hirth, Kolby C.
Fernández-Fueyo, Elena
Martínez, Ángel T.
Houtman, Carl J.
Hammel, Kenneth E.
author_role author
author2 Suzuki, Hideki
Hirth, Kolby C.
Fernández-Fueyo, Elena
Martínez, Ángel T.
Houtman, Carl J.
Hammel, Kenneth E.
author2_role author
author
author
author
author
author
dc.contributor.none.fl_str_mv Department of Energy (US)
Fernández-Fueyo, Elena [0000-0002-5079-2240]
Martínez, Ángel T. [0000-0002-1584-2863]
Houtman, Carl J. [0000-0001-8139-6673]
Hammel, Kenneth E. [0000-0002-2935-5847]
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv Fatty aldehydes
Free radicals
Ligninolysis
Manganese peroxidase
White rot fungus
topic Fatty aldehydes
Free radicals
Ligninolysis
Manganese peroxidase
White rot fungus
description 35 p.-6 fig.-2 tab.
publishDate 2024
dc.date.none.fl_str_mv 2024
2024
2024
dc.type.none.fl_str_mv info:eu-repo/semantics/article
http://purl.org/coar/resource_type/c_6501
Postprint
info:eu-repo/semantics/acceptedVersion
format article
status_str acceptedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/356856
url http://hdl.handle.net/10261/356856
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv https://doi.org/10.1128/aem.02044-23
Sí
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.publisher.none.fl_str_mv American Society for Microbiology
publisher.none.fl_str_mv American Society for Microbiology
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
_version_ 1869409167201009664
score 15,81155

Similares en LA Referencia