Dramatic performance of Clostridium thermocellum explained by its wide range of cellulase modalities

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.; Hettich, Robert L.; Brown, Steven D.; Lynd, Lee R.; Bayer, Edward A.; Himmel, Michael E.; Bomble, Yannick J.

doi:10.1126/sciadv.1501254

Dramatic performance of Clostridium thermocellum explained by its wide range of cellulase modalities

Journal Article · Fri Feb 05 00:00:00 EST 2016 · Science Advances

DOI:https://doi.org/10.1126/sciadv.1501254· OSTI ID:1244830

Xu, Qi ^[1]; Resch, Michael G. ^[2]; Podkaminer, Kara ^[1]; Yang, Shihui ^[3]; Baker, John O. ^[1]; Donohoe, Bryon S. ^[1]; Wilson, Charlotte ^[4]; Klingeman, Dawn M. ^[4]; Olson, Daniel G. ^[5]; Decker, Stephen R. ^[1]; Hettich, Robert L. ^[4]; Brown, Steven D. ^[4]; Lynd, Lee R. ^[5]; Bayer, Edward A. ^[6]; Himmel, Michael E. ^[1]; Bomble, Yannick J. ^[1]

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)

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. As a result, 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.

View Accepted Manuscript (DOE)

Research Organization:: National Renewable Energy Lab. (NREL), Golden, CO (United States); Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center (BESC)

Sponsoring Organization:: USDOE Bioenergy Science Center (BESC); USDOE Office of Science (SC)

Grant/Contract Number:: AC05-00OR22725; AC36-08GO28308

OSTI ID:: 1244830

Alternate ID(s):: OSTI ID: 1286890

Report Number(s):: NREL/JA--2700-65384

Journal Information:: Science Advances, Journal Name: Science Advances Journal Issue: 2 Vol. 2; ISSN 2375-2548

Publisher:: AAASCopyright Statement

Country of Publication:: United States

Language:: English

References (52)

