Oxidative cleavage of polysaccharides by a termite-derived superoxide dismutase boosts the degradation of biomass by glycoside hydrolases

Detalhes bibliográficos
Autor(a) principal: Franco Cairo, João Paulo L.
Data de Publicação: 2022
Outros Autores: Mandelli, Fernanda, Tramontina, Robson, Cannella, David, Paradisi, Alessandro, Ciano, Luisa, Ferreira, Marcel R. [UNESP], Liberato, Marcelo V., Brenelli, Lívia B., Gonçalves, Thiago A., Rodrigues, Gisele N., Alvarez, Thabata M., Mofatto, Luciana S., Carazzolle, Marcelo F., Pradella, José G. C., Paes Leme, Adriana F., Costa-Leonardo, Ana M. [UNESP], Oliveira-Neto, Mário [UNESP], Damasio, André, Davies, Gideon J., Felby, Claus, Walton, Paul H., Squina, Fabio M.
Tipo de documento: Artigo
Idioma: eng
Título da fonte: Repositório Institucional da UNESP
Texto Completo: http://dx.doi.org/10.1039/d1gc04519a
http://hdl.handle.net/11449/241937
Resumo: Wood-feeding termites effectively degrade plant biomass through enzymatic degradation. Despite their high efficiencies, however, individual glycoside hydrolases isolated from termites and their symbionts exhibit anomalously low effectiveness in lignocellulose degradation, suggesting hereto unknown enzymatic activities in their digestome. Herein, we demonstrate that an ancient redox-active enzyme encoded by the lower termite Coptotermes gestroi, a Cu/Zn superoxide dismutase (CgSOD-1), plays a previously unknown role in plant biomass degradation. We show that CgSOD-1 transcripts and peptides are up-regulated in response to an increased level of lignocellulose recalcitrance and that CgSOD-1 localizes in the lumen of the fore- and midguts of C. gestroi together with termite main cellulase, CgEG-1-GH9. CgSOD-1 boosts the saccharification of polysaccharides by CgEG-1-GH9. We show that the boosting effect of CgSOD-1 involves an oxidative mechanism of action in which CgSOD-1 generates reactive oxygen species that subsequently cleave the polysaccharide. SOD-type enzymes constitute a new addition to the growing family of oxidases, ones which are up-regulated when exposed to recalcitrant polysaccharides, and that are used by Nature for biomass degradation.
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spelling Oxidative cleavage of polysaccharides by a termite-derived superoxide dismutase boosts the degradation of biomass by glycoside hydrolasesWood-feeding termites effectively degrade plant biomass through enzymatic degradation. Despite their high efficiencies, however, individual glycoside hydrolases isolated from termites and their symbionts exhibit anomalously low effectiveness in lignocellulose degradation, suggesting hereto unknown enzymatic activities in their digestome. Herein, we demonstrate that an ancient redox-active enzyme encoded by the lower termite Coptotermes gestroi, a Cu/Zn superoxide dismutase (CgSOD-1), plays a previously unknown role in plant biomass degradation. We show that CgSOD-1 transcripts and peptides are up-regulated in response to an increased level of lignocellulose recalcitrance and that CgSOD-1 localizes in the lumen of the fore- and midguts of C. gestroi together with termite main cellulase, CgEG-1-GH9. CgSOD-1 boosts the saccharification of polysaccharides by CgEG-1-GH9. We show that the boosting effect of CgSOD-1 involves an oxidative mechanism of action in which CgSOD-1 generates reactive oxygen species that subsequently cleave the polysaccharide. SOD-type enzymes constitute a new addition to the growing family of oxidases, ones which are up-regulated when exposed to recalcitrant polysaccharides, and that are used by Nature for biomass degradation.Department of Biochemistry and Tissue Biology Institute of Biology University of Campinas (UNICAMP), São PauloDepartment of Geosciences and Natural Resource Management Faculty of Science University of Copenhagen, Rolighedsvej 23Department of Chemistry University of YorkBrazilian Biorenewables National Laboratory Brazilian Center for Research in Energy and Materials, São PauloPrograma de Processos Tecnológicos e Ambientais da Universidade