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Title: Peroxidase evolution in white-rot fungi follows wood lignin evolution in plants

Abstract

A comparison of sequenced Agaricomycotina genomes suggests that efficient degradation of wood lignin was associated with the appearance of secreted peroxidases with a solvent-exposed catalytic tryptophan. This hypothesis is experimentally demonstrated here by resurrecting ancestral fungal peroxidases, after sequence reconstruction from genomes of extant white-rot Polyporales, and evaluating their oxidative attack on the lignin polymer by state-of-the-art analytical techniques. Rapid stopped-flow estimation of the transient-state constants for the 2 successive one-electron transfers from lignin to the peroxide-activated enzyme ( k 2app and k 3app ) showed a progressive increase during peroxidase evolution (up to 50-fold higher values for the rate-limiting k 3app ). The above agreed with 2-dimensional NMR analyses during steady-state treatments of hardwood lignin, showing that its degradation (estimated from the normalized aromatic signals of lignin units compared with a control) and syringyl-to-guaiacyl ratio increased with the enzyme evolutionary distance from the first peroxidase ancestor. More interestingly, the stopped-flow estimations of electron transfer rates also showed how the most recent peroxidase ancestors that already incorporated the exposed tryptophan into their molecular structure (as well as the extant lignin peroxidase) were comparatively more efficient at oxidizing hardwood (angiosperm) lignin, while the most ancestralmore » “tryptophanless” enzymes were more efficient at abstracting electrons from softwood (conifer) lignin. A time calibration of the ancestry of Polyporales peroxidases localized the appearance of the first peroxidase with a solvent-exposed catalytic tryptophan to 194 ± 70 Mya, coincident with the diversification of angiosperm plants characterized by the appearance of dimethoxylated syringyl lignin units.« less

Authors:
ORCiD logo; ORCiD logo; ; ORCiD logo; ORCiD logo
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1564415
Alternate Identifier(s):
OSTI ID: 1625038
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Published Article
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Volume: 116 Journal Issue: 36; Journal ID: ISSN 0027-8424
Publisher:
Proceedings of the National Academy of Sciences
Country of Publication:
United States
Language:
English
Subject:
Science & Technology - Other Topics

Citation Formats

Ayuso-Fernández, Iván, Rencoret, Jorge, Gutiérrez, Ana, Ruiz-Dueñas, Francisco Javier, and Martínez, Angel T. Peroxidase evolution in white-rot fungi follows wood lignin evolution in plants. United States: N. p., 2019. Web. doi:10.1073/pnas.1905040116.
Ayuso-Fernández, Iván, Rencoret, Jorge, Gutiérrez, Ana, Ruiz-Dueñas, Francisco Javier, & Martínez, Angel T. Peroxidase evolution in white-rot fungi follows wood lignin evolution in plants. United States. doi:10.1073/pnas.1905040116.
Ayuso-Fernández, Iván, Rencoret, Jorge, Gutiérrez, Ana, Ruiz-Dueñas, Francisco Javier, and Martínez, Angel T. Mon . "Peroxidase evolution in white-rot fungi follows wood lignin evolution in plants". United States. doi:10.1073/pnas.1905040116.
@article{osti_1564415,
title = {Peroxidase evolution in white-rot fungi follows wood lignin evolution in plants},
author = {Ayuso-Fernández, Iván and Rencoret, Jorge and Gutiérrez, Ana and Ruiz-Dueñas, Francisco Javier and Martínez, Angel T.},
abstractNote = {A comparison of sequenced Agaricomycotina genomes suggests that efficient degradation of wood lignin was associated with the appearance of secreted peroxidases with a solvent-exposed catalytic tryptophan. This hypothesis is experimentally demonstrated here by resurrecting ancestral fungal peroxidases, after sequence reconstruction from genomes of extant white-rot Polyporales, and evaluating their oxidative attack on the lignin polymer by state-of-the-art analytical techniques. Rapid stopped-flow estimation of the transient-state constants for the 2 successive one-electron transfers from lignin to the peroxide-activated enzyme ( k 2app and k 3app ) showed a progressive increase during peroxidase evolution (up to 50-fold higher values for the rate-limiting k 3app ). The above agreed with 2-dimensional NMR analyses during steady-state treatments of hardwood lignin, showing that its degradation (estimated from the normalized aromatic signals of lignin units compared with a control) and syringyl-to-guaiacyl ratio increased with the enzyme evolutionary distance from the first peroxidase ancestor. More interestingly, the stopped-flow estimations of electron transfer rates also showed how the most recent peroxidase ancestors that already incorporated the exposed tryptophan into their molecular structure (as well as the extant lignin peroxidase) were comparatively more efficient at oxidizing hardwood (angiosperm) lignin, while the most ancestral “tryptophanless” enzymes were more efficient at abstracting electrons from softwood (conifer) lignin. A time calibration of the ancestry of Polyporales peroxidases localized the appearance of the first peroxidase with a solvent-exposed catalytic tryptophan to 194 ± 70 Mya, coincident with the diversification of angiosperm plants characterized by the appearance of dimethoxylated syringyl lignin units.},
doi = {10.1073/pnas.1905040116},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 36,
volume = 116,
place = {United States},
year = {2019},
month = {8}
}

Journal Article:
Free Publicly Available Full Text
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DOI: 10.1073/pnas.1905040116

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