Oxidation of a non-phenolic lignin model compound by two Irpex lacteus manganese peroxidases: evidence for implication of carboxylate and radicals

Abstract Background Manganese peroxidase is one of the Class II fungal peroxidases that are able to oxidize the low redox potential phenolic lignin compounds. For high redox potential non-phenolic lignin degradation, mediators such as GSH and unsaturated fatty acids are required in the reaction. How...

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Main Authors: Xing Qin, Xianhua Sun, Huoqing Huang, Yingguo Bai, Yuan Wang, Huiying Luo, Bin Yao, Xiaoyu Zhang, Xiaoyun Su
Format: Article
Language:English
Published: BMC 2017-04-01
Series:Biotechnology for Biofuels
Subjects:
Online Access:http://link.springer.com/article/10.1186/s13068-017-0787-z
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spelling doaj-1f97588f12e048aa8bf2524b1fe62eef2020-11-24T21:43:26ZengBMCBiotechnology for Biofuels1754-68342017-04-0110111310.1186/s13068-017-0787-zOxidation of a non-phenolic lignin model compound by two Irpex lacteus manganese peroxidases: evidence for implication of carboxylate and radicalsXing Qin0Xianhua Sun1Huoqing Huang2Yingguo Bai3Yuan Wang4Huiying Luo5Bin Yao6Xiaoyu Zhang7Xiaoyun Su8College of Life Science and Technology, Huazhong University of Science and TechnologyKey Laboratory for Feed Biotechnology of the Ministry of Agriculture, Feed Research Institute, Chinese Academy of Agricultural SciencesKey Laboratory for Feed Biotechnology of the Ministry of Agriculture, Feed Research Institute, Chinese Academy of Agricultural SciencesKey Laboratory for Feed Biotechnology of the Ministry of Agriculture, Feed Research Institute, Chinese Academy of Agricultural SciencesKey Laboratory for Feed Biotechnology of the Ministry of Agriculture, Feed Research Institute, Chinese Academy of Agricultural SciencesKey Laboratory for Feed Biotechnology of the Ministry of Agriculture, Feed Research Institute, Chinese Academy of Agricultural SciencesKey Laboratory for Feed Biotechnology of the Ministry of Agriculture, Feed Research Institute, Chinese Academy of Agricultural SciencesCollege of Life Science and Technology, Huazhong University of Science and TechnologyKey Laboratory for Feed Biotechnology of the Ministry of Agriculture, Feed Research Institute, Chinese Academy of Agricultural SciencesAbstract Background Manganese peroxidase is one of the Class II fungal peroxidases that are able to oxidize the low redox potential phenolic lignin compounds. For high redox potential non-phenolic lignin degradation, mediators such as GSH and unsaturated fatty acids are required in the reaction. However, it is not known whether carboxylic acids are a mediator for non-phenolic lignin degradation. Results The white rot fungus Irpex lacteus is one of the most potent fungi in degradation of lignocellulose and xenobiotics. Two manganese peroxidases (IlMnP1 and IlMnP2) from I. lacteus CD2 were over-expressed in Escherichia coli and successfully refolded from inclusion bodies. Both IlMnP1 and IlMnP2 oxidized the phenolic compounds efficiently. Surprisingly, they could degrade veratryl alcohol, a non-phenolic lignin compound, in a Mn2+-dependent fashion. Malonate or oxalate was found to be also essential in this degradation. The oxidation of non-phenolic lignin was further confirmed by analysis of the reaction products using LC–MS/MS. We proved that Mn2+ and a certain carboxylate are indispensable in oxidation and that the radicals generated under this condition, specifically superoxide radical, are at least partially involved in lignin oxidative degradation. IlMnP1 and IlMnP2 can also efficiently decolorize dyes with different structures. Conclusions We provide evidence that a carboxylic acid may mediate oxidation of non-phenolic lignin through the action of radicals. MnPs, but not LiP, VP, or DyP, are predominant peroxidases secreted by some white rot fungi such as I. lacteus and the selective lignocellulose degrader Ceriporiopsis subvermispora. Our finding will help understand how these fungi can utilize MnPs and an excreted organic acid, which is usually a normal metabolite, to efficiently degrade the non-phenolic lignin. The unique properties of IlMnP1 and IlMnP2 make them good candidates for exploring molecular mechanisms underlying non-phenolic lignin compounds oxidation by MnPs and for applications in lignocellulose degradation and environmental remediation.http://link.springer.com/article/10.1186/s13068-017-0787-zIrpex lacteusManganese peroxidaseNon-phenolic ligninVeratryl alcoholDye decolorizationCarboxylate
