Dramatic performance of Clostridium thermocellum explained by its wide range of cellulase modalities
Abstract
Clostridium thermocellum is the most efficient microorganism for solubilizing lignocellulosic biomass known to date. Its high cellulose digestion capability is attributed to efficient cellulases consisting of both a free-enzyme system and a tethered cellulosomal system wherein carbohydrate active enzymes (CAZymes) are organized by primary and secondary scaffoldin proteins to generate large protein complexes attached to the bacterial cell wall. This study demonstrates that C. thermocellum also uses a type of cellulosomal system not bound to the bacterial cell wall, called the “cell-free” cellulosomal system. The cell-free cellulosome complex can be seen as a “long range cellulosome” because it can diffuse away from the cell and degrade polysaccharide substrates remotely from the bacterial cell. The contribution of these two types of cellulosomal systems in C. thermocellum was elucidated by characterization of mutants with different combinations of scaffoldin gene deletions. The primary scaffoldin, CipA, was found to play the most important role in cellulose degradation by C. thermocellum, whereas the secondary scaffoldins have less important roles. Additionally, the distinct and efficient mode of action of the C. thermocellum exoproteome, wherein the cellulosomes splay or divide biomass particles, changes when either the primary or secondary scaffolds are removed, showing that the intact wild-typemore »
- Authors:
-
- National Renewable Energy Lab. (NREL), Golden, CO (United States); BioEnergy Science Center, Oak Ridge, TN (United States)
- BioEnergy Science Center, Oak Ridge, TN (United States); National Renewable Energy Lab. (NREL), Golden, CO (United States)
- National Renewable Energy Lab. (NREL), Golden, CO (United States)
- BioEnergy Science Center, Oak Ridge, TN (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
- BioEnergy Science Center, Oak Ridge, TN (United States); Dartmouth College, Hanover, NH (United States)
- The Weizmann Institute of Science, Rehovot (Israel)
- Publication Date:
- Research Org.:
- National Renewable Energy Laboratory (NREL), Golden, CO (United States); Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center (BESC)
- Sponsoring Org.:
- USDOE Office of Science (SC); USDOE Bioenergy Science Center (BESC)
- OSTI Identifier:
- 1244830
- Alternate Identifier(s):
- OSTI ID: 1286890
- Report Number(s):
- NREL/JA-2700-65384
Journal ID: ISSN 2375-2548
- Grant/Contract Number:
- AC36-08GO28308; AC05-00OR22725
- Resource Type:
- Journal Article: Accepted Manuscript
- Journal Name:
- Science Advances
- Additional Journal Information:
- Journal Volume: 2; Journal Issue: 2; Journal ID: ISSN 2375-2548
- Publisher:
- AAAS
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 09 BIOMASS FUELS; 59 BASIC BIOLOGICAL SCIENCES; cell biology; biomass; biofuels; cellulases; cellulosomes; 60 APPLIED LIFE SCIENCES
Citation Formats
Xu, Qi, Resch, Michael G., Podkaminer, Kara, Yang, Shihui, Baker, John O., Donohoe, Bryon S., Wilson, Charlotte, Klingeman, Dawn M., Olson, Daniel G., Decker, Stephen R., Richard J. Giannone, Hettich, Robert L., Brown, Steven D., Lynd, Lee R., Bayer, Edward A., Himmel, Michael E., and Bomble, Yannick J. Dramatic performance of Clostridium thermocellum explained by its wide range of cellulase modalities. United States: N. p., 2016.
Web. doi:10.1126/sciadv.1501254.
Xu, Qi, Resch, Michael G., Podkaminer, Kara, Yang, Shihui, Baker, John O., Donohoe, Bryon S., Wilson, Charlotte, Klingeman, Dawn M., Olson, Daniel G., Decker, Stephen R., Richard J. Giannone, Hettich, Robert L., Brown, Steven D., Lynd, Lee R., Bayer, Edward A., Himmel, Michael E., & Bomble, Yannick J. Dramatic performance of Clostridium thermocellum explained by its wide range of cellulase modalities. United States. https://doi.org/10.1126/sciadv.1501254
Xu, Qi, Resch, Michael G., Podkaminer, Kara, Yang, Shihui, Baker, John O., Donohoe, Bryon S., Wilson, Charlotte, Klingeman, Dawn M., Olson, Daniel G., Decker, Stephen R., Richard J. Giannone, Hettich, Robert L., Brown, Steven D., Lynd, Lee R., Bayer, Edward A., Himmel, Michael E., and Bomble, Yannick J. 2016.
"Dramatic performance of Clostridium thermocellum explained by its wide range of cellulase modalities". United States. https://doi.org/10.1126/sciadv.1501254. https://www.osti.gov/servlets/purl/1244830.