Cellulosomes—Structure and Ultrastructure Bayer, Edward A.; Shimon, Linda J. W.; Shoham, Yuval Journal of Structural Biology, Vol. 124, Issue 2-3 https://doi.org/10.1006/jsbi.1998.4065	journal	December 1998
A defined growth medium with very low background carbon for culturing Clostridium thermocellum Holwerda, Evert K.; Hirst, Kyle D.; Lynd, Lee R. Journal of Industrial Microbiology & Biotechnology, Vol. 39, Issue 6 https://doi.org/10.1007/s10295-012-1091-3	journal	February 2012
Comparison of different mechanical refining technologies on the enzymatic digestibility of low severity acid pretreated corn stover Chen, Xiaowen; Kuhn, Erik; Wang, Wei Bioresource Technology, Vol. 147 https://doi.org/10.1016/j.biortech.2013.07.109	journal	November 2013
Natural paradigms of plant cell wall degradation Wei, Hui; Xu, Qi; Taylor, Larry E. Current Opinion in Biotechnology, Vol. 20, Issue 3 https://doi.org/10.1016/j.copbio.2009.05.008	journal	June 2009
The cellulosome of Clostridium cellulolyticum Desvaux, Mickaël Enzyme and Microbial Technology, Vol. 37, Issue 4 https://doi.org/10.1016/j.enzmictec.2004.04.025	journal	September 2005
Cellulose, cellulases and cellulosomes Bayer, Edward A.; Chanzy, Henri; Lamed, Raphael Current Opinion in Structural Biology, Vol. 8, Issue 5 https://doi.org/10.1016/s0959-440x(98)80143-7	journal	October 1998
MyriMatch: Highly Accurate Tandem Mass Spectral Peptide Identification by Multivariate Hypergeometric Analysis Tabb, David L.; Fernando, Christopher G.; Chambers, Matthew C. Journal of Proteome Research, Vol. 6, Issue 2 https://doi.org/10.1021/pr0604054	journal	February 2007
IDPicker 2.0: Improved Protein Assembly with High Discrimination Peptide Identification Filtering Ma, Ze-Qiang; Dasari, Surendra; Chambers, Matthew C. Journal of Proteome Research, Vol. 8, Issue 8 https://doi.org/10.1021/pr900360j	journal	August 2009
Cellulosomes: plant-cell-wall-degrading enzyme complexes Doi, Roy H.; Kosugi, Akihiko Nature Reviews Microbiology, Vol. 2, Issue 7 https://doi.org/10.1038/nrmicro925	journal	July 2004
DAnTE: a statistical tool for quantitative analysis of -omics data Polpitiya, A. D.; Qian, W. -J.; Jaitly, N. Bioinformatics, Vol. 24, Issue 13 https://doi.org/10.1093/bioinformatics/btn217	journal	May 2008
DanteR: an extensible R-based tool for quantitative analysis of -omics data Taverner, Tom; Karpievitch, Yuliya V.; Polpitiya, Ashoka D. Bioinformatics, Vol. 28, Issue 18 https://doi.org/10.1093/bioinformatics/bts449	journal	July 2012
Protease inhibitors in bacteria: an emerging concept for the regulation of bacterial protein complexes? Schwarz, Wolfgang H.; Zverlov, Vladimir V. Molecular Microbiology, Vol. 60, Issue 6 https://doi.org/10.1111/j.1365-2958.2006.05181.x	journal	June 2006
Biomass Recalcitrance: Engineering Plants and Enzymes for Biofuels Production Himmel, M. E.; Ding, S.-Y.; Johnson, D. K. Science, Vol. 315, Issue 5813, p. 804-807 https://doi.org/10.1126/science.1137016	journal	February 2007
High Ethanol Titers from Cellulose by Using Metabolically Engineered Thermophilic, Anaerobic Microbes Argyros, D. Aaron; Tripathi, Shital A.; Barrett, Trisha F. Applied and Environmental Microbiology, Vol. 77, Issue 23, p. 8288-8294 https://doi.org/10.1128/aem.00646-11	journal	September 2011
