Building a Foundation for Structure-Based Cellulosome Design for Cellulosic Ethanol: Insight into Cohesin-Dockerin Complexation from Computer Simulation

Xu, Jiancong; Crowley, Michael F.; Smith, Jeremy C.

doi:10.1002/pro.105

Building a Foundation for Structure-Based Cellulosome Design for Cellulosic Ethanol: Insight into Cohesin-Dockerin Complexation from Computer Simulation

Journal Article · Thu Jan 01 04:00:00 EST 2009 · Protein Science

DOI:https://doi.org/10.1002/pro.105· OSTI ID:1021221

Xu, Jiancong; Crowley, Michael F.; Smith, Jeremy C.

The organization and assembly of the cellulosome, an extracellular multienzyme complex produced by anaerobic bacteria, is mediated by the high-affinity interaction of cohesin domains from scaffolding proteins with dockerins of cellulosomal enzymes. We have performed molecular dynamics simulations and free energy calculations on both the wild type (WT) and D39N mutant of the C. thermocellum Type I cohesin-dockerin complex in aqueous solution. The D39N mutation has been experimentally demonstrated to disrupt cohesin-dockerin binding. The present MD simulations indicate that the substitution triggers significant protein flexibility and causes a major change of the hydrogen-bonding network in the recognition strips - the conserved loop regions previously proposed to be involved in binding - through electrostatic and salt-bridge interactions between {beta}-strands 3 and 5 of the cohesin and {alpha}-helix 3 of the dockerin. The mutation-induced subtle disturbance in the local hydrogen-bond network is accompanied by conformational rearrangements of the protein side chains and bound water molecules. Additional free energy perturbation calculations of the D39N mutation provide differences in the cohesin-dockerin binding energy, thus offering a direct, quantitative comparison with experiments. The underlying molecular mechanism of cohesin-dockerin complexation is further investigated through the free energy profile, that is, potential of mean force (PMF) calculations of WT cohesin-dockerin complex. The PMF shows a high-free energy barrier against the dissociation and reveals a stepwise pattern involving both the central {beta}-sheet interface and its adjacent solvent-exposed loop/turn regions clustered at both ends of the {beta}-barrel structure.

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

Sponsoring Organization:: USDOE Office of Science, Office of Biological and Environmental Research

DOE Contract Number:: AC36-08GO28308

OSTI ID:: 1021221

Report Number(s):: NREL/JA-270-46148; MainId:48788; UUID:fae0c73c-bcd4-e411-b769-d89d67132a6d; MainAdminId:30880

Journal Information:: Protein Science, Journal Name: Protein Science Journal Issue: 5 Vol. 18

Country of Publication:: United States

Language:: English

References (48)