@article{osti_1244830,
title = {Dramatic performance of Clostridium thermocellum explained by its wide range of cellulase modalities},
author = {Xu, Qi and Resch, Michael G. and Podkaminer, Kara and Yang, Shihui and Baker, John O. and Donohoe, Bryon S. and Wilson, Charlotte and Klingeman, Dawn M. and Olson, Daniel G. and Decker, Stephen R. and Richard J. Giannone and Hettich, Robert L. and Brown, Steven D. and Lynd, Lee R. and Bayer, Edward A. and Himmel, Michael E. and Bomble, Yannick J.},
abstractNote = {Clostridium thermocellum is the most efficient microorganism for solubilizing lignocellulosic biomass known to date. Its high cellulose digestion capability is attributed to efficient cellulases consisting of both a free-enzyme system and a tethered cellulosomal system wherein carbohydrate active enzymes (CAZymes) are organized by primary and secondary scaffoldin proteins to generate large protein complexes attached to the bacterial cell wall. This study demonstrates that C. thermocellum also uses a type of cellulosomal system not bound to the bacterial cell wall, called the “cell-free” cellulosomal system. The cell-free cellulosome complex can be seen as a “long range cellulosome” because it can diffuse away from the cell and degrade polysaccharide substrates remotely from the bacterial cell. The contribution of these two types of cellulosomal systems in C. thermocellum was elucidated by characterization of mutants with different combinations of scaffoldin gene deletions. The primary scaffoldin, CipA, was found to play the most important role in cellulose degradation by C. thermocellum, whereas the secondary scaffoldins have less important roles. Additionally, the distinct and efficient mode of action of the C. thermocellum exoproteome, wherein the cellulosomes splay or divide biomass particles, changes when either the primary or secondary scaffolds are removed, showing that the intact wild-type cellulosomal system is necessary for this essential mode of action. This new transcriptional and proteomic evidence shows that a functional primary scaffoldin plays a more important role compared to secondary scaffoldins in the proper regulation of CAZyme genes, cellodextrin transport, and other cellular functions.},
doi = {10.1126/sciadv.1501254},
url = {https://www.osti.gov/biblio/1244830},
journal = {Science Advances},
issn = {2375-2548},
number = 2,
volume = 2,
place = {United States},
year = {Fri Feb 05 00:00:00 EST 2016},
month = {Fri Feb 05 00:00:00 EST 2016}
}
Web of Science
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- Li, Renmin; Feng, Yingang; Liu, Shiyue
- Microbial Biotechnology, Vol. 11, Issue 5
Simultaneous achievement of high ethanol yield and titer in Clostridium thermocellum
journal, June 2016
- Tian, Liang; Papanek, Beth; Olson, Daniel G.
- Biotechnology for Biofuels, Vol. 9, Issue 1
Integrated omics analyses reveal the details of metabolic adaptation of Clostridium thermocellum to lignocellulose-derived growth inhibitors released during the deconstruction of switchgrass
journal, January 2017
- Poudel, Suresh; Giannone, Richard J.; Rodriguez, Miguel
- Biotechnology for Biofuels, Vol. 10, Issue 1
Cellulosic ethanol production via consolidated bioprocessing by a novel thermophilic anaerobic bacterium isolated from a Himalayan hot spring
journal, March 2017
- Singh, Nisha; Mathur, Anshu S.; Tuli, Deepak K.
- Biotechnology for Biofuels, Vol. 10, Issue 1
Efficient whole-cell-catalyzing cellulose saccharification using engineered Clostridium thermocellum
journal, May 2017
- Zhang, Jie; Liu, Shiyue; Li, Renmin
- Biotechnology for Biofuels, Vol. 10, Issue 1
The LacI family protein GlyR3 co-regulates the celC operon and manB in Clostridium thermocellum
journal, June 2017
- Choi, Jinlyung; Klingeman, Dawn M.; Brown, Steven D.
- Biotechnology for Biofuels, Vol. 10, Issue 1
Adding tetrahydrofuran to dilute acid pretreatment provides new insights into substrate changes that greatly enhance biomass deconstruction by Clostridium thermocellum and fungal enzymes
journal, November 2017
- Thomas, Vanessa A.; Donohoe, Bryon S.; Li, Mi
- Biotechnology for Biofuels, Vol. 10, Issue 1
Clostridium thermocellum LL1210 pH homeostasis mechanisms informed by transcriptomics and metabolomics
journal, April 2018
- Whitham, Jason M.; Moon, Ji-Won; Rodriguez, Miguel
- Biotechnology for Biofuels, Vol. 11, Issue 1
An iterative computational design approach to increase the thermal endurance of a mesophilic enzyme
journal, July 2018
- Sammond, Deanne W.; Kastelowitz, Noah; Donohoe, Bryon S.
- Biotechnology for Biofuels, Vol. 11, Issue 1
Multiple levers for overcoming the recalcitrance of lignocellulosic biomass
journal, January 2019
- Holwerda, Evert K.; Worthen, Robert S.; Kothari, Ninad
- Biotechnology for Biofuels, Vol. 12, Issue 1
Characterization of a leukocidin identified in Staphylococcus pseudintermedius
journal, September 2018
- Abouelkhair, Mohamed A.; Bemis, David A.; Giannone, Richard J.
- PLOS ONE, Vol. 13, Issue 9
The Cellulosome Paradigm in An Extreme Alkaline Environment
journal, September 2019
- Phitsuwan,
- Microorganisms, Vol. 7, Issue 9