Global Gene Expression Patterns in Clostridium thermocellum as Determined by Microarray Analysis of Chemostat Cultures on Cellulose or Cellobiose Riederer, Allison; Takasuka, Taichi E.; Makino, Shin-ichi Applied and Environmental Microbiology, Vol. 77, Issue 4 https://doi.org/10.1128/aem.02008-10	journal	December 2010
The Cellulosome System of Acetivibrio cellulolyticus Includes a Novel Type of Adaptor Protein and a Cell Surface Anchoring Protein Xu, Q.; Gao, W.; Ding, S. -Y. Journal of Bacteriology, Vol. 185, Issue 15 https://doi.org/10.1128/jb.185.15.4548-4557.2003	journal	July 2003
A Novel Acetivibrio cellulolyticus Anchoring Scaffoldin That Bears Divergent Cohesins Xu, Q.; Barak, Y.; Kenig, R. Journal of Bacteriology, Vol. 186, Issue 17 https://doi.org/10.1128/jb.186.17.5782-5789.2004	journal	August 2004
Architecture of the Bacteroides cellulosolvens Cellulosome: Description of a Cell Surface-Anchoring Scaffoldin and a Family 48 Cellulase Xu, Q.; Bayer, E. A.; Goldman, M. Journal of Bacteriology, Vol. 186, Issue 4 https://doi.org/10.1128/jb.186.4.968-977.2004	journal	February 2004
The Cellulosomes: Multienzyme Machines for Degradation of Plant Cell Wall Polysaccharides Bayer, Edward A.; Belaich, Jean-Pierre; Shoham, Yuval Annual Review of Microbiology, Vol. 58, Issue 1 https://doi.org/10.1146/annurev.micro.57.030502.091022	journal	October 2004
Genome-wide analysis of Acetivibrio cellulolyticus provides a blueprint of an elaborate cellulosome system Dassa, Bareket; Borovok, Ilya; Lamed, Raphael BMC Genomics, Vol. 13, Issue 1 https://doi.org/10.1186/1471-2164-13-210	journal	January 2012
Clostridium thermocellum ATCC27405 transcriptomic, metabolomic and proteomic profiles after ethanol stress Yang, Shihui; Giannone, Richard J.; Dice, Lezlee BMC Genomics, Vol. 13, Issue 1 https://doi.org/10.1186/1471-2164-13-336	journal	January 2012
Improving activity of minicellulosomes by integration of intra- and intermolecular synergies Xu, Qi; Ding, Shi-You; Brunecky, Roman Biotechnology for Biofuels, Vol. 6, Issue 1 https://doi.org/10.1186/1754-6834-6-126	journal	January 2013
Clostridium thermocellum transcriptomic profiles after exposure to furfural or heat stress Wilson, Charlotte M.; Yang, Shihui; Rodriguez, Miguel Biotechnology for Biofuels, Vol. 6, Issue 1 https://doi.org/10.1186/1754-6834-6-131	journal	January 2013
Global transcriptome analysis of Clostridium thermocellum ATCC 27405 during growth on dilute acid pretreated Populus and switchgrass Wilson, Charlotte M.; Rodriguez, Miguel; Johnson, Courtney M. Biotechnology for Biofuels, Vol. 6, Issue 1 https://doi.org/10.1186/1754-6834-6-179	journal	January 2013
Cellulosomics of the cellulolytic thermophile Clostridium clariflavum Artzi, Lior; Dassa, Bareket; Borovok, Ilya Biotechnology for Biofuels, Vol. 7, Issue 1 https://doi.org/10.1186/1754-6834-7-100	journal	January 2014
Comparison of single-molecule sequencing and hybrid approaches for finishing the genome of Clostridium autoethanogenum and analysis of CRISPR systems in industrial relevant Clostridia Brown, Steven D.; Nagaraju, Shilpa; Utturkar, Sagar Biotechnology for Biofuels, Vol. 7, Issue 1 https://doi.org/10.1186/1754-6834-7-40	journal	January 2014
The contribution of cellulosomal scaffoldins to cellulose hydrolysis by Clostridium thermocellum analyzed by using thermotargetrons Hong, Wei; Zhang, Jie; Feng, Yingang Biotechnology for Biofuels, Vol. 7, Issue 1 https://doi.org/10.1186/1754-6834-7-80	journal	January 2014
