Oxidative cleavage of polysaccharides by a termite-derived superoxide dismutase boosts the degradation of biomass by glycoside hydrolases
Autor(a) principal: | |
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Data de Publicação: | 2022 |
Outros Autores: | , , , , , , , , , , , , , , , , , , , , , |
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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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 |
|
_version_ |
1808128976493740032 |