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

Su Sun; Fei Li; Muzi Li; Wenqian Zhang; Zhenxiong Jiang; Honglu Zhao; Yunqiao Pu; Arthur J Ragauskas; Susie Y Dai; Xiaoyu Zhang; Hongbo Yu; Joshua S Yuan; Shangxian Xie

doi:10.1016/j.isci.2023.107870

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

iScience. 2023 Sep 9;26(10):107870. doi: 10.1016/j.isci.2023.107870. eCollection 2023 Oct 20.

Authors

Su Sun^{1

2}, Fei Li^{1

3}, Muzi Li^{1

4}, Wenqian Zhang⁴, Zhenxiong Jiang⁴, Honglu Zhao¹, Yunqiao Pu⁵, Arthur J Ragauskas^{5

6}, Susie Y Dai⁴, Xiaoyu Zhang¹, Hongbo Yu¹, Joshua S Yuan⁷, Shangxian Xie¹

Affiliations

¹ Department of Biotechnology, Key Laboratory of Molecular Biophysics of the Ministry of Education, College of Life Science and Technology, Huazhong University of Science and Technology, Wuhan 430074, China.
² College of Urban Construction, Wuchang Shouyi University, Wuhan 430064, China.
³ Department of Bioengineering, School of Chemistry and Chemical Engineering, Wuhan University of Science and Technology, Wuhan 430081, China.
⁴ Texas A&M Agrilife Synthetic, Systems Biology Innovation Hub, Department of Plant Pathology and Microbiology, Texas A&M University, College Station, TX 77843, USA.
⁵ Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN 37831, USA.
⁶ Department of Chemical and Biomolecular Engineering, Department of Forestry, Wildlife, and Fisheries, University of Tennessee, Knoxville, TN 37996, USA.
⁷ Department of Energy, Environmental, and Chemical Engineering, Washington University in St. Louis, St. Louis, MO 63130, USA.

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.

Keywords: Biomass; Biotechnology.