Multifunctional cellulase catalysis targeted by fusion to different carbohydrate-binding modules

Walker, Johnnie A.; Takasuka, Taichi E.; Deng, Kai; Bianchetti, Christopher M.; Udell, Hannah S.; Prom, Ben M.; Kim, Hyunkee; Adams, Paul D.; Northen, Trent R.; Fox, Brian G.

doi:10.1186/s13068-015-0402-0

Title: Multifunctional cellulase catalysis targeted by fusion to different carbohydrate-binding modules

Journal Article · Mon Dec 21 00:00:00 EST 2015 · Biotechnology for Biofuels

DOI:https://doi.org/10.1186/s13068-015-0402-0· OSTI ID:1618633

Walker, Johnnie A.; Takasuka, Taichi E.; Deng, Kai; Bianchetti, Christopher M.; Udell, Hannah S.; Prom, Ben M.; Kim, Hyunkee; Adams, Paul D.; Northen, Trent R.; Fox, Brian G.

Carbohydrate binding modules (CBMs) bind polysaccharides and help target glycoside hydrolases catalytic domains to their appropriate carbohydrate substrates. To better understand how CBMs can improve cellulolytic enzyme reactivity, representatives from each of the 18 families of CBM found in Ruminoclostridium thermocellum were fused to the multifunctional GH5 catalytic domain of CelE (Cthe-0797, CelEcc), which can hydrolyze numerous types of polysaccharides including cellulose, mannan, and xylan. Since CelE is a cellulosomal enzyme, none of these fusions to a CBM previously existed. Results: CelEcc-CBM fusions were assayed for their ability to hydrolyze cellulose, lichenan, xylan, and mannan. Several CelEcc-CBM fusions showed enhanced hydrolytic activity with different substrates relative to the fusion to CBM3a from the cellulosome scaffoldin, which has high affinity for binding to crystalline cellulose. Additional binding studies and quantitative catalysis studies using nanostructure-initiator mass spectrometry (NIMS) were carried out with the CBM3a, CBM6, CBM30, and CBM44 fusion enzymes. In general, and consistent with observations of others, enhanced enzyme reactivity was correlated with moderate binding affinity of the CBM. Numerical analysis of reaction time courses showed that CelEcc-CBM44, a combination of a multifunctional enzyme domain with a CBM having broad binding specificity, gave the fastest rates for hydrolysis of both the hexose and pentose fractions of ionic-liquid pretreated switchgrass. Conclusion: We have shown that fusions of different CBMs to a single multifunctional GH5 catalytic domain can increase its rate of reaction with different pure polysaccharides and with pretreated biomass. This fusion approach, incorporating domains with broad specificity for binding and catalysis, provides a new avenue to improve reactivity of simple combinations of enzymes within the complexity of plant biomass.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Sandia National Lab. (SNL-NM), Albuquerque, NM (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); National Science Foundation (NSF); National Institutes of Health (NIH)

Grant/Contract Number:: FC02-07ER64494; AC02-05CH11231; DGE-1256259; AC04-94AL85000

OSTI ID:: 1618633

Alternate ID(s):: OSTI ID: 1257273; OSTI ID: 1262308; OSTI ID: 1378704

Report Number(s):: SAND-2016-6409J; 220; PII: 402

Journal Information:: Biotechnology for Biofuels, Journal Name: Biotechnology for Biofuels Vol. 8 Journal Issue: 1; ISSN 1754-6834

Publisher:: Springer Science + Business MediaCopyright Statement

Country of Publication:: Netherlands

Language:: English

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Cited by: 44 works

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References (94)