Biological lignocellulose solubilization: comparative evaluation of biocatalysts and enhancement via cotreatment Paye, Julie M. D.; Guseva, Anna; Hammer, Sarah K. Biotechnology for Biofuels, Vol. 9, Issue 1 https://doi.org/10.1186/s13068-015-0412-y	journal	January 2016
Impact of Pretreated Switchgrass and Biomass Carbohydrates on Clostridium thermocellum ATCC 27405 Cellulosome Composition: A Quantitative Proteomic Analysis Raman, Babu; Pan, Chongle; Hurst, Gregory B. PLoS ONE, Vol. 4, Issue 4, Article No. e5271 https://doi.org/10.1371/journal.pone.0005271	journal	April 2009
Elaborate cellulosome architecture of Acetivibrio cellulolyticus revealed by selective screening of cohesin–dockerin interactions Hamberg, Yuval; Ruimy-Israeli, Vered; Dassa, Bareket PeerJ, Vol. 2 https://doi.org/10.7717/peerj.636	journal	January 2014
Major characteristics of the cellulolytic system of Clostridium thermocellum coincide with those of the purified cellulosome Lamed, Raphael; Kenig, Rina; Setter, Eva Enzyme and Microbial Technology, Vol. 7, Issue 1 https://doi.org/10.1016/0141-0229(85)90008-0	journal	January 1985
Transformation of Clostridium Thermocellum by Electroporation Olson, Daniel G.; Lynd, Lee R. Cellulases https://doi.org/10.1016/B978-0-12-415931-0.00017-3	book	January 2012
Cellulose, cellulases and cellulosomes Bayer, Edward A.; Chanzy, Henri; Lamed, Raphael Current Opinion in Structural Biology, Vol. 8, Issue 5 https://doi.org/10.1016/S0959-440X(98)80143-7	journal	October 1998
Fungal cellulases and complexed cellulosomal enzymes exhibit synergistic mechanisms in cellulose deconstruction Resch, Michael G.; Donohoe, Bryon S.; Baker, John O. Energy & Environmental Science, Vol. 6, Issue 6 https://doi.org/10.1039/c3ee00019b	journal	January 2013
Clostridium thermocellum cellulosomal genes are regulated by extracytoplasmic polysaccharides via alternative sigma factors Nataf, Y.; Bahari, L.; Kahel-Raifer, H. Proceedings of the National Academy of Sciences, Vol. 107, Issue 43 https://doi.org/10.1073/pnas.1012175107	journal	October 2010
Identification of a region responsible for binding to the cell wall within the S-layer protein of Clostridium thermocellum Lemaire, M.; Miras, I.; Gounon, P. Microbiology, Vol. 144, Issue 1 https://doi.org/10.1099/00221287-144-1-211	journal	January 1998
Thermophilic lignocellulose deconstruction Blumer-Schuette, Sara E.; Brown, Steven D.; Sander, Kyle B. FEMS Microbiology Reviews, Vol. 38, Issue 3 https://doi.org/10.1111/1574-6976.12044	journal	May 2014
The functional repertoire of prokaryote cellulosomes includes the serpin superfamily of serine proteinase inhibitors Kang, Seungha; Barak, Yoav; Lamed, Raphael Molecular Microbiology, Vol. 60, Issue 6 https://doi.org/10.1111/j.1365-2958.2006.05182.x	journal	June 2006
High Ethanol Titers from Cellulose by Using Metabolically Engineered Thermophilic, Anaerobic Microbes Argyros, D. Aaron; Tripathi, Shital A.; Barrett, Trisha F. Applied and Environmental Microbiology, Vol. 77, Issue 23, p. 8288-8294 https://doi.org/10.1128/AEM.00646-11	journal	September 2011
Global Gene Expression Patterns in Clostridium thermocellum as Determined by Microarray Analysis of Chemostat Cultures on Cellulose or Cellobiose Riederer, Allison; Takasuka, Taichi E.; Makino, Shin-ichi Applied and Environmental Microbiology, Vol. 77, Issue 4 https://doi.org/10.1128/AEM.02008-10	journal	December 2010
