Discrete and Structurally Unique Proteins (T$\bar{a}$pirins) Mediate Attachment of Extremely Thermophilic Caldicellulosiruptor Species to Cellulose

Blumer-Schuette, S. E.; Alahuhta, M.; Conway, J. M.; Lee, L. L.; Zurawski, J. V.; Giannone, Richard J.; Hettich, R. L.; Lunin, V. V.; HImmel, M. E.; Kelly, R. M.

doi:10.1074/jbc.M115.641480

Discrete and Structurally Unique Proteins (T$$\bar{a}$$pirins) Mediate Attachment of Extremely Thermophilic Caldicellulosiruptor Species to Cellulose

Journal Article · Fri Apr 24 00:00:00 EDT 2015 · Journal of Biological Chemistry

DOI:https://doi.org/10.1074/jbc.M115.641480· OSTI ID:1220749

Blumer-Schuette, S. E. ^[1]; Alahuhta, M. ^[2]; Conway, J. M. ^[1]; Lee, L. L. ^[1]; Zurawski, J. V. ^[1]; Giannone, Richard J. ^[3]; Hettich, R. L. ^[3]; Lunin, V. V. ^[2]; HImmel, M. E. ^[2]; Kelly, R. M. ^[1]

North Carolina State Univ., Raleigh, NC (United States). Dept. of Chemical and Biomolecular Engineering
National Renewable Energy Lab. (NREL), Golden, CO (United States). Biosciences Center
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Division

A variety of catalytic and noncatalytic protein domains are deployed by select microorganisms to deconstruct lignocellulose. These extracellular proteins are used to attach to, modify, and hydrolyze the complex polysaccharides present in plant cell walls. Cellulolytic enzymes, often containing carbohydrate-binding modules, are key to this process; however, these enzymes are not solely responsible for attachment. Few mechanisms of attachment have been discovered among bacteria that do not form large polypeptide structures, called cellulosomes, to deconstruct biomass. In this study, bioinformatics and proteomics analyses identified unique, discrete, hypothetical proteins (“t$$\bar{a}$$pirins,” origin from M$$\bar{a}$$ori: to join), not directly associated with cellulases, that mediate attachment to cellulose by species in the noncellulosomal, extremely thermophilic bacterial genus Caldicellulosiruptor. Two t$$\bar{a}$$pirin genes are located directly downstream of a type IV pilus operon in strongly cellulolytic members of the genus, whereas homologs are absent from the weakly cellulolytic Caldicellulosiruptor species. Based on their amino acid sequence, t$$\bar{a}$$pirins are specific to these extreme thermophiles. T$$\bar{a}$$pirins are also unusual in that they share no detectable protein domain signatures with known polysaccharide-binding proteins. Adsorption isotherm and trans vivo analyses demonstrated the carbohydrate-binding module-like affinity of the t$$\bar{a}$$pirins for cellulose. Crystallization of a cellulose-binding truncation from one t$$\bar{a}$$pirin indicated that these proteins form a long β-helix core with a shielded hydrophobic face. In addition, they are structurally unique and define a new class of polysaccharide adhesins. Strongly cellulolytic Caldicellulosiruptor species employ t$$\bar{a}$$pirins to complement substrate-binding proteins from the ATP-binding cassette transporters and multidomain extracellular and S-layer-associated glycoside hydrolases to process the carbohydrate content of lignocellulose.

View Accepted Manuscript (DOE)

Research Organization:: NREL (National Renewable Energy Laboratory (NREL), Golden, CO (United States))

Sponsoring Organization:: USDOE Office of Science (SC)

OSTI ID:: 1220749

Alternate ID(s):: OSTI ID: 1286760

Report Number(s):: NREL/JA--2700-64273

Journal Information:: Journal of Biological Chemistry, Journal Name: Journal of Biological Chemistry Journal Issue: 17 Vol. 290; ISSN 0021-9258

Publisher:: American Society for Biochemistry and Molecular BiologyCopyright Statement

Country of Publication:: United States

Language:: English

References (76)

