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Title: Lignocellulose pretreatment in a fungus-cultivating termite

Abstract

Depolymerizing lignin, the complex phenolic polymer fortifying plant cell walls, is an essential but challenging starting point for the lignocellulosics industries. The variety of ether– and carbon–carbon interunit linkages produced via radical coupling during lignification limit chemical and biological depolymerization efficiency. In an ancient fungus-cultivating termite system, we reveal unprecedentedly rapid lignin depolymerization and degradation by combining laboratory feeding experiments, lignocellulosic compositional measurements, electron microscopy, 2D-NMR, and thermochemolysis. In a gut transit time of under 3.5 h, in young worker termites, poplar lignin sidechains are extensively cleaved and the polymer is significantly depleted, leaving a residue almost completely devoid of various condensed units that are traditionally recognized to be the most recalcitrant. Subsequently, the fungus-comb microbiome preferentially uses xylose and cleaves polysaccharides, thus facilitating final utilization of easily digestible oligosaccharides by old worker termites. This complementary symbiotic pretreatment process in the fungus-growing termite symbiosis reveals a previously unappreciated natural system for efficient lignocellulose degradation.

Authors:
 [1];  [2];  [3];  [4];  [5];  [6];  [6];  [7];  [7];  [7]; ORCiD logo [8];  [9];  [7]
  1. Zhejiang Univ., Hangzhou (China). Ministry of Agriculture Key Laboratory of Agricultural Entomology, Institute of Insect Sciences; Univ. of Wisconsin, Madison, WI (United States). Department of Energy Great Lakes Bioenergy Research Center, Wisconsin Energy Institute and Department of Bacteriology
  2. US Forest Products Laboratory, Madison, WI (United States)
  3. Zhejiang Univ., Hangzhou (China). Department of Chemistry
  4. Xiaoshan Management Center of Termite Control, Hangzhou (China)
  5. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  6. Zhejiang Univ., Hangzhou (China). State Key Laboratory of Plant Physiology and Biochemistry, College of Life Sciences
  7. Zhejiang Univ., Hangzhou (China). Ministry of Agriculture Key Laboratory of Agricultural Entomology, Institute of Insect Sciences
  8. Univ. of Wisconsin, Madison, WI (United States). Department of Energy Great Lakes Bioenergy Research Center, Wisconsin Energy Institute and Department of Biochemistry
  9. Univ. of Wisconsin, Madison, WI (United States). Department of Energy Great Lakes Bioenergy Research Center, Wisconsin Energy Institute and Department of Bacteriology
Publication Date:
Research Org.:
Univ. of Wisconsin, Madison, WI (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1427585
Grant/Contract Number:  
FC02-07ER64494
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Volume: 114; Journal Issue: 18; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences, Washington, DC (United States)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; lignin; carbohydrate; NMR; symbiosis; age polyethism

Citation Formats

Li, Hongjie, Yelle, Daniel J., Li, Chang, Yang, Mengyi, Ke, Jing, Zhang, Ruijuan, Liu, Yu, Zhu, Na, Liang, Shiyou, Mo, Xiaochang, Ralph, John, Currie, Cameron R., and Mo, Jianchu. Lignocellulose pretreatment in a fungus-cultivating termite. United States: N. p., 2017. Web. doi:10.1073/pnas.1618360114.
Li, Hongjie, Yelle, Daniel J., Li, Chang, Yang, Mengyi, Ke, Jing, Zhang, Ruijuan, Liu, Yu, Zhu, Na, Liang, Shiyou, Mo, Xiaochang, Ralph, John, Currie, Cameron R., & Mo, Jianchu. Lignocellulose pretreatment in a fungus-cultivating termite. United States. doi:10.1073/pnas.1618360114.
Li, Hongjie, Yelle, Daniel J., Li, Chang, Yang, Mengyi, Ke, Jing, Zhang, Ruijuan, Liu, Yu, Zhu, Na, Liang, Shiyou, Mo, Xiaochang, Ralph, John, Currie, Cameron R., and Mo, Jianchu. Wed . "Lignocellulose pretreatment in a fungus-cultivating termite". United States. doi:10.1073/pnas.1618360114. https://www.osti.gov/servlets/purl/1427585.
@article{osti_1427585,
title = {Lignocellulose pretreatment in a fungus-cultivating termite},
author = {Li, Hongjie and Yelle, Daniel J. and Li, Chang and Yang, Mengyi and Ke, Jing and Zhang, Ruijuan and Liu, Yu and Zhu, Na and Liang, Shiyou and Mo, Xiaochang and Ralph, John and Currie, Cameron R. and Mo, Jianchu},
abstractNote = {Depolymerizing lignin, the complex phenolic polymer fortifying plant cell walls, is an essential but challenging starting point for the lignocellulosics industries. The variety of ether– and carbon–carbon interunit linkages produced via radical coupling during lignification limit chemical and biological depolymerization efficiency. In an ancient fungus-cultivating termite system, we reveal unprecedentedly rapid lignin depolymerization and degradation by combining laboratory feeding experiments, lignocellulosic compositional measurements, electron microscopy, 2D-NMR, and thermochemolysis. In a gut transit time of under 3.5 h, in young worker termites, poplar lignin sidechains are extensively cleaved and the polymer is significantly depleted, leaving a residue almost completely devoid of various condensed units that are traditionally recognized to be the most recalcitrant. Subsequently, the fungus-comb microbiome preferentially uses xylose and cleaves polysaccharides, thus facilitating final utilization of easily digestible oligosaccharides by old worker termites. This complementary symbiotic pretreatment process in the fungus-growing termite symbiosis reveals a previously unappreciated natural system for efficient lignocellulose degradation.},
doi = {10.1073/pnas.1618360114},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 18,
volume = 114,
place = {United States},
year = {Wed Apr 19 00:00:00 EDT 2017},
month = {Wed Apr 19 00:00:00 EDT 2017}
}

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Works referenced in this record:

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