Mutations in the Scaffoldin Gene, cipA, of Clostridium thermocellum with Impaired Cellulosome Formation and Cellulose Hydrolysis: Insertions of a New Transposable Element, IS1447, and Implications for Cellulase Synergism on Crystalline Cellulose Zverlov, V. V.; Klupp, M.; Krauss, J. Journal of Bacteriology, Vol. 190, Issue 12 https://doi.org/10.1128/JB.00097-08	journal	April 2008
Caldicellulosiruptor Core and Pangenomes Reveal Determinants for Noncellulosomal Thermophilic Deconstruction of Plant Biomass Blumer-Schuette, S. E.; Giannone, R. J.; Zurawski, J. V. Journal of Bacteriology, Vol. 194, Issue 15 https://doi.org/10.1128/JB.00266-12	journal	May 2012
Cellodextrin and Laminaribiose ABC Transporters in Clostridium thermocellum Nataf, Y.; Yaron, S.; Stahl, F. Journal of Bacteriology, Vol. 191, Issue 1 https://doi.org/10.1128/JB.01190-08	journal	October 2008
Role of the CipA Scaffoldin Protein in Cellulose Solubilization, as Determined by Targeted Gene Deletion and Complementation in Clostridium thermocellum Olson, D. G.; Giannone, R. J.; Hettich, R. L. Journal of Bacteriology, Vol. 195, Issue 4 https://doi.org/10.1128/JB.02014-12	journal	November 2012
Distinct Affinity of Binding Sites for S-Layer Homologous Domains in Clostridium thermocellum and Bacillus anthracis Cell Envelopes Chauvaux, Sylvie; Matuschek, Markus; Beguin, Pierre Journal of Bacteriology, Vol. 181, Issue 8 https://doi.org/10.1128/JB.181.8.2455-2458.1999	journal	April 1999
The Cellulosome System of Acetivibrio cellulolyticus Includes a Novel Type of Adaptor Protein and a Cell Surface Anchoring Protein Xu, Q.; Gao, W.; Ding, S. -Y. Journal of Bacteriology, Vol. 185, Issue 15 https://doi.org/10.1128/JB.185.15.4548-4557.2003	journal	July 2003
A Novel Acetivibrio cellulolyticus Anchoring Scaffoldin That Bears Divergent Cohesins Xu, Q.; Barak, Y.; Kenig, R. Journal of Bacteriology, Vol. 186, Issue 17 https://doi.org/10.1128/JB.186.17.5782-5789.2004	journal	August 2004
Architecture of the Bacteroides cellulosolvens Cellulosome: Description of a Cell Surface-Anchoring Scaffoldin and a Family 48 Cellulase Xu, Q.; Bayer, E. A.; Goldman, M. Journal of Bacteriology, Vol. 186, Issue 4 https://doi.org/10.1128/JB.186.4.968-977.2004	journal	February 2004
Microbial Cellulose Utilization: Fundamentals and Biotechnology Lynd, L. R.; Weimer, P. J.; van Zyl, W. H. Microbiology and Molecular Biology Reviews, Vol. 66, Issue 3, p. 506-577 https://doi.org/10.1128/MMBR.66.3.506-577.2002	journal	September 2002
A conserved motif in S-layer proteins is involved in peptidoglycan binding in Thermus thermophilus. Olabarría, G.; Carrascosa, J. L.; de Pedro, M. A. Journal of Bacteriology, Vol. 178, Issue 16 https://doi.org/10.1128/jb.178.16.4765-4772.1996	journal	August 1996
Microbial enzyme systems for biomass conversion: emerging paradigms Himmel, Michael E.; Xu, Qi; Luo, Yonghua Biofuels, Vol. 1, Issue 2 https://doi.org/10.4155/bfs.09.25	journal	March 2010
Biological lignocellulose solubilization: comparative evaluation of biocatalysts and enhancement via cotreatment [Supplemental Data] Paye, Julie; Guseva, Anna; Hammer, Sarah figshare-Supplementary information for journal article at DOI: 10.1186/s13068-015-0412-y, 1 DOCX file (5.42 MB) https://doi.org/10.6084/m9.figshare.c.3609365	figure	January 2016