collection DOAJ
language English
format Article
sources DOAJ
author Xing Qin
Xianhua Sun
Huoqing Huang
Yingguo Bai
Yuan Wang
Huiying Luo
Bin Yao
Xiaoyu Zhang
Xiaoyun Su
spellingShingle Xing Qin
Xianhua Sun
Huoqing Huang
Yingguo Bai
Yuan Wang
Huiying Luo
Bin Yao
Xiaoyu Zhang
Xiaoyun Su
Oxidation of a non-phenolic lignin model compound by two Irpex lacteus manganese peroxidases: evidence for implication of carboxylate and radicals
Biotechnology for Biofuels
Irpex lacteus
Manganese peroxidase
Non-phenolic lignin
Veratryl alcohol
Dye decolorization
Carboxylate
author_facet Xing Qin
Xianhua Sun
Huoqing Huang
Yingguo Bai
Yuan Wang
Huiying Luo
Bin Yao
Xiaoyu Zhang
Xiaoyun Su
author_sort Xing Qin
title Oxidation of a non-phenolic lignin model compound by two Irpex lacteus manganese peroxidases: evidence for implication of carboxylate and radicals
title_short Oxidation of a non-phenolic lignin model compound by two Irpex lacteus manganese peroxidases: evidence for implication of carboxylate and radicals
title_full Oxidation of a non-phenolic lignin model compound by two Irpex lacteus manganese peroxidases: evidence for implication of carboxylate and radicals
title_fullStr Oxidation of a non-phenolic lignin model compound by two Irpex lacteus manganese peroxidases: evidence for implication of carboxylate and radicals
title_full_unstemmed Oxidation of a non-phenolic lignin model compound by two Irpex lacteus manganese peroxidases: evidence for implication of carboxylate and radicals
title_sort oxidation of a non-phenolic lignin model compound by two irpex lacteus manganese peroxidases: evidence for implication of carboxylate and radicals
publisher BMC
series Biotechnology for Biofuels
issn 1754-6834
publishDate 2017-04-01
description Abstract Background Manganese peroxidase is one of the Class II fungal peroxidases that are able to oxidize the low redox potential phenolic lignin compounds. For high redox potential non-phenolic lignin degradation, mediators such as GSH and unsaturated fatty acids are required in the reaction. However, it is not known whether carboxylic acids are a mediator for non-phenolic lignin degradation. Results The white rot fungus Irpex lacteus is one of the most potent fungi in degradation of lignocellulose and xenobiotics. Two manganese peroxidases (IlMnP1 and IlMnP2) from I. lacteus CD2 were over-expressed in Escherichia coli and successfully refolded from inclusion bodies. Both IlMnP1 and IlMnP2 oxidized the phenolic compounds efficiently. Surprisingly, they could degrade veratryl alcohol, a non-phenolic lignin compound, in a Mn2+-dependent fashion. Malonate or oxalate was found to be also essential in this degradation. The oxidation of non-phenolic lignin was further confirmed by analysis of the reaction products using LC–MS/MS. We proved that Mn2+ and a certain carboxylate are indispensable in oxidation and that the radicals generated under this condition, specifically superoxide radical, are at least partially involved in lignin oxidative degradation. IlMnP1 and IlMnP2 can also efficiently decolorize dyes with different structures. Conclusions We provide evidence that a carboxylic acid may mediate oxidation of non-phenolic lignin through the action of radicals. MnPs, but not LiP, VP, or DyP, are predominant peroxidases secreted by some white rot fungi such as I. lacteus and the selective lignocellulose degrader Ceriporiopsis subvermispora. Our finding will help understand how these fungi can utilize MnPs and an excreted organic acid, which is usually a normal metabolite, to efficiently degrade the non-phenolic lignin. The unique properties of IlMnP1 and IlMnP2 make them good candidates for exploring molecular mechanisms underlying non-phenolic lignin compounds oxidation by MnPs and for applications in lignocellulose degradation and environmental remediation.
topic Irpex lacteus
Manganese peroxidase
Non-phenolic lignin
Veratryl alcohol
Dye decolorization
Carboxylate
url http://link.springer.com/article/10.1186/s13068-017-0787-z
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