de Sorocaba (UNISO), SPDepartamento de Física e Biofísica Instituto de Biociências Universidade Estadual Paulista UNESP, São PauloPrograma de Mestrado e Doutorado em Biotecnologia Industrial Universidade Positivo, PRLaboratório de Genômica e Expressão Departamento de Genética Evolução e Bioagentes Instituto de Biologia Universidade de Campinas UNICAMP, São PauloLaboratório Nacional de Biociências (LNBio) Centro Nacional de Pesquisa em Energia e Materiais (CNPEM), São PauloLaboratório de Cupins Departamento de Biologia Geral e Aplicada Instituto de Biociências Universidade Estadual Paulista UNESP, São PauloDepartamento de Física e Biofísica Instituto de Biociências Universidade Estadual Paulista UNESP, São PauloLaboratório de Cupins Departamento de Biologia Geral e Aplicada Instituto de Biociências Universidade Estadual Paulista UNESP, São PauloUniversidade Estadual de Campinas (UNICAMP)University of CopenhagenUniversity of YorkBrazilian Center for Research in Energy and MaterialsPrograma de Processos Tecnológicos e Ambientais da Universidade de Sorocaba (UNISO)Universidade Estadual Paulista (UNESP)Universidade PositivoCentro Nacional de Pesquisa em Energia e Materiais (CNPEM)Franco Cairo, João Paulo L.Mandelli, FernandaTramontina, RobsonCannella, DavidParadisi, AlessandroCiano, LuisaFerreira, Marcel R. [UNESP]Liberato, Marcelo V.Brenelli, Lívia B.Gonçalves, Thiago A.Rodrigues, Gisele N.Alvarez, Thabata M.Mofatto, Luciana S.Carazzolle, Marcelo F.Pradella, José G. C.Paes Leme, Adriana F.Costa-Leonardo, Ana M. [UNESP]Oliveira-Neto, Mário [UNESP]Damasio, AndréDavies, Gideon J.Felby, ClausWalton, Paul H.Squina, Fabio M.2023-03-02T04:42:43Z2023-03-02T04:42:43Z2022-05-12info:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/article4845-4858http://dx.doi.org/10.1039/d1gc04519aGreen Chemistry, v. 24, n. 12, p. 4845-4858, 2022.1463-92701463-9262http://hdl.handle.net/11449/24193710.1039/d1gc04519a2-s2.0-85131887969Scopusreponame:Repositório Institucional da UNESPinstname:Universidade Estadual Paulista (UNESP)instacron:UNESPengGreen Chemistryinfo:eu-repo/semantics/openAccess2023-03-02T04:42:44Zoai:repositorio.unesp.br:11449/241937Repositório InstitucionalPUBhttp://repositorio.unesp.br/oai/requestopendoar:29462024-08-05T18:46:07.039493Repositório Institucional da UNESP - Universidade Estadual Paulista (UNESP)false
dc.title.none.fl_str_mv Oxidative cleavage of polysaccharides by a termite-derived superoxide dismutase boosts the degradation of biomass by glycoside hydrolases
title Oxidative cleavage of polysaccharides by a termite-derived superoxide dismutase boosts the degradation of biomass by glycoside hydrolases
spellingShingle Oxidative cleavage of polysaccharides by a termite-derived superoxide dismutase boosts the degradation of biomass by glycoside hydrolases
Franco Cairo, João Paulo L.
title_short Oxidative cleavage of polysaccharides by a termite-derived superoxide dismutase boosts the degradation of biomass by glycoside hydrolases
title_full Oxidative cleavage of polysaccharides by a termite-derived superoxide dismutase boosts the degradation of biomass by glycoside hydrolases
title_fullStr Oxidative cleavage of polysaccharides by a termite-derived superoxide dismutase boosts the degradation of biomass by glycoside hydrolases
title_full_unstemmed Oxidative cleavage of polysaccharides by a termite-derived superoxide dismutase boosts the degradation of biomass by glycoside hydrolases
title_sort Oxidative cleavage of polysaccharides by a termite-derived superoxide dismutase boosts the degradation of biomass by glycoside hydrolases
author Franco Cairo, João Paulo L.
author_facet Franco Cairo, João Paulo L.
Mandelli, Fernanda
Tramontina, Robson
Cannella, David
Paradisi, Alessandro
Ciano, Luisa
Ferreira, Marcel R. [UNESP]
Liberato, Marcelo V.
Brenelli, Lívia B.
Gonçalves, Thiago A.
Rodrigues, Gisele N.
Alvarez, Thabata M.
Mofatto, Luciana S.
Carazzolle, Marcelo F.
Pradella, José G. C.
Paes Leme, Adriana F.
Costa-Leonardo, Ana M. [UNESP]
Oliveira-Neto, Mário [UNESP]
Damasio, André
Davies, Gideon J.
