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Multi-omics analysis provides insights into lignocellulosic biomass degradation by Laetiporus sulphureus ATCC 52600

BACKGROUND: Wood-decay basidiomycetes are effective for the degradation of highly lignified and recalcitrant plant substrates. The degradation of lignocellulosic materials by brown-rot strains is carried out by carbohydrate-active enzymes and non-enzymatic Fenton mechanism. Differences in the lignoc...

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Autores principales: de Figueiredo, Fernanda Lopes, de Oliveira, Ana Carolina Piva, Terrasan, Cesar Rafael Fanchini, Gonçalves, Thiago Augusto, Gerhardt, Jaqueline Aline, Tomazetto, Geizecler, Persinoti, Gabriela Felix, Rubio, Marcelo Ventura, Peña, Jennifer Andrea Tamayo, Araújo, Michelle Fernandes, de Carvalho Silvello, Maria Augusta, Franco, Telma Teixeira, Rabelo, Sarita Cândida, Goldbeck, Rosana, Squina, Fabio Marcio, Damasio, André
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8052766/
https://www.ncbi.nlm.nih.gov/pubmed/33865436
http://dx.doi.org/10.1186/s13068-021-01945-7
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author de Figueiredo, Fernanda Lopes
de Oliveira, Ana Carolina Piva
Terrasan, Cesar Rafael Fanchini
Gonçalves, Thiago Augusto
Gerhardt, Jaqueline Aline
Tomazetto, Geizecler
Persinoti, Gabriela Felix
Rubio, Marcelo Ventura
Peña, Jennifer Andrea Tamayo
Araújo, Michelle Fernandes
de Carvalho Silvello, Maria Augusta
Franco, Telma Teixeira
Rabelo, Sarita Cândida
Goldbeck, Rosana
Squina, Fabio Marcio
Damasio, André
author_facet de Figueiredo, Fernanda Lopes
de Oliveira, Ana Carolina Piva
Terrasan, Cesar Rafael Fanchini
Gonçalves, Thiago Augusto
Gerhardt, Jaqueline Aline
Tomazetto, Geizecler
Persinoti, Gabriela Felix
Rubio, Marcelo Ventura
Peña, Jennifer Andrea Tamayo
Araújo, Michelle Fernandes
de Carvalho Silvello, Maria Augusta
Franco, Telma Teixeira
Rabelo, Sarita Cândida
Goldbeck, Rosana
Squina, Fabio Marcio
Damasio, André
author_sort de Figueiredo, Fernanda Lopes
collection PubMed
description BACKGROUND: Wood-decay basidiomycetes are effective for the degradation of highly lignified and recalcitrant plant substrates. The degradation of lignocellulosic materials by brown-rot strains is carried out by carbohydrate-active enzymes and non-enzymatic Fenton mechanism. Differences in the lignocellulose catabolism among closely related brown rots are not completely understood. Here, a multi-omics approach provided a global understanding of the strategies employed by L. sulphureus ATCC 52600 for lignocellulose degradation. RESULTS: The genome of Laetiporus sulphureus ATCC 52600 was sequenced and phylogenomic analysis supported monophyletic clades for the Order Polyporales and classification of this species within the family Laetiporaceae. Additionally, the plasticity of its metabolism was revealed in growth analysis on mono- and disaccharides, and polysaccharides such as cellulose, hemicelluloses, and polygalacturonic acid. The response of this fungus to the presence of lignocellulosic substrates was analyzed by transcriptomics and proteomics and evidenced the occurrence of an integrated oxidative–hydrolytic metabolism. The transcriptomic profile in response to a short cultivation period on sugarcane bagasse revealed 125 upregulated transcripts, which included CAZymes (redox enzymes and hemicellulases) as well as non-CAZy redox enzymes and genes related to the synthesis of low-molecular-weight compounds. The exoproteome produced in response to extended cultivation time on Avicel, and steam-exploded sugarcane bagasse, sugarcane straw, and Eucalyptus revealed 112 proteins. Contrasting with the mainly oxidative profile observed in the transcriptome, the secretomes showed a diverse hydrolytic repertoire including constitutive cellulases and hemicellulases, in addition to 19 upregulated CAZymes. The secretome induced for 7 days on sugarcane bagasse, representative of the late response, was applied in the saccharification of hydrothermally pretreated grass (sugarcane straw) and softwood (pine) by supplementing a commercial cocktail. CONCLUSION: This study shows the singularity of L. sulphureus ATCC 52600 compared to other Polyporales brown rots, regarding the presence of cellobiohydrolase and peroxidase class II. The multi-omics analysis reinforces the oxidative–hydrolytic metabolism involved in lignocellulose deconstruction, providing insights into the overall mechanisms as well as specific proteins of each step. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13068-021-01945-7.