Characterization of hybrid proteins consisting of the catalytic domains of Clostridium and Ruminococcus endoglucanases, fused to Pseudomonas non-catalytic cellulose-binding domains Poole, D. M.; Durrant, A. J.; Hazlewood, G. P. Biochemical Journal, Vol. 279, Issue 3 https://doi.org/10.1042/bj2790787	journal	November 1991
Putting an N-terminal end to the Clostridium thermocellum xylanase Xyn10B story: Crystal structure of the CBM22-1–GH10 modules complexed with xylohexaose Najmudin, Shabir; Pinheiro, Benedita A.; Prates, José A. M. Journal of Structural Biology, Vol. 172, Issue 3 https://doi.org/10.1016/j.jsb.2010.07.009	journal	December 2010
The Green Fluorescent Protein Tsien, Roger Y. Annual Review of Biochemistry, Vol. 67, Issue 1, p. 509-544 https://doi.org/10.1146/annurev.biochem.67.1.509	journal	June 1998
Influence of physico-chemical changes on enzymatic digestibility of ionic liquid and AFEX pretreated corn stover Li, Chenlin; Cheng, Gang; Balan, Venkatesh Bioresource Technology, Vol. 102, Issue 13 https://doi.org/10.1016/j.biortech.2011.04.005	journal	July 2011
The Location of the Ligand-binding Site of Carbohydrate-binding Modules That Have Evolved from a Common Sequence Is Not Conserved Czjzek, Mirjam; Bolam, David N.; Mosbah, Amor Journal of Biological Chemistry, Vol. 276, Issue 51 https://doi.org/10.1074/jbc.M109142200	journal	October 2001
An Oxidative Enzyme Boosting the Enzymatic Conversion of Recalcitrant Polysaccharides Vaaje-Kolstad, Gustav; Westereng, Bjørge; Horn, Svein J. Science, Vol. 330, Issue 6001, p. 219-222 https://doi.org/10.1126/science.1192231	journal	October 2010
High temperatures enhance cooperative motions between CBM and catalytic domains of a thermostable cellulase: mechanism insights from essential dynamics Batista, Paulo Ricardo; de Souza Costa, Mauricio Garcia; Pascutti, Pedro Geraldo Physical Chemistry Chemical Physics, Vol. 13, Issue 30 https://doi.org/10.1039/c0cp02697b	journal	January 2011
Comparison of dilute acid and ionic liquid pretreatment of switchgrass: Biomass recalcitrance, delignification and enzymatic saccharification Li, Chenlin; Knierim, Bernhard; Manisseri, Chithra Bioresource Technology, Vol. 101, Issue 13 https://doi.org/10.1016/j.biortech.2009.10.066	journal	July 2010
X-ray Structure of Mercerized Cellulose II at 1 Å Resolution Langan, Paul; Nishiyama, Yoshiharu; Chanzy, Henri Biomacromolecules, Vol. 2, Issue 2 https://doi.org/10.1021/bm005612q	journal	June 2001
Extra tyrosine in the carbohydrate-binding module of Irpex lacteus Xyn10B enhances its cellulose-binding ability Nishijima, Hiroto; Nozaki, Kouichi; Mizuno, Masahiro Bioscience, Biotechnology, and Biochemistry, Vol. 79, Issue 5 https://doi.org/10.1080/09168451.2014.996203	journal	January 2015
A C4-oxidizing Lytic Polysaccharide Monooxygenase Cleaving Both Cellulose and Cello-oligosaccharides Isaksen, Trine; Westereng, Bjørge; Aachmann, Finn L. Journal of Biological Chemistry, Vol. 289, Issue 5 https://doi.org/10.1074/jbc.M113.530196	journal	December 2013
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
How biotech can transform biofuels Lynd, Lee R.; Laser, Mark S.; Bransby, David Nature Biotechnology, Vol. 26, Issue 2, p. 169-172 https://doi.org/10.1038/nbt0208-169	journal	February 2008
Versatile derivatives of carbohydrate-binding modules for imaging of complex carbohydrates approaching the molecular level of resolution Ding, Shi-You; Xu, Qi; Ali, Mursheda K. BioTechniques, Vol. 41, Issue 4 https://doi.org/10.2144/000112244	journal	October 2006
Deconstruction of Lignocellulosic Biomass to Fuels and Chemicals Chundawat, Shishir P. S.; Beckham, Gregg T.; Himmel, Michael E. Annual Review of Chemical and Biomolecular Engineering, Vol. 2, Issue 1, p. 121-145 https://doi.org/10.1146/annurev-chembioeng-061010-114205	journal	July 2011
Discovery and characterization of a new family of lytic polysaccharide monooxygenases Hemsworth, Glyn R.; Henrissat, Bernard; Davies, Gideon J. Nature Chemical Biology, Vol. 10, Issue 2 https://doi.org/10.1038/nchembio.1417	journal	December 2013
Cellulase Linkers Are Optimized Based on Domain Type and Function: Insights from Sequence Analysis, Biophysical Measurements, and Molecular Simulation Sammond, Deanne W.; Payne, Christina M.; Brunecky, Roman PLoS ONE, Vol. 7, Issue 11 https://doi.org/10.1371/journal.pone.0048615	journal	November 2012
Native Cellulose: A Composite of Two Distinct Crystalline Forms Atalla, R. H.; Vanderhart, D. L. Science, Vol. 223, Issue 4633 https://doi.org/10.1126/science.223.4633.283	journal	January 1984
