A Fungal Secretome Adapted for Stress Enabled a Radical Wood Decay Mechanism

ABSTRACT Brown rot fungi release massive amounts of carbon from forest deadwood, particularly at high latitudes. These fungi degrade wood by generating small reactive oxygen species (ROS) to loosen lignocellulose, to then selectively remove carbohydrates. The ROS mechanism has long been considered t...

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Autores principales:	Jesus Castaño, Jiwei Zhang, Mowei Zhou, Chia-Feng Tsai, Joon Yong Lee, Carrie Nicora, Jonathan Schilling
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2021
Materias:	brown rot fungi ROS tolerance glycosyl hydrolases proteomics Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/3fa1c5f2d2674a6d8c1824677c2fac44
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spelling	oai:doaj.org-article:3fa1c5f2d2674a6d8c1824677c2fac442021-11-10T18:37:52ZA Fungal Secretome Adapted for Stress Enabled a Radical Wood Decay Mechanism10.1128/mBio.02040-212150-7511https://doaj.org/article/3fa1c5f2d2674a6d8c1824677c2fac442021-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02040-21https://doaj.org/toc/2150-7511ABSTRACT Brown rot fungi release massive amounts of carbon from forest deadwood, particularly at high latitudes. These fungi degrade wood by generating small reactive oxygen species (ROS) to loosen lignocellulose, to then selectively remove carbohydrates. The ROS mechanism has long been considered the key adaptation defining brown rot wood decomposition, but recently, we found preliminary evidence that fungal glycoside hydrolases (GHs) implicated in early cell wall loosening might have been adapted to tolerate ROS stress and to synergize with ROS to loosen woody lignocellulose. In the current study, we found more specifically that side chain hemicellulases that help in the early deconstruction of the lignocellulosic complex are significantly more tolerant of ROS in the brown rot fungus Rhodonia placenta than in a white rot fungus (Trametes versicolor) and a soft rot fungus (Trichoderma reesei). Using proteomics to understand the extent of tolerance, we found that significant oxidation of secreted R. placenta proteins exposed to ROS was less than half of the oxidation observed for T. versicolor or T. reesei. The principal oxidative modifications observed in all cases were monooxidation and dioxidation/trioxidation (mainly in methionine and tryptophan residues), some of which were critical for enzyme activity. At the peptide level, we found that GHs in R. placenta were the least ROS affected among our tested fungi. These results confirm and describe underlying mechanisms of tolerance in early-secreted brown rot fungal hemicellulases. These enzymatic adaptations may have been as important as nonenzymatic ROS pathway adaptations in brown rot fungal evolution. IMPORTANCE Brown rot fungi play a critical role in carbon recycling and are of industrial interest. These fungi typically use reactive oxygen species (ROS) to indiscriminately “loosen” wood cell walls at the outset of decay. Brown rot fungi avoid oxidative stress associated with this ROS step by delaying the expression/secretion of many carbohydrate-active enzymes, but there are exceptions, notably some side chain hemicellulases, implicated in loosening lignocellulose. In this study, we provide enzyme activity and secretomic evidence that these enzymes in the brown rot model Rhodonia placenta are more ROS tolerant than the white and soft rot isolates tested. For R. placenta, and perhaps all brown rot lineages, these ROS tolerance adaptions may have played a long-overshadowed role in enabling brown rot.Jesus CastañoJiwei ZhangMowei ZhouChia-Feng TsaiJoon Yong LeeCarrie NicoraJonathan SchillingAmerican Society for Microbiologyarticlebrown rot fungiROS toleranceglycosyl hydrolasesproteomicsMicrobiologyQR1-502ENmBio, Vol 12, Iss 4 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	brown rot fungi ROS tolerance glycosyl hydrolases proteomics Microbiology QR1-502
spellingShingle	brown rot fungi ROS tolerance glycosyl hydrolases proteomics Microbiology QR1-502 Jesus Castaño Jiwei Zhang Mowei Zhou Chia-Feng Tsai Joon Yong Lee Carrie Nicora Jonathan Schilling A Fungal Secretome Adapted for Stress Enabled a Radical Wood Decay Mechanism
description	ABSTRACT Brown rot fungi release massive amounts of carbon from forest deadwood, particularly at high latitudes. These fungi degrade wood by generating small reactive oxygen species (ROS) to loosen lignocellulose, to then selectively remove carbohydrates. The ROS mechanism has long been considered the key adaptation defining brown rot wood decomposition, but recently, we found preliminary evidence that fungal glycoside hydrolases (GHs) implicated in early cell wall loosening might have been adapted to tolerate ROS stress and to synergize with ROS to loosen woody lignocellulose. In the current study, we found more specifically that side chain hemicellulases that help in the early deconstruction of the lignocellulosic complex are significantly more tolerant of ROS in the brown rot fungus Rhodonia placenta than in a white rot fungus (Trametes versicolor) and a soft rot fungus (Trichoderma reesei). Using proteomics to understand the extent of tolerance, we found that significant oxidation of secreted R. placenta proteins exposed to ROS was less than half of the oxidation observed for T. versicolor or T. reesei. The principal oxidative modifications observed in all cases were monooxidation and dioxidation/trioxidation (mainly in methionine and tryptophan residues), some of which were critical for enzyme activity. At the peptide level, we found that GHs in R. placenta were the least ROS affected among our tested fungi. These results confirm and describe underlying mechanisms of tolerance in early-secreted brown rot fungal hemicellulases. These enzymatic adaptations may have been as important as nonenzymatic ROS pathway adaptations in brown rot fungal evolution. IMPORTANCE Brown rot fungi play a critical role in carbon recycling and are of industrial interest. These fungi typically use reactive oxygen species (ROS) to indiscriminately “loosen” wood cell walls at the outset of decay. Brown rot fungi avoid oxidative stress associated with this ROS step by delaying the expression/secretion of many carbohydrate-active enzymes, but there are exceptions, notably some side chain hemicellulases, implicated in loosening lignocellulose. In this study, we provide enzyme activity and secretomic evidence that these enzymes in the brown rot model Rhodonia placenta are more ROS tolerant than the white and soft rot isolates tested. For R. placenta, and perhaps all brown rot lineages, these ROS tolerance adaptions may have played a long-overshadowed role in enabling brown rot.
format	article
author	Jesus Castaño Jiwei Zhang Mowei Zhou Chia-Feng Tsai Joon Yong Lee Carrie Nicora Jonathan Schilling
author_facet	Jesus Castaño Jiwei Zhang Mowei Zhou Chia-Feng Tsai Joon Yong Lee Carrie Nicora Jonathan Schilling
author_sort	Jesus Castaño
title	A Fungal Secretome Adapted for Stress Enabled a Radical Wood Decay Mechanism
title_short	A Fungal Secretome Adapted for Stress Enabled a Radical Wood Decay Mechanism
title_full	A Fungal Secretome Adapted for Stress Enabled a Radical Wood Decay Mechanism
title_fullStr	A Fungal Secretome Adapted for Stress Enabled a Radical Wood Decay Mechanism
title_full_unstemmed	A Fungal Secretome Adapted for Stress Enabled a Radical Wood Decay Mechanism
title_sort	fungal secretome adapted for stress enabled a radical wood decay mechanism
publisher	American Society for Microbiology
publishDate	2021
url	https://doaj.org/article/3fa1c5f2d2674a6d8c1824677c2fac44
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A Fungal Secretome Adapted for Stress Enabled a Radical Wood Decay Mechanism

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