Glycoside hydrolase inventory drives plant polysaccharide deconstruction by the extremely thermophilic bacterium Caldicellulosiruptor saccharolyticus VanFossen, Amy L.; Ozdemir, Inci; Zelin, Samantha L. Biotechnology and Bioengineering, Vol. 108, Issue 7 https://doi.org/10.1002/bit.23093	journal	March 2011
Predicting transmembrane protein topology with a hidden markov model: application to complete genomes11Edited by F. Cohen Krogh, Anders; Larsson, Björn; von Heijne, Gunnar Journal of Molecular Biology, Vol. 305, Issue 3 https://doi.org/10.1006/jmbi.2000.4315	journal	January 2001
celA, another gene coding for a multidomain cellulase from the extreme thermophile Caldocellum saccharolyticum Te'o, V. S. J.; Saul, D. J.; Bergquist, P. L. Applied Microbiology and Biotechnology, Vol. 43, Issue 2 https://doi.org/10.1007/BF00172827	journal	June 1995
Characterization of a spontaneous adhesion-defective mutant of Ruminococcus albus strain 20 Mosoni, Pascale; Gaillard-Martinie, Brigitte Archives of Microbiology, Vol. 176, Issue 1-2 https://doi.org/10.1007/s002030100292	journal	July 2001
celA, another gene coding for a multidomain cellulase from the extreme thermophile Caldocellum saccharolyticum Te'o, V. S. J.; Saul, D. J.; Bergquist, P. L. Applied Microbiology and Biotechnology, Vol. 43, Issue 2 https://doi.org/10.1007/s002530050405	journal	May 1995
Multidomain and Multifunctional Glycosyl Hydrolases from the Extreme Thermophile Caldicellulosiruptor Isolate Tok7B.1 Gibbs, Moreland D.; Reeves, Rosalind A.; Farrington, G. King Current Microbiology, Vol. 40, Issue 5, p. 333-340 https://doi.org/10.1007/s002849910066	journal	May 2000
Precise excision of the cellulose binding domains from two Cellulomonas fimi cellulases by a homologous protease and the effect on catalysis. Gilkes, N. R.; Warren, R. A.; Miller, R. C. Journal of Biological Chemistry, Vol. 263, Issue 21 https://doi.org/10.1016/S0021-9258(19)81530-2	journal	July 1988
Characterization and affinity applications of cellulose-binding domains Tomme, Peter; Boraston, Al; McLean, Brad Journal of Chromatography B: Biomedical Sciences and Applications, Vol. 715, Issue 1 https://doi.org/10.1016/S0378-4347(98)00053-X	journal	September 1998
Construction of engineered yeast with the ability of binding to cellulose Nam, Jin-Min; Fujita, Yasuya; Arai, Terukazu Journal of Molecular Catalysis B: Enzymatic, Vol. 17, Issue 3-5 https://doi.org/10.1016/S1381-1177(02)00028-0	journal	June 2002
Cellulosic ethanol production by combination of cellulase-displaying yeast cells Baek, Seung-Ho; Kim, Sujin; Lee, Kyusung Enzyme and Microbial Technology, Vol. 51, Issue 6-7 https://doi.org/10.1016/j.enzmictec.2012.08.005	journal	December 2012
A novel family of carbohydrate-binding modules identified with Ruminococcus albus proteins Xu, Qi; Morrison, Mark; Nelson, Karen E. FEBS Letters, Vol. 566, Issue 1-3 https://doi.org/10.1016/j.febslet.2004.04.005	journal	April 2004
Mining metagenomic data for novel domains: BACON, a new carbohydrate-binding module Mello, Luciane V.; Chen, Xin; Rigden, Daniel J. FEBS Letters, Vol. 584, Issue 11 https://doi.org/10.1016/j.febslet.2010.04.045	journal	April 2010
Highly Stable Binding Proteins Derived from the Hyperthermophilic Sso7d Scaffold Gera, Nimish; Hussain, Mahmud; Wright, Robert C. Journal of Molecular Biology, Vol. 409, Issue 4 https://doi.org/10.1016/j.jmb.2011.04.020	journal	June 2011
Protocols for production of selenomethionine-labeled proteins in 2-L polyethylene terephthalate bottles using auto-induction medium Sreenath, Hassan K.; Bingman, Craig A.; Buchan, Blake W. Protein Expression and Purification, Vol. 40, Issue 2 https://doi.org/10.1016/j.pep.2004.12.022	journal	April 2005