Visualization of biomass solubilization and cellulose regeneration during ionic liquid pretreatment of switchgrass Singh, Seema; Simmons, Blake A.; Vogel, Kenneth P. Biotechnology and Bioengineering, Vol. 104, Issue 1, p. 68-75 https://doi.org/10.1002/bit.22386	journal	September 2009
Understanding, improving and using green fluorescent proteins Cubitt, Andrew B.; Heim, Roger; Adams, Stephen R. Trends in Biochemical Sciences, Vol. 20, Issue 11 https://doi.org/10.1016/S0968-0004(00)89099-4	journal	November 1995
The Hill equation revisited: uses and misuses. Weiss, J. N. The FASEB Journal, Vol. 11, Issue 11 https://doi.org/10.1096/fasebj.11.11.9285481	journal	September 1997
Evidence that family 35 carbohydrate binding modules display conserved specificity but divergent function Montanier, C.; van Bueren, A. L.; Dumon, C. Proceedings of the National Academy of Sciences, Vol. 106, Issue 9 https://doi.org/10.1073/pnas.0808972106	journal	February 2009
How nature can exploit nonspecific catalytic and carbohydrate binding modules to create enzymatic specificity Cuskin, F.; Flint, J. E.; Gloster, T. M. Proceedings of the National Academy of Sciences, Vol. 109, Issue 51 https://doi.org/10.1073/pnas.1212034109	journal	December 2012
Fungal cellulose degradation by oxidative enzymes: from dysfunctional GH61 family to powerful lytic polysaccharide monooxygenase family Morgenstern, I.; Powlowski, J.; Tsang, A. Briefings in Functional Genomics, Vol. 13, Issue 6 https://doi.org/10.1093/bfgp/elu032	journal	September 2014
Construction and characterization of chimeric cellulases with enhanced catalytic activity towards insoluble cellulosic substrates Telke, Amar A.; Ghatge, Sunil S.; Kang, Seo-Hee Bioresource Technology, Vol. 112, p. 10-17 https://doi.org/10.1016/j.biortech.2012.02.066	journal	May 2012
Crystal structure of a bacterial family-III cellulose-binding domain: a general mechanism for attachment to cellulose. Tormo, J.; Lamed, R.; Chirino, A. J. The EMBO Journal, Vol. 15, Issue 21, p. 5739-5751 https://doi.org/10.1002/j.1460-2075.1996.tb00960.x	journal	November 1996
The hierarchical structure and mechanics of plant materials Gibson, Lorna J. Journal of The Royal Society Interface, Vol. 9, Issue 76 https://doi.org/10.1098/rsif.2012.0341	journal	June 2012
Ab Initio Structure Determination and Functional Characterization Of CBM36 Jamal-Talabani, Sheelan; Boraston, Alisdair B.; Turkenburg, Johan P. Structure, Vol. 12, Issue 7 https://doi.org/10.1016/j.str.2004.04.022	journal	July 2004
Constructing and Exploiting the Fluorescent Protein Paintbox (Nobel Lecture) Tsien, Roger Y. Angewandte Chemie International Edition, Vol. 48, Issue 31 https://doi.org/10.1002/anie.200901916	journal	July 2009
Features of promising technologies for pretreatment of lignocellulosic biomass Mosier, Nathan; Wyman, Charles; Dale, Bruce Bioresource Technology, Vol. 96, Issue 6, p. 673-686 https://doi.org/10.1016/j.biortech.2004.06.025	journal	April 2005
Increased enzyme binding to substrate is not necessary for more efficient cellulose hydrolysis Gao, D.; Chundawat, S. P. S.; Sethi, A. Proceedings of the National Academy of Sciences, Vol. 110, Issue 27 https://doi.org/10.1073/pnas.1213426110	journal	June 2013
Carbohydrate-binding domains: multiplicity of biological roles Guillén, Daniel; Sánchez, Sergio; Rodríguez-Sanoja, Romina Applied Microbiology and Biotechnology, Vol. 85, Issue 5 https://doi.org/10.1007/s00253-009-2331-y	journal	November 2009
The role of solid state NMR spectroscopy in studies of the nature of native celluloses Atalla, R. H.; VanderHart, D. L. Solid State Nuclear Magnetic Resonance, Vol. 15, Issue 1 https://doi.org/10.1016/S0926-2040(99)00042-9	journal	October 1999
Enhanced Bacterial Protein Expression During Auto-Induction Obtained by Alteration of Lac Repressor Dosage and Medium Composition Blommel, Paul G.; Becker, Katie J.; Duvnjak, Petar Biotechnology Progress, Vol. 23, Issue 3 https://doi.org/10.1021/bp070011x	journal	January 2007
Xyloglucan Is Recognized by Carbohydrate-binding Modules That Interact with β-Glucan Chains Najmudin, Shabir; Guerreiro, Catarina I. P. D.; Carvalho, Ana L. Journal of Biological Chemistry, Vol. 281, Issue 13 https://doi.org/10.1074/jbc.M510559200	journal	November 2005
Structural and mechanistic insight into N-glycan processing by endo- -mannosidase Thompson, A. J.; Williams, R. J.; Hakki, Z. Proceedings of the National Academy of Sciences, Vol. 109, Issue 3 https://doi.org/10.1073/pnas.1111482109	journal	January 2012
