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Open Access Research

Structure and regulation of the cellulose degradome in Clostridium cellulolyticum

Chenggang Xu1, Ranran Huang1, Lin Teng1, Dongmei Wang1, Christopher L Hemme2, Ilya Borovok3, Qiang He4, Raphael Lamed3, Edward A Bayer5, Jizhong Zhou2 and Jian Xu1*

Author Affiliations

1 BioEnergy Genome Center, CAS Key Laboratory of Biofuels and Shandong Key Laboratory of Energy Genetics, Qingdao Institute of Bioenergy and Bioprocess Technology, Chinese Academy of Sciences, Qingdao, Shandong 266101, China

2 Institute for Environmental Genomics, Department of Botany and Microbiology, University of Oklahoma, Norman, OK 73072, USA

3 Department of Molecular Microbiology and Biotechnology, Tel Aviv University, Ramat Aviv 69978, Israel

4 Department of Civil and Environmental Engineering, University of Tennessee, Knoxville, TN 37996, USA

5 Department of Biological Chemistry, Weizmann Institute of Science, Rehovot 76100, Israel

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Biotechnology for Biofuels 2013, 6:73  doi:10.1186/1754-6834-6-73

Published: 8 May 2013

Abstract

Background

Many bacteria efficiently degrade lignocellulose yet the underpinning genome-wide metabolic and regulatory networks remain elusive. Here we revealed the “cellulose degradome” for the model mesophilic cellulolytic bacterium Clostridium cellulolyticum ATCC 35319, via an integrated analysis of its complete genome, its transcriptomes under glucose, xylose, cellobiose, cellulose, xylan or corn stover and its extracellular proteomes under glucose, cellobiose or cellulose.

Results

Proteins for core metabolic functions, environment sensing, gene regulation and polysaccharide metabolism were enriched in the cellulose degradome. Analysis of differentially expressed genes revealed a “core” set of 48 CAZymes required for degrading cellulose-containing substrates as well as an “accessory” set of 76 CAZymes required for specific non-cellulose substrates. Gene co-expression analysis suggested that Carbon Catabolite Repression (CCR) related regulators sense intracellular glycolytic intermediates and control the core CAZymes that mainly include cellulosomal components, whereas 11 sets of Two-Component Systems (TCSs) respond to availability of extracellular soluble sugars and respectively regulate most of the accessory CAZymes and associated transporters. Surprisingly, under glucose alone, the core cellulases were highly expressed at both transcript and protein levels. Furthermore, glucose enhanced cellulolysis in a dose-dependent manner, via inducing cellulase transcription at low concentrations.

Conclusion

A molecular model of cellulose degradome in C. cellulolyticum (Ccel) was proposed, which revealed the substrate-specificity of CAZymes and the transcriptional regulation of core cellulases by CCR where the glucose acts as a CCR inhibitor instead of a trigger. These features represent a distinct environment-sensing strategy for competing while collaborating for cellulose utilization, which can be exploited for process and genetic engineering of microbial cellulolysis.

Keywords:
Cellulose degradation; Transcription; Two-component systems; Catabolite control proteins; CcpA-like; LacI family