Cited By (28)

Specialized activities and expression differences for Clostridium thermocellum biofilm and planktonic cells Dumitrache, Alexandru; Klingeman, Dawn M.; Natzke, Jace Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/srep43583	journal	February 2017
Inducing effects of cellulosic hydrolysate components of lignocellulose on cellulosome synthesis in Clostridium thermocellum Li, Renmin; Feng, Yingang; Liu, Shiyue Microbial Biotechnology, Vol. 11, Issue 5 https://doi.org/10.1111/1751-7915.13293	journal	June 2018
Simultaneous achievement of high ethanol yield and titer in Clostridium thermocellum Tian, Liang; Papanek, Beth; Olson, Daniel G. Biotechnology for Biofuels, Vol. 9, Issue 1 https://doi.org/10.1186/s13068-016-0528-8	journal	June 2016
Integrated omics analyses reveal the details of metabolic adaptation of Clostridium thermocellum to lignocellulose-derived growth inhibitors released during the deconstruction of switchgrass Poudel, Suresh; Giannone, Richard J.; Rodriguez, Miguel Biotechnology for Biofuels, Vol. 10, Issue 1 https://doi.org/10.1186/s13068-016-0697-5	journal	January 2017
Cellulosic ethanol production via consolidated bioprocessing by a novel thermophilic anaerobic bacterium isolated from a Himalayan hot spring Singh, Nisha; Mathur, Anshu S.; Tuli, Deepak K. Biotechnology for Biofuels, Vol. 10, Issue 1 https://doi.org/10.1186/s13068-017-0756-6	journal	March 2017
Efficient whole-cell-catalyzing cellulose saccharification using engineered Clostridium thermocellum Zhang, Jie; Liu, Shiyue; Li, Renmin Biotechnology for Biofuels, Vol. 10, Issue 1 https://doi.org/10.1186/s13068-017-0796-y	journal	May 2017
The LacI family protein GlyR3 co-regulates the celC operon and manB in Clostridium thermocellum Choi, Jinlyung; Klingeman, Dawn M.; Brown, Steven D. Biotechnology for Biofuels, Vol. 10, Issue 1 https://doi.org/10.1186/s13068-017-0849-2	journal	June 2017
Adding tetrahydrofuran to dilute acid pretreatment provides new insights into substrate changes that greatly enhance biomass deconstruction by Clostridium thermocellum and fungal enzymes Thomas, Vanessa A.; Donohoe, Bryon S.; Li, Mi Biotechnology for Biofuels, Vol. 10, Issue 1 https://doi.org/10.1186/s13068-017-0937-3	journal	November 2017
Clostridium thermocellum LL1210 pH homeostasis mechanisms informed by transcriptomics and metabolomics Whitham, Jason M.; Moon, Ji-Won; Rodriguez, Miguel Biotechnology for Biofuels, Vol. 11, Issue 1 https://doi.org/10.1186/s13068-018-1095-y	journal	April 2018
An iterative computational design approach to increase the thermal endurance of a mesophilic enzyme Sammond, Deanne W.; Kastelowitz, Noah; Donohoe, Bryon S. Biotechnology for Biofuels, Vol. 11, Issue 1 https://doi.org/10.1186/s13068-018-1178-9	journal	July 2018
Multiple levers for overcoming the recalcitrance of lignocellulosic biomass Holwerda, Evert K.; Worthen, Robert S.; Kothari, Ninad Biotechnology for Biofuels, Vol. 12, Issue 1 https://doi.org/10.1186/s13068-019-1353-7	journal	January 2019
Characterization of a leukocidin identified in Staphylococcus pseudintermedius Abouelkhair, Mohamed A.; Bemis, David A.; Giannone, Richard J. PLOS ONE, Vol. 13, Issue 9 https://doi.org/10.1371/journal.pone.0204450	journal	September 2018
The Cellulosome Paradigm in An Extreme Alkaline Environment No authors listed Microorganisms, Vol. 7, Issue 9 https://doi.org/10.3390/microorganisms7090347	journal	September 2019
Genomics-informed isolation and characterization of a symbiotic Nanoarchaeota system from a terrestrial geothermal environment Wurch, Louie; Giannone, Richard J.; Belisle, Bernard S. Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms12115	journal	July 2016
Cellulosomes: bacterial nanomachines for dismantling plant polysaccharides Artzi, Lior; Bayer, Edward A.; Moraïs, Sarah Nature Reviews Microbiology, Vol. 15, Issue 2 https://doi.org/10.1038/nrmicro.2016.164	journal	December 2016
Structural basis of cell wall anchoring by SLH domains in Paenibacillus alvei Blackler, Ryan J.; López-Guzmán, Arturo; Hager, Fiona F. Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-05471-3	journal	August 2018