Carbohydrate-binding modules from a thermostable Rhodothermus marinus xylanase: cloning, expression and binding studies Abou Hachem, Maher; Nordberg Karlsson, Eva; Bartonek-RoxÅ, Eva Biochemical Journal, Vol. 345, Issue 1 https://doi.org/10.1042/0264-6021:3450053	journal	January 2000
Bacterial cellulases Béguin, Pierre; Millet, Jacqueline; Chauvaux, Sylvie Biochemical Society Transactions, Vol. 20, Issue 1 https://doi.org/10.1042/bst0200042	journal	February 1992
Heterogeneity in the chemistry, structure and function of plant cell walls Burton, Rachel A.; Gidley, Michael J.; Fincher, Geoffrey B. Nature Chemical Biology, Vol. 6, Issue 10 https://doi.org/10.1038/nchembio.439	journal	September 2010
Crystal Structure and Hydrogen Bonding System in Cellulose I _α from Synchrotron X-ray and Neutron Fiber Diffraction Nishiyama, Yoshiharu; Sugiyama, Junji; Chanzy, Henri Journal of the American Chemical Society, Vol. 125, Issue 47 https://doi.org/10.1021/ja037055w	journal	November 2003
Outlook for cellulase improvement: Screening and selection strategies Percival Zhang, Y.-H.; Himmel, Michael E.; Mielenz, Jonathan R. Biotechnology Advances, Vol. 24, Issue 5, p. 452-481 https://doi.org/10.1016/j.biotechadv.2006.03.003	journal	September 2006
A Simplex Method for Function Minimization Nelder, J. A.; Mead, R. The Computer Journal, Vol. 7, Issue 4 https://doi.org/10.1093/comjnl/7.4.308	journal	January 1965
Techno-economic analysis of lignocellulosic ethanol: A review Gnansounou, Edgard; Dauriat, Arnaud Bioresource Technology, Vol. 101, Issue 13 https://doi.org/10.1016/j.biortech.2010.02.009	journal	July 2010
Insight into Ligand Diversity and Novel Biological Roles for Family 32 Carbohydrate-Binding Modules Abbott, D. W.; Eirin-Lopez, J. M.; Boraston, A. B. Molecular Biology and Evolution, Vol. 25, Issue 1 https://doi.org/10.1093/molbev/msm243	journal	November 2007
Co-operative binding of triplicate carbohydrate-binding modules from a thermophilic xylanase Boraston, Alisdair B.; McLean, Bradley W.; Chen, Grace Molecular Microbiology, Vol. 43, Issue 1 https://doi.org/10.1046/j.1365-2958.2002.02730.x	journal	January 2002
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
How the walls come crumbling down: recent structural biochemistry of plant polysaccharide degradation Gilbert, H.; Stalbrand, H.; Brumer, H. Current Opinion in Plant Biology, Vol. 11, Issue 3 https://doi.org/10.1016/j.pbi.2008.03.004	journal	June 2008
Crystal Structure and Hydrogen-Bonding System in Cellulose Iβ from Synchrotron X-ray and Neutron Fiber Diffraction Nishiyama, Yoshiharu; Langan, Paul; Chanzy, Henri Journal of the American Chemical Society, Vol. 124, Issue 31 https://doi.org/10.1021/ja0257319	journal	August 2002
Bioconversion of lignocellulosic biomass: biochemical and molecular perspectives Kumar, Raj; Singh, Sompal; Singh, Om V. Journal of Industrial Microbiology & Biotechnology, Vol. 35, Issue 5 https://doi.org/10.1007/s10295-008-0327-8	journal	March 2008
Recent insights into copper-containing lytic polysaccharide mono-oxygenases Hemsworth, Glyn R.; Davies, Gideon J.; Walton, Paul H. Current Opinion in Structural Biology, Vol. 23, Issue 5, p. 660-668 https://doi.org/10.1016/j.sbi.2013.05.006	journal	October 2013
Hemicellulose biosynthesis Pauly, Markus; Gille, Sascha; Liu, Lifeng Planta, Vol. 238, Issue 4 https://doi.org/10.1007/s00425-013-1921-1	journal	June 2013
Lignin Biosynthesis Boerjan, Wout; Ralph, John; Baucher, Marie Annual Review of Plant Biology, Vol. 54, Issue 1, p. 519-546 https://doi.org/10.1146/annurev.arplant.54.031902.134938	journal	June 2003
Modeling cellulase kinetics on lignocellulosic substrates Bansal, Prabuddha; Hall, Mélanie; Realff, Matthew J. Biotechnology Advances, Vol. 27, Issue 6 https://doi.org/10.1016/j.biotechadv.2009.06.005	journal	November 2009
The Polymerase Incomplete Primer Extension (PIPE) Method Applied to High-Throughput Cloning and Site-Directed Mutagenesis Klock, Heath E.; Lesley, Scott A. Methods in Molecular Biology https://doi.org/10.1007/978-1-59745-196-3_6	book	January 2009
Characterization of a cellulose-binding, cellulase-containing complex in Clostridium thermocellum. Lamed, R.; Setter, E.; Bayer, E. A. Journal of Bacteriology, Vol. 156, Issue 2 https://doi.org/10.1128/JB.156.2.828-836.1983	journal	January 1983
The X6 “Thermostabilizing” Domains of Xylanases Are Carbohydrate-Binding Modules: Structure and Biochemistry of the Clostridium thermocellum X6b Domain ^† ^, ^‡ Charnock, Simon J.; Bolam, David N.; Turkenburg, Johan P. Biochemistry, Vol. 39, Issue 17 https://doi.org/10.1021/bi992821q	journal	May 2000