Protein production by auto-induction in high-density shaking cultures Studier, F. William Protein Expression and Purification, Vol. 41, Issue 1, p. 207-234 https://doi.org/10.1016/j.pep.2005.01.016	journal	May 2005
Improvement of Cellulose-Degrading Ability of a Yeast Strain Displaying Trichoderma reesei Endoglucanase II by Recombination of Cellulose-Binding Domains Ito, J.; Fujita, Y.; Ueda, M. Biotechnology Progress, Vol. 20, Issue 3 https://doi.org/10.1021/bp034332u	journal	June 2004
Structure of Bordetella pertussis virulence factor P.69 pertactin Emsley, Paul; Charles, Ian G.; Fairweather, Neil F. Nature, Vol. 381, Issue 6577 https://doi.org/10.1038/381090a0	journal	May 1996
Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite Warnecke, Falk; Luginbühl, Peter; Ivanova, Natalia Nature, Vol. 450, Issue 7169 https://doi.org/10.1038/nature06269	journal	November 2007
Yeast surface display for screening combinatorial polypeptide libraries Boder, Eric T.; Wittrup, K. Dane Nature Biotechnology, Vol. 15, Issue 6 https://doi.org/10.1038/nbt0697-553	journal	June 1997
Automatic protein structure solution from weak X-ray data Skubák, Pavol; Pannu, Navraj S. Nature Communications, Vol. 4, Issue 1 https://doi.org/10.1038/ncomms3777	journal	November 2013
SignalP 4.0: discriminating signal peptides from transmembrane regions Petersen, Thomas Nordahl; Brunak, Søren; von Heijne, Gunnar Nature Methods, Vol. 8, Issue 10 https://doi.org/10.1038/nmeth.1701	journal	September 2011
In situ proteolysis for protein crystallization and structure determination Dong, Aiping; Xu, Xiaohui; Edwards, Aled M. Nature Methods, Vol. 4, Issue 12 https://doi.org/10.1038/nmeth1118	journal	November 2007
Carbohydrate-binding modules: fine-tuning polysaccharide recognition Boraston, Alisdair B.; Bolam, David N.; Gilbert, Harry J. Biochemical Journal, Vol. 382, Issue 3 https://doi.org/10.1042/BJ20040892	journal	September 2004
A hierarchical classification of polysaccharide lyases for glycogenomics Lombard, Vincent; Bernard, Thomas; Rancurel, Corinne Biochemical Journal, Vol. 432, Issue 3 https://doi.org/10.1042/BJ20101185	journal	November 2010
The crystal structure of filamentous hemagglutinin secretion domain and its implications for the two-partner secretion pathway Clantin, B.; Hodak, H.; Willery, E. Proceedings of the National Academy of Sciences, Vol. 101, Issue 16 https://doi.org/10.1073/pnas.0400291101	journal	April 2004
Gene-centric metagenomics of the fiber-adherent bovine rumen microbiome reveals forage specific glycoside hydrolases Brulc, Jennifer M.; Antonopoulos, Dionysios A.; Berg Miller, Margret E. Proceedings of the National Academy of Sciences, Vol. 106, Issue 6 https://doi.org/10.1073/pnas.0806191105	journal	January 2009
Self-surface assembly of cellulosomes with two miniscaffoldins on Saccharomyces cerevisiae for cellulosic ethanol production Fan, L. -H.; Zhang, Z. -J.; Yu, X. -Y. Proceedings of the National Academy of Sciences, Vol. 109, Issue 33 https://doi.org/10.1073/pnas.1209856109	journal	August 2012
Structural basis for entropy-driven cellulose binding by a type-A cellulose-binding module (CBM) and bacterial expansin Georgelis, N.; Yennawar, N. H.; Cosgrove, D. J. Proceedings of the National Academy of Sciences, Vol. 109, Issue 37 https://doi.org/10.1073/pnas.1213200109	journal	August 2012
Characterization of a Double Cellulose-binding Domain: SYNERGISTIC HIGH AFFINITY BINDING TO CRYSTALLINE CELLULOSE Linder, Markus; Salovuori, Irma; Ruohonen, Laura Journal of Biological Chemistry, Vol. 271, Issue 35 https://doi.org/10.1074/jbc.271.35.21268	journal	August 1996
The Structure of the Haemophilus influenzae HMW1 Pro-piece Reveals a Structural Domain Essential for Bacterial Two-partner Secretion Yeo, Hye-Jeong; Yokoyama, Takeshi; Walkiewicz, Katarzyna Journal of Biological Chemistry, Vol. 282, Issue 42 https://doi.org/10.1074/jbc.M705750200	journal	August 2007
MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0 Tamura, Koichiro; Stecher, Glen; Peterson, Daniel Molecular Biology and Evolution, Vol. 30, Issue 12 https://doi.org/10.1093/molbev/mst197	journal	October 2013
MUSCLE: multiple sequence alignment with high accuracy and high throughput Edgar, R. C. Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797 https://doi.org/10.1093/nar/gkh340	journal	March 2004
The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics Cantarel, B. L.; Coutinho, P. M.; Rancurel, C. Nucleic Acids Research, Vol. 37, Issue Database https://doi.org/10.1093/nar/gkn663	journal	January 2009
Insights into plant biomass conversion from the genome of the anaerobic thermophilic bacterium Caldicellulosiruptor bescii DSM 6725 Dam, Phuongan; Kataeva, Irina; Yang, Sung-Jae Nucleic Acids Research, Vol. 39, Issue 8 https://doi.org/10.1093/nar/gkq1281	journal	January 2011
The InterPro protein families database: the classification resource after 15 years Mitchell, Alex; Chang, Hsin-Yu; Daugherty, Louise Nucleic Acids Research, Vol. 43, Issue D1 https://doi.org/10.1093/nar/gku1243	journal	November 2014
Adhesion to cellulose of the Gram-positive bacterium Ruminococcus albus involves type IV pili Rakotoarivonina, Harivony; Hebraud, Michel; Mosoni, Pascale Microbiology, Vol. 148, Issue 6 https://doi.org/10.1099/00221287-148-6-1871	journal	June 2002
Reclassification of Thermoanaerobium acetigenum as Caldicellulosiruptor acetigenus comb. nov. and emendation of the genus description Onyenwoke, R. U. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 56, Issue 6 https://doi.org/10.1099/ijs.0.63723-0	journal	June 2006
The Ruminococcus albus pilA1-pilA2 locus: expression and putative role of two adjacent pil genes in pilus formation and bacterial adhesion to cellulose Rakotoarivonina, H. Microbiology, Vol. 151, Issue 4 https://doi.org/10.1099/mic.0.27735-0	journal	April 2005
Phaser crystallographic software McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D. Journal of Applied Crystallography, Vol. 40, Issue 4 https://doi.org/10.1107/S0021889807021206	journal	July 2007
Accurate bond and angle parameters for X-ray protein structure refinement Engh, R. A.; Huber, R. Acta Crystallographica Section A Foundations of Crystallography, Vol. 47, Issue 4 https://doi.org/10.1107/S0108767391001071	journal	July 1991
Substructure search procedures for macromolecular structures Grosse-Kunstleve, R. W.; Adams, P. D. Acta Crystallographica Section D Biological Crystallography, Vol. 59, Issue 11 https://doi.org/10.1107/S0907444903018043	journal	October 2003
Simple algorithm for a maximum-likelihood SAD function McCoy, Airlie J.; Storoni, Laurent C.; Read, Randy J. Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 7 https://doi.org/10.1107/S0907444904009990	journal	June 2004
Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions Krissinel, E.; Henrick, K. Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12 https://doi.org/10.1107/S0907444904026460	journal	November 2004
MolProbity : all-atom structure validation for macromolecular crystallography Chen, Vincent B.; Arendall, W. Bryan; Headd, Jeffrey J. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 1 https://doi.org/10.1107/S0907444909042073	journal	December 2009
Features and development of Coot Emsley, P.; Lohkamp, B.; Scott, W. G. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/S0907444910007493	journal	March 2010
Overview of the CCP 4 suite and current developments Winn, Martyn D.; Ballard, Charles C.; Cowtan, Kevin D. Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S0907444910045749	journal	March 2011
