Binding Preferences, Surface Attachment, Diffusivity, and Orientation of a Family 1 Carbohydrate-Binding Module on Cellulose

Nimlos, Mark R.; Beckham, Gregg T.; Matthews, James F.; Bu, Lintao; Himmel, Michael E.; Crowley, Michael F.

doi:10.1074/jbc.M112.358184

Title: Binding Preferences, Surface Attachment, Diffusivity, and Orientation of a Family 1 Carbohydrate-Binding Module on Cellulose

Journal Article · Fri Jun 08 00:00:00 EDT 2012 · Journal of Biological Chemistry

DOI:https://doi.org/10.1074/jbc.M112.358184· OSTI ID:1046293

Nimlos, Mark R.; Beckham, Gregg T.; Matthews, James F.; Bu, Lintao; Himmel, Michael E.; Crowley, Michael F.

Cellulase enzymes often contain carbohydrate-binding modules (CBMs) for binding to cellulose. The mechanisms by which CBMs recognize specific surfaces of cellulose and aid in deconstruction are essential to understand cellulase action. The Family 1 CBM from the Trichoderma reesei Family 7 cellobiohydrolase, Cel7A, is known to selectively bind to hydrophobic surfaces of native cellulose. It is most commonly suggested that three aromatic residues identify the planar binding face of this CBM, but several recent studies have challenged this hypothesis. Here, we use molecular simulation to study the CBM binding orientation and affinity on hydrophilic and hydrophobic cellulose surfaces. Roughly 43 {mu}s of molecular dynamics simulations were conducted, which enables statistically significant observations. We quantify the fractions of the CBMs that detach from crystal surfaces or diffuse to other surfaces, the diffusivity along the hydrophobic surface, and the overall orientation of the CBM on both hydrophobic and hydrophilic faces. The simulations demonstrate that there is a thermodynamic driving force for the Cel7A CBM to bind preferentially to the hydrophobic surface of cellulose relative to hydrophilic surfaces. In addition, the simulations demonstrate that the CBM can diffuse from hydrophilic surfaces to the hydrophobic surface, whereas the reverse transition is not observed. Lastly, our simulations suggest that the flat faces of Family 1 CBMs are the preferred binding surfaces. These results enhance our understanding of how Family 1 CBMs interact with and recognize specific cellulose surfaces and provide insights into the initial events of cellulase adsorption and diffusion on cellulose.

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

Sponsoring Organization:: USDOE Office of Energy Efficiency and Renewable Energy Biomass Program

DOE Contract Number:: AC36-08GO28308

OSTI ID:: 1046293

Report Number(s):: NREL/JA-5100-55137; JBCHA3; TRN: US201216%%140

Journal Information:: Journal of Biological Chemistry, Vol. 287, Issue 24; ISSN 0021-9258

Country of Publication:: United States

Language:: English

References (64)