Hemicelluloses Scheller, Henrik Vibe; Ulvskov, Peter Annual Review of Plant Biology, Vol. 61, Issue 1 https://doi.org/10.1146/annurev-arplant-042809-112315	journal	June 2010
The non-catalytic cellulose-binding domain of a novel cellulase from Pseudomonas fluorescens subsp. cellulosa is important for the efficient hydrolysis of Avicel Hall, J.; Black, G. W.; Ferreira, L. M. A. Biochemical Journal, Vol. 309, Issue 3 https://doi.org/10.1042/bj3090749	journal	August 1995
Expression, purification and characterization of a functional carbohydrate-binding module from Streptomyces sp. SirexAA-E Lim, Sungsoo; Chundawat, Shishir P. S.; Fox, Brian G. Protein Expression and Purification, Vol. 98 https://doi.org/10.1016/j.pep.2014.02.013	journal	June 2014
A Transition from Cellulose Swelling to Cellulose Dissolution by o -Phosphoric Acid: Evidence from Enzymatic Hydrolysis and Supramolecular Structure Zhang, Y. -H. Percival; Cui, Jingbiao; Lynd, Lee R. Biomacromolecules, Vol. 7, Issue 2 https://doi.org/10.1021/bm050799c	journal	February 2006
Rapid Kinetic Characterization of Glycosyl Hydrolases Based on Oxime Derivatization and Nanostructure-Initiator Mass Spectrometry (NIMS) Deng, Kai; Takasuka, Taichi E.; Heins, Richard ACS Chemical Biology, Vol. 9, Issue 7 https://doi.org/10.1021/cb5000289	journal	May 2014
Binding modules alter the activity of chimeric cellulases: Effects of biomass pretreatment and enzyme source Kim, Tae-Wan; Chokhawala, Harshal A.; Nadler, Dana Biotechnology and Bioengineering, Vol. 107, Issue 4, p. 601-611 https://doi.org/10.1002/bit.22856	journal	July 2010
Carbohydrate-binding modules promote the enzymatic deconstruction of intact plant cell walls by targeting and proximity effects Herve, C.; Rogowski, A.; Blake, A. W. Proceedings of the National Academy of Sciences, Vol. 107, Issue 34 https://doi.org/10.1073/pnas.1005732107	journal	August 2010
Synergistic proteins for the enhanced enzymatic hydrolysis of cellulose by cellulase Kim, In Jung; Lee, Hee Jin; Choi, In-Geol Applied Microbiology and Biotechnology, Vol. 98, Issue 20 https://doi.org/10.1007/s00253-014-6001-3	journal	August 2014
Hemicelluloses for fuel ethanol: A review Gírio, F. M.; Fonseca, C.; Carvalheiro, F. Bioresource Technology, Vol. 101, Issue 13 https://doi.org/10.1016/j.biortech.2010.01.088	journal	July 2010
New insights into enzymatic hydrolysis of heterogeneous cellulose by using carbohydrate-binding module 3 containing GFP and carbohydrate-binding module 17 containing CFP Gao, Shuhong; You, Chun; Renneckar, Scott Biotechnology for Biofuels, Vol. 7, Issue 1 https://doi.org/10.1186/1754-6834-7-24	journal	January 2014
Microbial hemicellulases Shallom, Dalia; Shoham, Yuval Current Opinion in Microbiology, Vol. 6, Issue 3, p. 219-228 https://doi.org/10.1016/S1369-5274(03)00056-0	journal	June 2003
X4 Modules Represent a New Family of Carbohydrate-binding Modules That Display Novel Properties Bolam, David N.; Xie, Hefang; Pell, Gavin Journal of Biological Chemistry, Vol. 279, Issue 22 https://doi.org/10.1074/jbc.M313317200	journal	March 2004
Quantitative Determination of Cellulose Accessibility to Cellulase Based on Adsorption of a Nonhydrolytic Fusion Protein Containing CBM and GFP with Its Applications Hong, Jiong; Ye, Xinhao; Zhang, Y. -H. Percival Langmuir, Vol. 23, Issue 25 https://doi.org/10.1021/la7025686	journal	December 2007
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
Integration of bacterial lytic polysaccharide monooxygenases into designer cellulosomes promotes enhanced cellulose degradation Arfi, Y.; Shamshoum, M.; Rogachev, I. Proceedings of the National Academy of Sciences, Vol. 111, Issue 25 https://doi.org/10.1073/pnas.1404148111	journal	June 2014
Fine-structural variance of family 3 carbohydrate-binding modules as extracellular biomass-sensing components of Clostridium thermocellum anti-σ ^I factors Yaniv, Oren; Fichman, Galit; Borovok, Ilya Acta Crystallographica Section D Biological Crystallography, Vol. 70, Issue 2 https://doi.org/10.1107/S139900471302926X	journal	January 2014
Influence of the Transposition of the Thermostabilizing Domain of Clostridium thermocellum Xylanase (XynX) on Xylan Binding and Thermostabilization Shin, E. -S.; Yang, M. -J.; Jung, K. H. Applied and Environmental Microbiology, Vol. 68, Issue 7 https://doi.org/10.1128/AEM.68.7.3496-3501.2002	journal	July 2002
