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Proc Natl Acad Sci U S A. 2017 May 2;114(18):4709-4714. doi: 10.1073/pnas.1618360114. Epub 2017 Apr 19.

Lignocellulose pretreatment in a fungus-cultivating termite.

Author information

1
Ministry of Agriculture Key Laboratory of Agricultural Entomology, Institute of Insect Sciences, Zhejiang University, 310058 Hangzhou, China.
2
Department of Energy Great Lakes Bioenergy Research Center, Wisconsin Energy Institute, University of Wisconsin-Madison, Madison, WI 53726.
3
Department of Bacteriology, University of Wisconsin-Madison, Madison WI 53706.
4
US Forest Products Laboratory, Madison, WI 53726.
5
Department of Chemistry, Zhejiang University, 310058 Hangzhou, China.
6
Xiaoshan Management Center of Termite Control, 311200 Hangzhou, China.
7
Department of Energy Joint Genome Institute, Walnut Creek, CA 94598.
8
State Key Laboratory of Plant Physiology and Biochemistry, College of Life Sciences, Zhejiang University, 310058 Hangzhou, China.
9
Department of Energy Great Lakes Bioenergy Research Center, Wisconsin Energy Institute, University of Wisconsin-Madison, Madison, WI 53726; mojianchu@zju.edu.cn currie@bact.wisc.edu jralph@wisc.edu.
10
Department of Biochemistry, University of Wisconsin-Madison, Madison WI 53706.
11
Ministry of Agriculture Key Laboratory of Agricultural Entomology, Institute of Insect Sciences, Zhejiang University, 310058 Hangzhou, China; mojianchu@zju.edu.cn currie@bact.wisc.edu jralph@wisc.edu.

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.

KEYWORDS:

NMR; age polyethism; carbohydrate; lignin; symbiosis

PMID:
28424249
PMCID:
PMC5422824
DOI:
10.1073/pnas.1618360114
[Indexed for MEDLINE]
Free PMC Article

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