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
Cellulases and biofuels Wilson, David B. Current Opinion in Biotechnology, Vol. 20, Issue 3, p. 295-299 https://doi.org/10.1016/j.copbio.2009.05.007	journal	June 2009
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
Determination of the three-dimensional solution structure of the C-terminal domain of cellobiohydrolase I from Trichoderma reesei. A study using nuclear magnetic resonance and hybrid distance geometry-dynamical simulated annealing Kraulis, Per J.; Clore, G. Marius; Nilges, Michael Biochemistry, Vol. 28, Issue 18 https://doi.org/10.1021/bi00444a016	journal	September 1989
Three-dimensional structure of cellobiohydrolase II from Trichoderma reesei Rouvinen, J.; Bergfors, T.; Teeri, T. Science, Vol. 249, Issue 4967 https://doi.org/10.1126/science.2377893	journal	July 1990
The three-dimensional crystal structure of the catalytic core of cellobiohydrolase I from Trichoderma reesei Divne, C.; Stahlberg, J.; Reinikainen, T. Science, Vol. 265, Issue 5171 https://doi.org/10.1126/science.8036495	journal	July 1994
The difference in affinity between two fungal cellulose-binding domains is dominated by a single amino acid substitution Linder, Markus; Lindeberg, Gunnar; Reinikainen, Tapani FEBS Letters, Vol. 372, Issue 1 https://doi.org/10.1016/0014-5793(95)00961-8	journal	September 1995
The crystal structure of the catalytic core domain of endoglucanase I from Trichoderma reesei at 3.6 Å resolution, and a comparison with related enzymes Kleywegt, Gerard J.; Zou, Jin-Yu; Divne, Christina Journal of Molecular Biology, Vol. 272, Issue 3, p. 383-397 https://doi.org/10.1006/jmbi.1997.1243	journal	September 1997
High-resolution crystal structures reveal how a cellulose chain is bound in the 50 Å long tunnel of cellobiohydrolase I from Trichoderma reesei Divne, Christina; Ståhlberg, Jerry; Teeri, Tuula T. Journal of Molecular Biology, Vol. 275, Issue 2, p. 309-325 https://doi.org/10.1006/jmbi.1997.1437	journal	January 1998
Tryptophan 272: an essential determinant of crystalline cellulose degradation by Trichoderma reesei cellobiohydrolase Cel6A Koivula, Anu; Kinnari, Tiina; Harjunpää, Vesa FEBS Letters, Vol. 429, Issue 3 https://doi.org/10.1016/S0014-5793(98)00596-1	journal	June 1998
Characterization of cellobiohydrolase I (Cel7A) glycoforms from extracts of Trichoderma reesei using capillary isoelectric focusing and electrospray mass spectrometry Hui, Joseph P. M.; Lanthier, Patricia; White, Theresa C. Journal of Chromatography B: Biomedical Sciences and Applications, Vol. 752, Issue 2 https://doi.org/10.1016/S0378-4347(00)00373-X	journal	March 2001
The X-ray crystal structure of the Trichoderma reesei family 12 endoglucanase 3, Cel12A, at 1.9 Å resolution1 1Edited by A. R. Fersht Sandgren, Mats; Shaw, Andrew; Ropp, Traci H. Journal of Molecular Biology, Vol. 308, Issue 2 https://doi.org/10.1006/jmbi.2001.4583	journal	April 2001
Factors influencing glycosylation of Trichoderma reesei cellulases. II: N-glycosylation of Cel7A core protein isolated from different strains Stals, I. Glycobiology, Vol. 14, Issue 8 https://doi.org/10.1093/glycob/cwh081	journal	March 2004
Factors influencing glycosylation of Trichoderma reesei cellulases. I: Postsecretorial changes of the O- and N-glycosylation pattern of Cel7A Stals, I. Glycobiology, Vol. 14, Issue 8 https://doi.org/10.1093/glycob/cwh080	journal	March 2004
The First Structure of a Glycoside Hydrolase Family 61 Member, Cel61B from Hypocrea jecorina, at 1.6 Å Resolution Karkehabadi, Saeid; Hansson, Henrik; Kim, Steve Journal of Molecular Biology, Vol. 383, Issue 1, p. 144-154 https://doi.org/10.1016/j.jmb.2008.08.016	journal	October 2008
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
High Speed Atomic Force Microscopy Visualizes Processive Movement of Trichoderma reesei Cellobiohydrolase I on Crystalline Cellulose Igarashi, Kiyohiko; Koivula, Anu; Wada, Masahisa Journal of Biological Chemistry, Vol. 284, Issue 52 https://doi.org/10.1074/jbc.M109.034611	journal	October 2009