Cellulosomes: Highly Efficient Nanomachines Designed to Deconstruct Plant Cell Wall Complex Carbohydrates Fontes, Carlos M. G. A.; Gilbert, Harry J. Annual Review of Biochemistry, Vol. 79, Issue 1 https://doi.org/10.1146/annurev-biochem-091208-085603	journal	June 2010
Protein Disorder: Conformational Distribution of the Flexible Linker in a Chimeric Double Cellulase von Ossowski, Ingemar; Eaton, Julian T.; Czjzek, Mirjam Biophysical Journal, Vol. 88, Issue 4 https://doi.org/10.1529/biophysj.104.050146	journal	April 2005
Lignin Biosynthesis and Structure Vanholme, R.; Demedts, B.; Morreel, K. Plant Physiology, Vol. 153, Issue 3, p. 895-905 https://doi.org/10.1104/pp.110.155119	journal	May 2010
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
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
Effect of cellulose fine structure on kinetics of its digestion by mixed ruminal microorganisms in vitro. Weimer, P. J.; Lopez-Guisa, J. M.; French, A. D. Applied and Environmental Microbiology, Vol. 56, Issue 8 https://doi.org/10.1128/AEM.56.8.2421-2429.1990	journal	January 1990
Use of Dinitrosalicylic Acid Reagent for Determination of Reducing Sugar Miller, G. L. Analytical Chemistry, Vol. 31, Issue 3 https://doi.org/10.1021/ac60147a030	journal	March 1959
Oxidoreductive Cellulose Depolymerization by the Enzymes Cellobiose Dehydrogenase and Glycoside Hydrolase 61 Langston, James A.; Shaghasi, Tarana; Abbate, Eric Applied and Environmental Microbiology, Vol. 77, Issue 19, p. 7007-7015 https://doi.org/10.1128/AEM.05815-11	journal	August 2011
Fusion of a family 9 cellulose-binding module improves catalytic potential of Clostridium thermocellum cellodextrin phosphorylase on insoluble cellulose Ye, Xinhao; Zhu, Zhiguang; Zhang, Chenming Applied Microbiology and Biotechnology, Vol. 92, Issue 3 https://doi.org/10.1007/s00253-011-3346-8	journal	June 2011
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
Enzymatic deconstruction of xylan for biofuel production Dodd, Dylan; Cann, Isaac K. O. GCB Bioenergy, Vol. 1, Issue 1 https://doi.org/10.1111/j.1757-1707.2009.01004.x	journal	February 2009
Recent advances in understanding the role of cellulose accessibility in enzymatic hydrolysis of lignocellulosic substrates Meng, Xianzhi; Ragauskas, Arthur Jonas Current Opinion in Biotechnology, Vol. 27 https://doi.org/10.1016/j.copbio.2014.01.014	journal	June 2014
A combined approach to improving large-scale production of tobacco etch virus protease Blommel, Paul G.; Fox, Brian G. Protein Expression and Purification, Vol. 55, Issue 1, p. 53-68 https://doi.org/10.1016/j.pep.2007.04.013	journal	September 2007
Modifying plants for biofuel and biomaterial production Furtado, Agnelo; Lupoi, Jason S.; Hoang, Nam V. Plant Biotechnology Journal, Vol. 12, Issue 9 https://doi.org/10.1111/pbi.12300	journal	November 2014
Cell-Free Translation of Biofuel Enzymes Takasuka, Taichi E.; Walker, Johnnie A.; Bergeman, Lai F. Methods in Molecular Biology https://doi.org/10.1007/978-1-62703-782-2_5	book	December 2013
Multifaceted characterization of cell wall decomposition products formed during ammonia fiber expansion (AFEX) and dilute acid based pretreatments Chundawat, Shishir P. S.; Vismeh, Ramin; Sharma, Lekh N. Bioresource Technology, Vol. 101, Issue 21 https://doi.org/10.1016/j.biortech.2010.06.027	journal	November 2010
Linker length and flexibility induces new cellobiohydrolase activity of PoCel6A from Penicillium oxalicum Gao, Le; Wang, Lushan; Jiang, Xukai Biotechnology Journal, Vol. 10, Issue 6 https://doi.org/10.1002/biot.201400734	journal	May 2015
Genome sequencing and analysis of the biomass-degrading fungus Trichoderma reesei (syn. Hypocrea jecorina) Martinez, Diego; Berka, Randy M.; Henrissat, Bernard Nature Biotechnology, Vol. 26, Issue 5 https://doi.org/10.1038/nbt1403	journal	May 2008
Purification and characterization of a new xylanase (xylanase B) produced by Streptomyces lividans 66 Kluepfel, D.; Vats-Mehta, S.; Aumont, F. Biochemical Journal, Vol. 267, Issue 1 https://doi.org/10.1042/bj2670045	journal	April 1990
Plant cell walls to ethanol Jordan, Douglas B.; Bowman, Michael J.; Braker, Jay D. Biochemical Journal, Vol. 442, Issue 2 https://doi.org/10.1042/BJ20111922	journal	February 2012
Expansion of the enzymatic repertoire of the CAZy database to integrate auxiliary redox enzymes Levasseur, Anthony; Drula, Elodie; Lombard, Vincent Biotechnology for Biofuels, Vol. 6, Issue 1, Article No. 41 https://doi.org/10.1186/1754-6834-6-41	journal	January 2013