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spelling pubmed-80527662021-04-19 Multi-omics analysis provides insights into lignocellulosic biomass degradation by Laetiporus sulphureus ATCC 52600 de Figueiredo, Fernanda Lopes de Oliveira, Ana Carolina Piva Terrasan, Cesar Rafael Fanchini Gonçalves, Thiago Augusto Gerhardt, Jaqueline Aline Tomazetto, Geizecler Persinoti, Gabriela Felix Rubio, Marcelo Ventura Peña, Jennifer Andrea Tamayo Araújo, Michelle Fernandes de Carvalho Silvello, Maria Augusta Franco, Telma Teixeira Rabelo, Sarita Cândida Goldbeck, Rosana Squina, Fabio Marcio Damasio, André Biotechnol Biofuels Research BACKGROUND: Wood-decay basidiomycetes are effective for the degradation of highly lignified and recalcitrant plant substrates. The degradation of lignocellulosic materials by brown-rot strains is carried out by carbohydrate-active enzymes and non-enzymatic Fenton mechanism. Differences in the lignocellulose catabolism among closely related brown rots are not completely understood. Here, a multi-omics approach provided a global understanding of the strategies employed by L. sulphureus ATCC 52600 for lignocellulose degradation. RESULTS: The genome of Laetiporus sulphureus ATCC 52600 was sequenced and phylogenomic analysis supported monophyletic clades for the Order Polyporales and classification of this species within the family Laetiporaceae. Additionally, the plasticity of its metabolism was revealed in growth analysis on mono- and disaccharides, and polysaccharides such as cellulose, hemicelluloses, and polygalacturonic acid. The response of this fungus to the presence of lignocellulosic substrates was analyzed by transcriptomics and proteomics and evidenced the occurrence of an integrated oxidative–hydrolytic metabolism. The transcriptomic profile in response to a short cultivation period on sugarcane bagasse revealed 125 upregulated transcripts, which included CAZymes (redox enzymes and hemicellulases) as well as non-CAZy redox enzymes and genes related to the synthesis of low-molecular-weight compounds. The exoproteome produced in response to extended cultivation time on Avicel, and steam-exploded sugarcane bagasse, sugarcane straw, and Eucalyptus revealed 112 proteins. Contrasting with the mainly oxidative profile observed in the transcriptome, the secretomes showed a diverse hydrolytic repertoire including constitutive cellulases and hemicellulases, in addition to 19 upregulated CAZymes. The secretome induced for 7 days on sugarcane bagasse, representative of the late response, was applied in the saccharification of hydrothermally pretreated grass (sugarcane straw) and softwood (pine) by supplementing a commercial cocktail. CONCLUSION: This study shows the singularity of L. sulphureus ATCC 52600 compared to other Polyporales brown rots, regarding the presence of cellobiohydrolase and peroxidase class II. The multi-omics analysis reinforces the oxidative–hydrolytic metabolism involved in lignocellulose deconstruction, providing insights into the overall mechanisms as well as specific proteins of each step. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13068-021-01945-7. BioMed Central 2021-04-17 /pmc/articles/PMC8052766/ /pubmed/33865436 http://dx.doi.org/10.1186/s13068-021-01945-7 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
de Figueiredo, Fernanda Lopes
de Oliveira, Ana Carolina Piva
Terrasan, Cesar Rafael Fanchini
Gonçalves, Thiago Augusto
Gerhardt, Jaqueline Aline
Tomazetto, Geizecler
Persinoti, Gabriela Felix
Rubio, Marcelo Ventura
Peña, Jennifer Andrea Tamayo
Araújo, Michelle Fernandes
de Carvalho Silvello, Maria Augusta
Franco, Telma Teixeira
Rabelo, Sarita Cândida
Goldbeck, Rosana
Squina, Fabio Marcio
Damasio, André
Multi-omics analysis provides insights into lignocellulosic biomass degradation by Laetiporus sulphureus ATCC 52600
title Multi-omics analysis provides insights into lignocellulosic biomass degradation by Laetiporus sulphureus ATCC 52600
title_full Multi-omics analysis provides insights into lignocellulosic biomass degradation by Laetiporus sulphureus ATCC 52600
title_fullStr Multi-omics analysis provides insights into lignocellulosic biomass degradation by Laetiporus sulphureus ATCC 52600
title_full_unstemmed Multi-omics analysis provides insights into lignocellulosic biomass degradation by Laetiporus sulphureus ATCC 52600
title_short Multi-omics analysis provides insights into lignocellulosic biomass degradation by Laetiporus sulphureus ATCC 52600
title_sort multi-omics analysis provides insights into lignocellulosic biomass degradation by laetiporus sulphureus atcc 52600
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8052766/
https://www.ncbi.nlm.nih.gov/pubmed/33865436
http://dx.doi.org/10.1186/s13068-021-01945-7
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