REFMAC 5 for the refinement of macromolecular crystal structures Murshudov, Garib N.; Skubák, Pavol; Lebedev, Andrey A. Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S0907444911001314	journal	March 2011
A new family of β-helix proteins with similarities to the polysaccharide lyases Close, Devin W.; D'Angelo, Sara; Bradbury, Andrew R. M. Acta Crystallographica Section D Biological Crystallography, Vol. 70, Issue 10 https://doi.org/10.1107/S1399004714015934	journal	September 2014
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 cellulose-binding domain of endoglucanase A (CenA) from Cellulomonas fimi: evidence for the involvement of tryptophan residues in binding Din, Neena; Forsythe, Ian J.; Burtnick, Leslie D. Molecular Microbiology, Vol. 11, Issue 4 https://doi.org/10.1111/j.1365-2958.1994.tb00352.x	journal	February 1994
Studies of the cellulolytic system of Trichoderma reesei QM 9414. Analysis of domain function in two cellobiohydrolases by limited proteolysis TOMME, Peter; TILBEURGH, Herman; PETTERSSON, Goran European Journal of Biochemistry, Vol. 170, Issue 3, p. 575-581 https://doi.org/10.1111/j.1432-1033.1988.tb13736.x	journal	January 1988
The modular cellulase CelZ of the thermophilic bacterium Clostridium stercorarium contains a thermostabilizing domain Riedel, Kathrin; Ritter, Johannes; Bauer, Stefan FEMS Microbiology Letters, Vol. 164, Issue 2 https://doi.org/10.1111/j.1574-6968.1998.tb13096.x	journal	July 1998
Metagenomic Discovery of Biomass-Degrading Genes and Genomes from Cow Rumen Hess, M.; Sczyrba, A.; Egan, R. Science, Vol. 331, Issue 6016 https://doi.org/10.1126/science.1200387	journal	January 2011
Revealing Nature's Cellulase Diversity The Digestion Mechanism of Caldicellulosiruptor bescii CelA Brunecky, R.; Alahuhta, M.; Xu, Q. Science, Vol. 342, Issue 6165, p. 1513-1516 https://doi.org/10.1126/science.1244273	journal	December 2013
Phylogenetic, Microbiological, and Glycoside Hydrolase Diversities within the Extremely Thermophilic, Plant Biomass-Degrading Genus Caldicellulosiruptor Blumer-Schuette, S. E.; Lewis, D. L.; Kelly, R. M. Applied and Environmental Microbiology, Vol. 76, Issue 24, p. 8084-8092 https://doi.org/10.1128/AEM.01400-10	journal	October 2010
Yeast Surface Display of Trifunctional Minicellulosomes for Simultaneous Saccharification and Fermentation of Cellulose to Ethanol Wen, F.; Sun, J.; Zhao, H. Applied and Environmental Microbiology, Vol. 76, Issue 4 https://doi.org/10.1128/AEM.01687-09	journal	December 2009
Surface Display of a Functional Minicellulosome by Intracellular Complementation Using a Synthetic Yeast Consortium and Its Application to Cellulose Hydrolysis and Ethanol Production Tsai, S. -L.; Goyal, G.; Chen, W. Applied and Environmental Microbiology, Vol. 76, Issue 22 https://doi.org/10.1128/AEM.01777-10	journal	October 2010
Carbohydrate Utilization Patterns for the Extremely Thermophilic Bacterium Caldicellulosiruptor saccharolyticus Reveal Broad Growth Substrate Preferences VanFossen, A. L.; Verhaart, M. R. A.; Kengen, S. M. W. Applied and Environmental Microbiology, Vol. 75, Issue 24 https://doi.org/10.1128/AEM.01959-09	journal	October 2009
S-Layer Homology Domain Proteins Csac_0678 and Csac_2722 Are Implicated in Plant Polysaccharide Deconstruction by the Extremely Thermophilic Bacterium Caldicellulosiruptor saccharolyticus Ozdemir, Inci; Blumer-Schuette, Sara E.; Kelly, Robert M. Applied and Environmental Microbiology, Vol. 78, Issue 3 https://doi.org/10.1128/AEM.07031-11	journal	December 2011
The beta-mannanase from "Caldocellum saccharolyticum" is part of a multidomain enzyme. Gibbs, M. D.; Saul, D. J.; Lüthi, E. Applied and Environmental Microbiology, Vol. 58, Issue 12 https://doi.org/10.1128/AEM.58.12.3864-3867.1992	journal	January 1992
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