Hypocrea jecorina CEL6A protein engineering Lantz, Suzanne E.; Goedegebuur, Frits; Hommes, Ronald Biotechnology for Biofuels, Vol. 3, Issue 1, Article No. 20 https://doi.org/10.1186/1754-6834-3-20	journal	September 2010
Identification of a gene coding for a deglycosylating enzyme in Hypocrea jecorina Stals, Ingeborg; Samyn, Bart; Sergeant, Kjell FEMS Microbiology Letters, Vol. 303, Issue 1 https://doi.org/10.1111/j.1574-6968.2009.01849.x	journal	February 2010
Protein glycosylation pathways in filamentous fungi Deshpande, Nandan; Wilkins, Marc R.; Packer, Nicolle Glycobiology, Vol. 18, Issue 8, p. 626-637 https://doi.org/10.1093/glycob/cwn044	journal	May 2008
Stimulation of Lignocellulosic Biomass Hydrolysis by Proteins of Glycoside Hydrolase Family 61 Structure and Function of a Large, Enigmatic Family Harris, Paul; Welner, Ditte; McFarland, K. Biochemistry, Vol. 49, Issue 15, p. 3305-3316 https://doi.org/10.1021/bi100009p	journal	April 2010
Quantitative Proteomic Approach for Cellulose Degradation by Neurospora crassa Phillips, Christopher M.; Iavarone, Anthony T.; Marletta, Michael A. Journal of Proteome Research, Vol. 10, Issue 9 https://doi.org/10.1021/pr200329b	journal	September 2011
Modified glycosylation of cellobiohydrolase I from a high cellulase-producing mutant strain of Trichoderma reesei Harrison, Mathew J.; Nouwens, Amanda S.; Jardine, Daniel R. European Journal of Biochemistry, Vol. 256, Issue 1 https://doi.org/10.1046/j.1432-1327.1998.2560119.x	journal	August 1998
The O-Glycosylated Linker from the Trichoderma reesei Family 7 Cellulase Is a Flexible, Disordered Protein Beckham, Gregg T.; Bomble, Yannick J.; Matthews, James F. Biophysical Journal, Vol. 99, Issue 11 https://doi.org/10.1016/j.bpj.2010.10.032	journal	December 2010
Identification of functionally important amino acids in the cellulose-binding domain of Trichoderma reesei cellobiohydrolase I : Effect of amino acid substitutions on CBHt CBD Linder, Markus; Mattinen, Maija-Liisa; Kontteli, Maarit Protein Science, Vol. 4, Issue 6 https://doi.org/10.1002/pro.5560040604	journal	June 1995
The binding specificity and affinity determinants of family 1 and family 3 cellulose binding modules Lehtio, J.; Sugiyama, J.; Gustavsson, M. Proceedings of the National Academy of Sciences, Vol. 100, Issue 2 https://doi.org/10.1073/pnas.212651999	journal	January 2003
Hypocrea jecorina (Trichoderma reesei) Cel7A as a molecular machine: A docking study Mulakala, Chandrika; Reilly, Peter J. Proteins: Structure, Function, and Bioinformatics, Vol. 60, Issue 4 https://doi.org/10.1002/prot.20547	journal	July 2005
Sugar-binding sites on the surface of the carbohydrate-binding module of CBH I from Trichoderma reesei Tavagnacco, Letizia; Mason, Philip E.; Schnupf, Udo Carbohydrate Research, Vol. 346, Issue 6 https://doi.org/10.1016/j.carres.2011.01.019	journal	May 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
Access to cellulose limits the efficiency of enzymatic hydrolysis: the role of amorphogenesis Arantes, Valdeir; Saddler, Jack N. Biotechnology for Biofuels, Vol. 3, Issue 1 https://doi.org/10.1186/1754-6834-3-4	journal	January 2010
Biological pretreatment of cellulose: Enhancing enzymatic hydrolysis rate using cellulose-binding domains from cellulases Hall, Mélanie; Bansal, Prabuddha; Lee, Jay H. Bioresource Technology, Vol. 102, Issue 3 https://doi.org/10.1016/j.biortech.2010.11.010	journal	February 2011
Applications of computational science for understanding enzymatic deconstruction of cellulose Beckham, Gregg T.; Bomble, Yannick J.; Bayer, Edward A. Current Opinion in Biotechnology, Vol. 22, Issue 2 https://doi.org/10.1016/j.copbio.2010.11.005	journal	April 2011
The Energy Landscape for the Interaction of the Family 1 Carbohydrate-Binding Module and the Cellulose Surface is Altered by Hydrolyzed Glycosidic Bonds Bu, Lintao; Beckham, Gregg T.; Crowley, Michael F. The Journal of Physical Chemistry B, Vol. 113, Issue 31 https://doi.org/10.1021/jp904003z	journal	August 2009
