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
Affiliations
Su Sun
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; College of Urban Construction, Wuchang Shouyi University, Wuhan 430064, China
Fei Li
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; Department of Bioengineering, School of Chemistry and Chemical Engineering, Wuhan University of Science and Technology, Wuhan 430081, China
Muzi Li
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; Texas A&M Agrilife Synthetic, Systems Biology Innovation Hub, Department of Plant Pathology and Microbiology, Texas A&M University, College Station, TX 77843, USA
Wenqian Zhang
Texas A&M Agrilife Synthetic, Systems Biology Innovation Hub, Department of Plant Pathology and Microbiology, Texas A&M University, College Station, TX 77843, USA
Zhenxiong Jiang
Texas A&M Agrilife Synthetic, Systems Biology Innovation Hub, Department of Plant Pathology and Microbiology, Texas A&M University, College Station, TX 77843, USA
Honglu Zhao
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
Yunqiao Pu
Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN 37831, USA
Arthur J. Ragauskas
Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN 37831, USA; Department of Chemical and Biomolecular Engineering, Department of Forestry, Wildlife, and Fisheries, University of Tennessee, Knoxville, TN 37996, USA
Susie Y. Dai
Texas A&M Agrilife Synthetic, Systems Biology Innovation Hub, Department of Plant Pathology and Microbiology, Texas A&M University, College Station, TX 77843, USA
Xiaoyu Zhang
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
Hongbo Yu
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; Corresponding author
Joshua S. Yuan
Department of Energy, Environmental, and Chemical Engineering, Washington University in St. Louis, St. Louis, MO 63130, USA; Corresponding author
Shangxian Xie
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; Corresponding author
Summary: 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.