Outer Membrane Proteins of Fibrobacter succinogenes with Potential Roles in Adhesion to Cellulose and in Cellulose Digestion Jun, H. -S.; Qi, M.; Gong, J. Journal of Bacteriology, Vol. 189, Issue 19 https://doi.org/10.1128/JB.00560-07	journal	July 2007
Cell Surface Enzyme Attachment Is Mediated by Family 37 Carbohydrate-Binding Modules, Unique to Ruminococcus albus Ezer, A.; Matalon, E.; Jindou, S. Journal of Bacteriology, Vol. 190, Issue 24 https://doi.org/10.1128/JB.00609-08	journal	October 2008
Extracellular Secretion of Noncatalytic Plant Cell Wall-Binding Proteins by the Cellulolytic Thermophile Caldicellulosiruptor bescii Yokoyama, H.; Yamashita, T.; Morioka, R. Journal of Bacteriology, Vol. 196, Issue 21 https://doi.org/10.1128/JB.01897-14	journal	August 2014
Adherence of the Gram-Positive BacteriumRuminococcus albus to Cellulose and Identification of a Novel Form of Cellulose-Binding Protein Which Belongs to the Pil Family of Proteins Pegden, Randall S.; Larson, Marilynn A.; Grant, Richard J. Journal of Bacteriology, Vol. 180, Issue 22 https://doi.org/10.1128/JB.180.22.5921-5927.1998	journal	November 1998
Cellulose-binding proteins of Fibrobacter succinogenes and the possible role of a 180-kDa cellulose-binding glycoprotein in adhesion to cellulose Gong, Jianhua; Egbosimba, Emmanuel E.; Forsberg, Cecil W. Canadian Journal of Microbiology, Vol. 42, Issue 5 https://doi.org/10.1139/m96-062	journal	May 1996
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
BLAST+: architecture and applications Camacho, Christiam; Coulouris, George; Avagyan, Vahram BMC Bioinformatics, Vol. 10, Issue 1 https://doi.org/10.1186/1471-2105-10-421	journal	January 2009
Structure- and context-based analysis of the GxGYxYP family reveals a new putative class of Glycoside Hydrolase Rigden, Daniel J.; Eberhardt, Ruth Y.; Gilbert, Harry J. BMC Bioinformatics, Vol. 15, Issue 1 https://doi.org/10.1186/1471-2105-15-196	journal	June 2014
How recombinant swollenin from Kluyveromyces lactis affects cellulosic substrates and accelerates their hydrolysis Jäger, Gernot; Girfoglio, Michele; Dollo, Florian Biotechnology for Biofuels, Vol. 4, Issue 1 https://doi.org/10.1186/1754-6834-4-33	journal	January 2011
fSpatial and temporal dynamics of cellulose degradation and biofilm formation by Caldicellulosiruptor obsidiansis and Clostridium thermocellum Wang, Zhi-Wu; Lee, Seung-Hwan; Elkins, James G. AMB Express, Vol. 1, Issue 1 https://doi.org/10.1186/2191-0855-1-30	journal	January 2011
Deletion of Caldicellulosiruptor besciiCelA reveals its crucial role in the deconstruction of lignocellulosic biomass Young, Jenna; Chung, Daehwan; Bomble, Yannick J. Biotechnology for Biofuels, Vol. 7, Issue 1 https://doi.org/10.1186/s13068-014-0142-6	journal	October 2014
Polysaccharide Degradation and Synthesis by Extremely Thermophilic Anaerobes VanFossen, Amy L.; Lewis, Derrick L.; Nichols, Jason D. Annals of the New York Academy of Sciences, Vol. 1125, Issue 1, p. 322-337 https://doi.org/10.1196/annals.1419.017	journal	March 2008
In Situ Proteolysis to Generate Crystals for Structure Determination: An Update Wernimont, Amy; Edwards, Aled PLoS ONE, Vol. 4, Issue 4 https://doi.org/10.1371/journal.pone.0005094	journal	April 2009
The Complete Genome Sequence of Fibrobacter succinogenes S85 Reveals a Cellulolytic and Metabolic Specialist Suen, Garret; Weimer, Paul J.; Stevenson, David M. PLoS ONE, Vol. 6, Issue 4 https://doi.org/10.1371/journal.pone.0018814	journal	April 2011
Expression of Cellulosome Components and Type IV Pili within the Extracellular Proteome of Ruminococcus flavefaciens 007 Vodovnik, Maša; Duncan, Sylvia H.; Reid, Martin D. PLoS ONE, Vol. 8, Issue 6 https://doi.org/10.1371/journal.pone.0065333	journal	June 2013

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