Identification of Amino Acids Responsible for Processivity in a Family 1 Carbohydrate-Binding Module from a Fungal Cellulase Beckham, Gregg T.; Matthews, James F.; Bomble, Yannick J. The Journal of Physical Chemistry B, Vol. 114, Issue 3 https://doi.org/10.1021/jp908810a	journal	January 2010
Systematic survey on crystalline features of algal celluloses Koyama, Makiko; Sugiyana, Junji; Itoh, Takao Cellulose, Vol. 4, Issue 2, p. 147-160 https://doi.org/10.1023/A:1018427604670	journal	January 1997
Molecular Imaging ofHalocynthia papillosaCellulose Helbert, William; Nishiyama, Yoshiharu; Okano, Takeshi Journal of Structural Biology, Vol. 124, Issue 1 https://doi.org/10.1006/jsbi.1998.4045	journal	December 1998
Preferential Uniplanar Orientation of Cellulose Microfibrils Reinvestigated by the FTIR Technique Horikawa, Yoshiki; Itoh, Takao; Sugiyama, Junji Cellulose, Vol. 13, Issue 3 https://doi.org/10.1007/s10570-005-9037-9	journal	April 2006
Structure and properties of the cellulose microfibril Nishiyama, Yoshiharu Journal of Wood Science, Vol. 55, Issue 4 https://doi.org/10.1007/s10086-009-1029-1	journal	August 2009
Nanostructure of cellulose microfibrils in spruce wood Fernandes, A. N.; Thomas, L. H.; Altaner, C. M. Proceedings of the National Academy of Sciences, Vol. 108, Issue 47 https://doi.org/10.1073/pnas.1108942108	journal	November 2011
Computer simulation studies of microcrystalline cellulose Iβ Matthews, James F.; Skopec, Cathy E.; Mason, Philip E. Carbohydrate Research, Vol. 341, Issue 1 https://doi.org/10.1016/j.carres.2005.09.028	journal	January 2006
Molecular-Level Origins of Biomass Recalcitrance: Decrystallization Free Energies for Four Common Cellulose Polymorphs Beckham, Gregg T.; Matthews, James F.; Peters, Baron The Journal of Physical Chemistry B, Vol. 115, Issue 14 https://doi.org/10.1021/jp1106394	journal	April 2011
Probing Carbohydrate Product Expulsion from a Processive Cellulase with Multiple Absolute Binding Free Energy Methods Bu, Lintao; Beckham, Gregg T.; Shirts, Michael R. Journal of Biological Chemistry, Vol. 286, Issue 20 https://doi.org/10.1074/jbc.M110.212076	journal	March 2011
Restructuring the Crystalline Cellulose Hydrogen Bond Network Enhances Its Depolymerization Rate Chundawat, Shishir P. S.; Bellesia, Giovanni; Uppugundla, Nirmal Journal of the American Chemical Society, Vol. 133, Issue 29 https://doi.org/10.1021/ja2011115	journal	July 2011
Decrystallization of Oligosaccharides from the Cellulose Iβ Surface with Molecular Simulation Payne, Christina M.; Himmel, Michael E.; Crowley, Michael F. The Journal of Physical Chemistry Letters, Vol. 2, Issue 13 https://doi.org/10.1021/jz2005122	journal	June 2011
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
Comparison of Cellulose Iβ Simulations with Three Carbohydrate Force Fields Matthews, James F.; Beckham, Gregg T.; Bergenstråhle-Wohlert, Malin Journal of Chemical Theory and Computation, Vol. 8, Issue 2 https://doi.org/10.1021/ct2007692	journal	January 2012
Clustering Molecular Dynamics Trajectories: 1. Characterizing the Performance of Different Clustering Algorithms Shao, Jianyin; Tanner, Stephen W.; Thompson, Nephi Journal of Chemical Theory and Computation, Vol. 3, Issue 6 https://doi.org/10.1021/ct700119m	journal	October 2007
Surface Diffusion of Cellulases and Their Isolated Binding Domains on Cellulose Jervis, Eric J.; Haynes, Charles A.; Kilburn, Douglas G. Journal of Biological Chemistry, Vol. 272, Issue 38 https://doi.org/10.1074/jbc.272.38.24016	journal	September 1997
All-Atom Empirical Potential for Molecular Modeling and Dynamics Studies of Proteins ^† MacKerell, A. D.; Bashford, D.; Bellott, M. The Journal of Physical Chemistry B, Vol. 102, Issue 18 https://doi.org/10.1021/jp973084f	journal	April 1998