Identification of endoxylanase XynE from Clostridium thermocellum as the first xylanase of glycoside hydrolase family GH141 Heinze, Simon; Mechelke, Matthias; Kornberger, Petra Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-11598-y	journal	September 2017
Regulation of biomass degradation by alternative σ factors in cellulolytic clostridia Ortiz de Ora, Lizett; Lamed, Raphael; Liu, Ya-Jun Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-29245-5	journal	July 2018
Cellulosomes localise on the surface of membrane vesicles from the cellulolytic bacterium Clostridium thermocellum Ichikawa, Shunsuke; Ogawa, Satoru; Nishida, Ayami FEMS Microbiology Letters, Vol. 366, Issue 12 https://doi.org/10.1093/femsle/fnz145	journal	June 2019
Unique genetic cassettes in a Thermoanaerobacterium contribute to simultaneous conversion of cellulose and monosugars into butanol Li, Tinggang; Zhang, Chen; Yang, Kun-Lin Science Advances, Vol. 4, Issue 3 https://doi.org/10.1126/sciadv.1701475	journal	March 2018
The effects of micronutrient deficiencies on bacterial species from the human gut microbiota Hibberd, Matthew C.; Wu, Meng; Rodionov, Dmitry A. Science Translational Medicine, Vol. 9, Issue 390 https://doi.org/10.1126/scitranslmed.aal4069	journal	May 2017
Spatial Distribution and Diverse Metabolic Functions of Lignocellulose-Degrading Uncultured Bacteria as Revealed by Genome-Centric Metagenomics Kougias, Panagiotis G.; Campanaro, Stefano; Treu, Laura Applied and Environmental Microbiology, Vol. 84, Issue 18 https://doi.org/10.1128/aem.01244-18	journal	July 2018
Temporal proteome dynamics of Clostridium cellulovorans cultured with major plant cell wall polysaccharides Aburaya, Shunsuke; Aoki, Wataru; Kuroda, Kouichi BMC Microbiology, Vol. 19, Issue 1 https://doi.org/10.1186/s12866-019-1480-0	journal	June 2019
Unique organization and unprecedented diversity of the Bacteroides (Pseudobacteroides) cellulosolvens cellulosome system Zhivin, Olga; Dassa, Bareket; Moraïs, Sarah Biotechnology for Biofuels, Vol. 10, Issue 1 https://doi.org/10.1186/s13068-017-0898-6	journal	September 2017
How does cellulosome composition influence deconstruction of lignocellulosic substrates in Clostridium (Ruminiclostridium) thermocellum DSM 1313? Yoav, Shahar; Barak, Yoav; Shamshoum, Melina Biotechnology for Biofuels, Vol. 10, Issue 1 https://doi.org/10.1186/s13068-017-0909-7	journal	September 2017
Optimizing the composition of a synthetic cellulosome complex for the hydrolysis of softwood pulp: identification of the enzymatic core functions and biochemical complex characterization Leis, Benedikt; Held, Claudia; Andreeßen, Björn Biotechnology for Biofuels, Vol. 11, Issue 1 https://doi.org/10.1186/s13068-018-1220-y	journal	August 2018
Unraveling essential cellulosomal components of the (Pseudo)Bacteroides cellulosolvens reveals an extensive reservoir of novel catalytic enzymes Zhivin-Nissan, Olga; Dassa, Bareket; Morag, Ely Biotechnology for Biofuels, Vol. 12, Issue 1 https://doi.org/10.1186/s13068-019-1447-2	journal	May 2019
Substrate-Related Factors Affecting Cellulosome-Induced Hydrolysis for Lignocellulose Valorization Wang, Ying; Leng, Ling; Islam, Md Khairul International Journal of Molecular Sciences, Vol. 20, Issue 13 https://doi.org/10.3390/ijms20133354	journal	July 2019

Similar Records

Contribution of Scaffoldins to Biomass Degradation by Clostridium Thermocellum: The Effect of Scaffoldin-Deletions on Expression of Other Genes

Conference · Mon Apr 28 00:00:00 EDT 2014 · OSTI ID:1259806

Insights into Higher-Order Organization of the Cellulosome Revealed by a Dissect-and build Approach: Crystal Structure of Interacting Clostridium thermocellum Multimodular components

Journal Article · Fri Dec 30 23:00:00 EST 2011 · Journal of Molecular Biology · OSTI ID:1041878

Related Subjects

09 BIOMASS FUELS
59 BASIC BIOLOGICAL SCIENCES
60 APPLIED LIFE SCIENCES
biofuels
biomass
cell biology
cellulases
cellulosomes

Dramatic performance of Clostridium thermocellum explained by its wide range of cellulase modalities

Citation Formats

References (52)

Cited By (28)

Similar Records

Related Subjects