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Fusion of Carbohydrate Binding Modules to Bifunctional Cellulase to Enhance Binding Affinity and Cellulolytic Activity Maharjan, Anoth; Alkotaini, Bassam; Kim, Beom Soo Biotechnology and Bioprocess Engineering, Vol. 23, Issue 1 https://doi.org/10.1007/s12257-018-0011-4	journal	February 2018
Profiling microbial lignocellulose degradation and utilization by emergent omics technologies Rosnow, Joshua J.; Anderson, Lindsey N.; Nair, Reji N. Critical Reviews in Biotechnology, Vol. 37, Issue 5 https://doi.org/10.1080/07388551.2016.1209158	journal	July 2016
Replacement of carbohydrate binding modules improves acetyl xylan esterase activity and its synergistic hydrolysis of different substrates with xylanase Liu, Shiping; Ding, Shaojun BMC Biotechnology, Vol. 16, Issue 1 https://doi.org/10.1186/s12896-016-0305-6	journal	October 2016
Determination of glycoside hydrolase specificities during hydrolysis of plant cell walls using glycome profiling Walker, Johnnie A.; Pattathil, Sivakumar; Bergeman, Lai F. Biotechnology for Biofuels, Vol. 10, Issue 1 https://doi.org/10.1186/s13068-017-0703-6	journal	February 2017
Genetically Engineered Proteins to Improve Biomass Conversion: New Advances and Challenges for Tailoring Biocatalysts Ribeiro, Lucas Ferreira; Amarelle, Vanesa; Alves, Luana de Fátima Molecules, Vol. 24, Issue 16 https://doi.org/10.3390/molecules24162879	journal	August 2019