Extending the treatment of backbone energetics in protein force fields: Limitations of gas-phase quantum mechanics in reproducing protein conformational distributions in molecular dynamics simulations Mackerell, Alexander D.; Feig, Michael; Brooks, Charles L. Journal of Computational Chemistry, Vol. 25, Issue 11 https://doi.org/10.1002/jcc.20065	journal	August 2004
Comparison of simple potential functions for simulating liquid water Jorgensen, William L.; Chandrasekhar, Jayaraman; Madura, Jeffry D. The Journal of Chemical Physics, Vol. 79, Issue 2 https://doi.org/10.1063/1.445869	journal	July 1983
Solvent-Induced Forces between Two Hydrophilic Groups Durell, Stewart R.; Brooks, Bernard R.; Ben-Naim, Arieh The Journal of Physical Chemistry, Vol. 98, Issue 8 https://doi.org/10.1021/j100059a038	journal	February 1994
Additive empirical force field for hexopyranose monosaccharides Guvench, Olgun; Greene, Shannon N.; Kamath, Ganesh Journal of Computational Chemistry, Vol. 29, Issue 15 https://doi.org/10.1002/jcc.21004	journal	November 2008
CHARMM Additive All-Atom Force Field for Glycosidic Linkages between Hexopyranoses Guvench, Olgun; Hatcher, Elizabeth; Venable, Richard M. Journal of Chemical Theory and Computation, Vol. 5, Issue 9 https://doi.org/10.1021/ct900242e	journal	August 2009
CHAMBER: Comprehensive support for CHARMM force fields within the AMBER software Crowley, Michael F.; Williamson, Mark J.; Walker, Ross C. International Journal of Quantum Chemistry, Vol. 109, Issue 15 https://doi.org/10.1002/qua.22372	journal	December 2009
The Amber biomolecular simulation programs Case, David A.; Cheatham, Thomas E.; Darden, Tom Journal of Computational Chemistry, Vol. 26, Issue 16 https://doi.org/10.1002/jcc.20290	journal	January 2005
Numerical integration of the cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes Ryckaert, Jean-Paul; Ciccotti, Giovanni; Berendsen, Herman J. C. Journal of Computational Physics, Vol. 23, Issue 3 https://doi.org/10.1016/0021-9991(77)90098-5	journal	March 1977
A smooth particle mesh Ewald method Essmann, Ulrich; Perera, Lalith; Berkowitz, Max L. The Journal of Chemical Physics, Vol. 103, Issue 19 https://doi.org/10.1063/1.470117	journal	November 1995
Crystal Structure and Pair Potentials: A Molecular-Dynamics Study Parrinello, M.; Rahman, A. Physical Review Letters, Vol. 45, Issue 14 https://doi.org/10.1103/PhysRevLett.45.1196	journal	October 1980
Constant pressure molecular dynamics for molecular systems Nosé, Shuichi; Klein, M. L. Molecular Physics, Vol. 50, Issue 5 https://doi.org/10.1080/00268978300102851	journal	December 1983
Canonical dynamics: Equilibrium phase-space distributions Hoover, William G. Physical Review A, Vol. 31, Issue 3 https://doi.org/10.1103/PhysRevA.31.1695	journal	March 1985
Nonphysical sampling distributions in Monte Carlo free-energy estimation: Umbrella sampling Torrie, G. M.; Valleau, J. P. Journal of Computational Physics, Vol. 23, Issue 2 https://doi.org/10.1016/0021-9991(77)90121-8	journal	February 1977
Dynamics of ligand escape from the heme pocket of myoglobin Kottalam, J.; Case, David A. Journal of the American Chemical Society, Vol. 110, Issue 23 https://doi.org/10.1021/ja00231a018	journal	November 1988
THE weighted histogram analysis method for free-energy calculations on biomolecules. I. The method Kumar, Shankar; Rosenberg, John M.; Bouzida, Djamal Journal of Computational Chemistry, Vol. 13, Issue 8 https://doi.org/10.1002/jcc.540130812	journal	October 1992

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09 BIOMASS FUELS
37 INORGANIC
ORGANIC
PHYSICAL AND ANALYTICAL CHEMISTRY
59 BASIC BIOLOGICAL SCIENCES
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CARBOHYDRATES
CELLULASE
CELLULOSE
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PROTEIN STRUCTURE
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TRICHODERMA VIRIDE
cellulase
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Title: Binding Preferences, Surface Attachment, Diffusivity, and Orientation of a Family 1 Carbohydrate-Binding Module on Cellulose

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