Felby, Claus
Walton, Paul H.
Squina, Fabio M.
author_role author
author2 Mandelli, Fernanda
Tramontina, Robson
Cannella, David
Paradisi, Alessandro
Ciano, Luisa
Ferreira, Marcel R. [UNESP]
Liberato, Marcelo V.
Brenelli, Lívia B.
Gonçalves, Thiago A.
Rodrigues, Gisele N.
Alvarez, Thabata M.
Mofatto, Luciana S.
Carazzolle, Marcelo F.
Pradella, José G. C.
Paes Leme, Adriana F.
Costa-Leonardo, Ana M. [UNESP]
Oliveira-Neto, Mário [UNESP]
Damasio, André
Davies, Gideon J.
Felby, Claus
Walton, Paul H.
Squina, Fabio M.
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Universidade Estadual de Campinas (UNICAMP)
University of Copenhagen
University of York
Brazilian Center for Research in Energy and Materials
Programa de Processos Tecnológicos e Ambientais da Universidade de Sorocaba (UNISO)
Universidade Estadual Paulista (UNESP)
Universidade Positivo
Centro Nacional de Pesquisa em Energia e Materiais (CNPEM)
dc.contributor.author.fl_str_mv Franco Cairo, João Paulo L.
Mandelli, Fernanda
Tramontina, Robson
Cannella, David
Paradisi, Alessandro
Ciano, Luisa
Ferreira, Marcel R. [UNESP]
Liberato, Marcelo V.
Brenelli, Lívia B.
Gonçalves, Thiago A.
Rodrigues, Gisele N.
Alvarez, Thabata M.
Mofatto, Luciana S.
Carazzolle, Marcelo F.
Pradella, José G. C.
Paes Leme, Adriana F.
Costa-Leonardo, Ana M. [UNESP]
Oliveira-Neto, Mário [UNESP]
Damasio, André
Davies, Gideon J.
Felby, Claus
Walton, Paul H.
Squina, Fabio M.
description Wood-feeding termites effectively degrade plant biomass through enzymatic degradation. Despite their high efficiencies, however, individual glycoside hydrolases isolated from termites and their symbionts exhibit anomalously low effectiveness in lignocellulose degradation, suggesting hereto unknown enzymatic activities in their digestome. Herein, we demonstrate that an ancient redox-active enzyme encoded by the lower termite Coptotermes gestroi, a Cu/Zn superoxide dismutase (CgSOD-1), plays a previously unknown role in plant biomass degradation. We show that CgSOD-1 transcripts and peptides are up-regulated in response to an increased level of lignocellulose recalcitrance and that CgSOD-1 localizes in the lumen of the fore- and midguts of C. gestroi together with termite main cellulase, CgEG-1-GH9. CgSOD-1 boosts the saccharification of polysaccharides by CgEG-1-GH9. We show that the boosting effect of CgSOD-1 involves an oxidative mechanism of action in which CgSOD-1 generates reactive oxygen species that subsequently cleave the polysaccharide. SOD-type enzymes constitute a new addition to the growing family of oxidases, ones which are up-regulated when exposed to recalcitrant polysaccharides, and that are used by Nature for biomass degradation.
publishDate 2022
dc.date.none.fl_str_mv 2022-05-12
2023-03-02T04:42:43Z
2023-03-02T04:42:43Z
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://dx.doi.org/10.1039/d1gc04519a
Green Chemistry, v. 24, n. 12, p. 4845-4858, 2022.
1463-9270
1463-9262
http://hdl.handle.net/11449/241937
10.1039/d1gc04519a
2-s2.0-85131887969
url http://dx.doi.org/10.1039/d1gc04519a
http://hdl.handle.net/11449/241937
identifier_str_mv Green Chemistry, v. 24, n. 12, p. 4845-4858, 2022.
1463-9270
1463-9262
10.1039/d1gc04519a
2-s2.0-85131887969
dc.language.iso.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv Green Chemistry
dc.rights.driver.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv 4845-4858
dc.source.none.fl_str_mv Scopus
reponame:Repositório Institucional da UNESP
instname:Universidade Estadual Paulista (UNESP)
instacron:UNESP
instname_str Universidade Estadual Paulista (UNESP)
instacron_str UNESP
institution UNESP
reponame_str Repositório Institucional da UNESP
collection Repositório Institucional da UNESP
repository.name.fl_str_mv Repositório Institucional da UNESP - Universidade Estadual Paulista (UNESP)
repository.mail.fl_str_mv
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