Functional metagenomics reveals abundant polysaccharide-degrading gene clusters and cellobiose utilization pathways within gut microbiota of a wood-feeding higher termite
Abstract
Plant cell-wall polysaccharides constitute the most abundant but recalcitrant organic carbon source in nature. Microbes residing in the digestive tract of herbivorous bilaterians are particularly efficient at depolymerizing polysaccharides into fermentable sugars and play a significant support role towards their host’s lifestyle. Here, we combine large-scale functional screening of fosmid libraries, shotgun sequencing, and biochemical assays to interrogate the gut microbiota of the wood-feeding “higher” termite Globitermes brachycerastes. A number of putative polysaccharide utilization gene clusters were identified with multiple fibrolytic genes. Our large-scale functional screening of 50,000 fosmid clones resulted in 464 clones demonstrating plant polysaccharide-degrading activities, including 267 endoglucanase-, 24 exoglucanase-, 72 β-glucosidase-, and 101 endoxylanase-positive clones. We sequenced 173 functionally active clones and identified ~219 genes encoding putative carbohydrate-active enzymes (CAZymes) targeting cellulose, hemicellulose and pectin. Further analyses revealed that 68 of 154 contigs encode one or more CAZyme, which includes 35 examples of putative saccharolytic operons, suggesting that clustering of CAZymes is common in termite gut microbial inhabitants. Biochemical characterization of a representative xylanase cluster demonstrated that constituent enzymes exhibited complementary physicochemical properties and saccharolytic capabilities. Furthermore, diverse cellobiose-metabolizing enzymes include β-glucosidases, cellobiose phosphorylases, and phopho-6-β-glucosidases were identified and functionally verified, indicating that the termite gutmore »
- Authors:
-
[2];
[5];
[6];
- Chinese Academy of Sciences, Shanghai (China); Zhejiang Academy of Agricultural Sciences, Hangzhou (China)
- Univ. of Wisconsin, Madison, WI (United States)
- Chinese Academy of Sciences, Shanghai (China)
- Chinese Academy of Sciences, Shenzhen (China)
- Univ. of Kentucky, Lexington, KY (United States)
- Norwegian Univ. of Life Sciences, Ås (Norway)
- Chinese Academy of Sciences, Shanghai (China); Tongji Univ. School of Medicine, Shanghai (China)
- Publication Date:
- Research Org.:
- Univ. of Wisconsin, Madison, WI (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC)
- OSTI Identifier:
- 1609239
- Grant/Contract Number:
- FC02-07ER64494
- Resource Type:
- Accepted Manuscript
- Journal Name:
- The ISME Journal
- Additional Journal Information:
- Journal Volume: 13; Journal Issue: 1; Journal ID: ISSN 1751-7362
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Environmental Sciences & Ecology; Microbiology; Applied microbiology; Microbial ecology
Citation Formats
Liu, Ning, Li, Hongjie, Chevrette, Marc G., Zhang, Lei, Cao, Lin, Zhou, Haokui, Zhou, Xuguo, Zhou, Zhihua, Pope, Phillip B., Currie, Cameron R., Huang, Yongping, and Wang, Qian. Functional metagenomics reveals abundant polysaccharide-degrading gene clusters and cellobiose utilization pathways within gut microbiota of a wood-feeding higher termite. United States: N. p., 2018.
Web. doi:10.1038/s41396-018-0255-1.
Liu, Ning, Li, Hongjie, Chevrette, Marc G., Zhang, Lei, Cao, Lin, Zhou, Haokui, Zhou, Xuguo, Zhou, Zhihua, Pope, Phillip B., Currie, Cameron R., Huang, Yongping, & Wang, Qian. Functional metagenomics reveals abundant polysaccharide-degrading gene clusters and cellobiose utilization pathways within gut microbiota of a wood-feeding higher termite. United States. https://doi.org/10.1038/s41396-018-0255-1
Liu, Ning, Li, Hongjie, Chevrette, Marc G., Zhang, Lei, Cao, Lin, Zhou, Haokui, Zhou, Xuguo, Zhou, Zhihua, Pope, Phillip B., Currie, Cameron R., Huang, Yongping, and Wang, Qian. Thu .
"Functional metagenomics reveals abundant polysaccharide-degrading gene clusters and cellobiose utilization pathways within gut microbiota of a wood-feeding higher termite". United States. https://doi.org/10.1038/s41396-018-0255-1. https://www.osti.gov/servlets/purl/1609239.
@article{osti_1609239,
title = {Functional metagenomics reveals abundant polysaccharide-degrading gene clusters and cellobiose utilization pathways within gut microbiota of a wood-feeding higher termite},
author = {Liu, Ning and Li, Hongjie and Chevrette, Marc G. and Zhang, Lei and Cao, Lin and Zhou, Haokui and Zhou, Xuguo and Zhou, Zhihua and Pope, Phillip B. and Currie, Cameron R. and Huang, Yongping and Wang, Qian},
abstractNote = {Plant cell-wall polysaccharides constitute the most abundant but recalcitrant organic carbon source in nature. Microbes residing in the digestive tract of herbivorous bilaterians are particularly efficient at depolymerizing polysaccharides into fermentable sugars and play a significant support role towards their host’s lifestyle. Here, we combine large-scale functional screening of fosmid libraries, shotgun sequencing, and biochemical assays to interrogate the gut microbiota of the wood-feeding “higher” termite Globitermes brachycerastes. A number of putative polysaccharide utilization gene clusters were identified with multiple fibrolytic genes. Our large-scale functional screening of 50,000 fosmid clones resulted in 464 clones demonstrating plant polysaccharide-degrading activities, including 267 endoglucanase-, 24 exoglucanase-, 72 β-glucosidase-, and 101 endoxylanase-positive clones. We sequenced 173 functionally active clones and identified ~219 genes encoding putative carbohydrate-active enzymes (CAZymes) targeting cellulose, hemicellulose and pectin. Further analyses revealed that 68 of 154 contigs encode one or more CAZyme, which includes 35 examples of putative saccharolytic operons, suggesting that clustering of CAZymes is common in termite gut microbial inhabitants. Biochemical characterization of a representative xylanase cluster demonstrated that constituent enzymes exhibited complementary physicochemical properties and saccharolytic capabilities. Furthermore, diverse cellobiose-metabolizing enzymes include β-glucosidases, cellobiose phosphorylases, and phopho-6-β-glucosidases were identified and functionally verified, indicating that the termite gut micro-ecosystem utilizes diverse metabolic pathways to interconnect hydrolysis and central metabolism. Collectively, these results provide an in-depth view of the adaptation and digestive strategies employed by gut microbiota within this tiny-yet-efficient host-associated ecosystem.},
doi = {10.1038/s41396-018-0255-1},
journal = {The ISME Journal},
number = 1,
volume = 13,
place = {United States},
year = {Thu Aug 16 00:00:00 EDT 2018},
month = {Thu Aug 16 00:00:00 EDT 2018}
}
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