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Title: Lytic polysaccharide monooxygenase synergized with lignin-degrading enzymes for efficient lignin degradation

Abstract

Even though the discovery of lytic polysaccharide monooxygenases (LPMOs) has fundamentally shifted our understanding of biomass degradation, most of the current studies focused on their roles in carbohydrate oxidation. However, no study demonstrated if LPMO could directly participate to the process of lignin degradation in lignin-degrading microbes. This study showed that LPMO could synergize with lignin-degrading enzymes for efficient lignin degradation in white-rot fungi. The transcriptomics analysis of fungi Irpex lacteus and Dichomitus squalens during their lignocellulosic biomass degradation processes surprisingly highlighted that LPMOs co-regulated with lignin-degrading enzymes, indicating their more versatile roles in the redox network. Biochemical analysis further confirmed that the purified LPMO from I. lacteus CD2 could use diverse electron donors to produce H2O2, drive Fenton reaction, and synergize with manganese peroxidase for lignin oxidation. The results thus indicated that LPMO might uniquely leverage the redox network toward dynamic and efficient degradation of different cell wall components.

Authors:
 [1];  [2];  [3];  [4];  [4];  [5]; ORCiD logo [6]; ORCiD logo [7];  [4];  [5];  [5];  [8];  [5]
+ Show Author Affiliations
  1. Huazhong Univ. of Science and Technology, Wuhan (China); Wuchang Shouyi University, Wuhan, (China)
  2. Huazhong Univ. of Science and Technology, Wuhan (China); Wuhan University of Science and Technology (China)
  3. Huazhong Univ. of Science and Technology, Wuhan (China); Texas A & M Univ., College Station, TX (United States)
  4. Texas A & M Univ., College Station, TX (United States)
  5. Huazhong Univ. of Science and Technology, Wuhan (China)
  6. Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
  7. Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States); Univ. of Tennessee, Knoxville, TN (United States)
  8. Washington Univ., St. Louis, MO (United States)
Publication Date:
Research Org.:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE; National Natural Science Foundation of China (NSFC); Natural Science Foundation of Hubei Province; Department of Education of Hubei Province
OSTI Identifier:
2267623
Grant/Contract Number:  
AC05-00OR22725; 31970098; 32170122; 31900081; 32000067; 2022CFB507; B2022398
Resource Type:
Accepted Manuscript
Journal Name:
iScience
Additional Journal Information:
Journal Volume: 26; Journal Issue: 10; Journal ID: ISSN 2589-0042
Publisher:
Elsevier
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; biotechnology; biomass

Citation Formats

Sun, Su, Li, Fei, Li, Muzi, Zhang, Wenqian, Jiang, Zhenxiong, Zhao, Honglu, Pu, Yunqiao, Ragauskas, Arthur J., Dai, Susie Y., Zhang, Xiaoyu, Yu, Hongbo, Yuan, Joshua S., and Xie, Shangxian. Lytic polysaccharide monooxygenase synergized with lignin-degrading enzymes for efficient lignin degradation. United States: N. p., 2023. Web. doi:10.1016/j.isci.2023.107870.
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Sun, Su, Li, Fei, Li, Muzi, Zhang, Wenqian, Jiang, Zhenxiong, Zhao, Honglu, Pu, Yunqiao, Ragauskas, Arthur J., Dai, Susie Y., Zhang, Xiaoyu, Yu, Hongbo, Yuan, Joshua S., & Xie, Shangxian. Lytic polysaccharide monooxygenase synergized with lignin-degrading enzymes for efficient lignin degradation. United States. https://doi.org/10.1016/j.isci.2023.107870
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Sun, Su, Li, Fei, Li, Muzi, Zhang, Wenqian, Jiang, Zhenxiong, Zhao, Honglu, Pu, Yunqiao, Ragauskas, Arthur J., Dai, Susie Y., Zhang, Xiaoyu, Yu, Hongbo, Yuan, Joshua S., and Xie, Shangxian. Sat . "Lytic polysaccharide monooxygenase synergized with lignin-degrading enzymes for efficient lignin degradation". United States. https://doi.org/10.1016/j.isci.2023.107870. https://www.osti.gov/servlets/purl/2267623.
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@article{osti_2267623,
title = {Lytic polysaccharide monooxygenase synergized with lignin-degrading enzymes for efficient lignin degradation},
author = {Sun, Su and Li, Fei and Li, Muzi and Zhang, Wenqian and Jiang, Zhenxiong and Zhao, Honglu and Pu, Yunqiao and Ragauskas, Arthur J. and Dai, Susie Y. and Zhang, Xiaoyu and Yu, Hongbo and Yuan, Joshua S. and Xie, Shangxian},
abstractNote = {Even though the discovery of lytic polysaccharide monooxygenases (LPMOs) has fundamentally shifted our understanding of biomass degradation, most of the current studies focused on their roles in carbohydrate oxidation. However, no study demonstrated if LPMO could directly participate to the process of lignin degradation in lignin-degrading microbes. This study showed that LPMO could synergize with lignin-degrading enzymes for efficient lignin degradation in white-rot fungi. The transcriptomics analysis of fungi Irpex lacteus and Dichomitus squalens during their lignocellulosic biomass degradation processes surprisingly highlighted that LPMOs co-regulated with lignin-degrading enzymes, indicating their more versatile roles in the redox network. Biochemical analysis further confirmed that the purified LPMO from I. lacteus CD2 could use diverse electron donors to produce H2O2, drive Fenton reaction, and synergize with manganese peroxidase for lignin oxidation. The results thus indicated that LPMO might uniquely leverage the redox network toward dynamic and efficient degradation of different cell wall components.},
doi = {10.1016/j.isci.2023.107870},
journal = {iScience},
number = 10,
volume = 26,
place = {United States},
year = {Sat Sep 09 00:00:00 EDT 2023},
month = {Sat Sep 09 00:00:00 EDT 2023}
}
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