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Related Subjects

59 BASIC BIOLOGICAL SCIENCES
cellulase
xylanase
hemicellulase
mannanase
carbohydrate binding module
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enzyme engineering
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Multifunctional cellulase catalysis targeted by fusion to different carbohydrate-binding modules [Supplementary Data] Walker, Johnnie; Takasuka, Taichi; Deng, Kai https://doi.org/10.6084/m9.figshare.c.3641288 The current record is supplemented by this collection	collection	December 2015
Multifunctional cellulase catalysis targeted by fusion to different carbohydrate-binding modules [Supplementary Data] Walker, Johnnie; Takasuka, Taichi; Deng, Kai https://doi.org/10.6084/m9.figshare.c.3641288.v1 The current record is supplemented by this collection	collection	December 2015
MOESM2 of Multifunctional cellulase catalysis targeted by fusion to different carbohydrate-binding modules Walker, Johnnie; Takasuka, Taichi; Deng, Kai https://doi.org/10.6084/m9.figshare.c.3641288_d1 The current record is supplemented by this dataset	dataset	December 2015
MOESM2 of Multifunctional cellulase catalysis targeted by fusion to different carbohydrate-binding modules Walker, Johnnie; Takasuka, Taichi; Deng, Kai https://doi.org/10.6084/m9.figshare.c.3641288_d1.v1 The current record is supplemented by this dataset	dataset	December 2015
MOESM3 of Multifunctional cellulase catalysis targeted by fusion to different carbohydrate-binding modules Walker, Johnnie; Takasuka, Taichi; Deng, Kai https://doi.org/10.6084/m9.figshare.c.3641288_d2 The current record is supplemented by this dataset	dataset	December 2015
MOESM3 of Multifunctional cellulase catalysis targeted by fusion to different carbohydrate-binding modules Walker, Johnnie; Takasuka, Taichi; Deng, Kai https://doi.org/10.6084/m9.figshare.c.3641288_d2.v1 The current record is supplemented by this dataset	dataset	December 2015
MOESM1 of Multifunctional cellulase catalysis targeted by fusion to different carbohydrate-binding modules Walker, Johnnie; Takasuka, Taichi; Deng, Kai https://doi.org/10.6084/m9.figshare.c.3641288_d3.v1 The current record is supplemented by this dataset	dataset	December 2015