Solution Structure of a Type I Dockerin Domain, a Novel Prokaryotic, Extracellular Calcium-binding Domain11Edited by P. E. Wright Lytle, Betsy L.; Volkman, Brian F.; Westler, William M. Journal of Molecular Biology, Vol. 307, Issue 3 https://doi.org/10.1006/jmbi.2001.4522	journal	March 2001
Revisiting Free Energy Calculations: A Theoretical Connection to MM/PBSA and Direct Calculation of the Association Free Energy Swanson, Jessica M. J.; Henchman, Richard H.; McCammon, J. Andrew Biophysical Journal, Vol. 86, Issue 1 https://doi.org/10.1016/S0006-3495(04)74084-9	journal	January 2004
VMD: Visual molecular dynamics Humphrey, William; Dalke, Andrew; Schulten, Klaus Journal of Molecular Graphics, Vol. 14, Issue 1 https://doi.org/10.1016/0263-7855(96)00018-5	journal	February 1996
Calcium-binding affinity and calcium-enhanced activity of Clostridium thermocellum endoglucanase D Chauvaux, S.; Beguin, P.; Aubert, J. P. Biochemical Journal, Vol. 265, Issue 1 https://doi.org/10.1042/bj2650261	journal	January 1990
Crystal structure of a cohesin module from Clostridium cellulolyticum: implications for dockerin recognition Spinelli, Silvia; Fiérobe, Henri-Pierre; Belaı̈ch, Anne Journal of Molecular Biology, Vol. 304, Issue 2 https://doi.org/10.1006/jmbi.2000.4191	journal	November 2000
A cohesin domain from Clostridium thermocellum: the crystal structure provides new insights into cellulosome assembly Shimon, Linda JW; Bayer, Edward A.; Morag, Ely Structure, Vol. 5, Issue 3 https://doi.org/10.1016/S0969-2126(97)00195-0	journal	March 1997
Cohesin–dockerin interaction in cellulosome assembly: a single Asp‐to‐Asn mutation disrupts high‐affinity cohesin–dockerin binding Handelsman, Tal; Barak, Yoav; Nakar, David FEBS Letters, Vol. 572, Issue 1-3 https://doi.org/10.1016/j.febslet.2004.07.040	journal	July 2004
Constant pressure molecular dynamics simulation: The Langevin piston method Feller, Scott E.; Zhang, Yuhong; Pastor, Richard W. The Journal of Chemical Physics, Vol. 103, Issue 11 https://doi.org/10.1063/1.470648	journal	September 1995
Involvement of Both Dockerin Subdomains in Assembly of the Clostridium thermocellum Cellulosome Lytle, Betsy; Wu, J. H. David Journal of Bacteriology, Vol. 180, Issue 24 https://doi.org/10.1128/JB.180.24.6581-6585.1998	journal	December 1998
The statistical-thermodynamic basis for computation of binding affinities: a critical review Gilson, M. K.; Given, J. A.; Bush, B. L. Biophysical Journal, Vol. 72, Issue 3 https://doi.org/10.1016/S0006-3495(97)78756-3	journal	March 1997
Stabilization of protein structure by interaction of α-helix dipole with a charged side chain S˘ali, Das̆a; Bycroft, Mark; Fersht, Alan R. Nature, Vol. 335, Issue 6192 https://doi.org/10.1038/335740a0	journal	October 1988
The potential of cellulases and cellulosomes for cellulosic waste management Bayer, Edward A.; Lamed, Raphael; Himmel, Michael E. Current Opinion in Biotechnology, Vol. 18, Issue 3 https://doi.org/10.1016/j.copbio.2007.04.004	journal	June 2007
Method for estimating the configurational entropy of macromolecules Karplus, Martin; Kushick, Joseph N. Macromolecules, Vol. 14, Issue 2 https://doi.org/10.1021/ma50003a019	journal	March 1981
Mapping by Site-Directed Mutagenesis of the Region Responsible for Cohesin−Dockerin Interaction on the Surface of the Seventh Cohesin Domain of Clostridium thermocellum CipA Miras, Isabelle; Schaeffer, Francis; Béguin, Pierre Biochemistry, Vol. 41, Issue 7 https://doi.org/10.1021/bi011854e	journal	January 2002
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
Cellulosomes from Mesophilic Bacteria Doi, Roy H.; Kosugi, Akihiko; Murashima, Koichiro Journal of Bacteriology, Vol. 185, Issue 20 https://doi.org/10.1128/JB.185.20.5907-5914.2003	journal	October 2003
Incorporating the effect of ionic strength in free energy calculations using explicit ions Donnini, Serena; Mark, Alan E.; Juffer, André H. Journal of Computational Chemistry, Vol. 26, Issue 2 https://doi.org/10.1002/jcc.20156	journal	December 2004
Evidence for a dual binding mode of dockerin modules to cohesins Carvalho, A. L.; Dias, F. M. V.; Nagy, T. Proceedings of the National Academy of Sciences, Vol. 104, Issue 9 https://doi.org/10.1073/pnas.0611173104	journal	February 2007
Scalable molecular dynamics with NAMD Phillips, James C.; Braun, Rosemary; Wang, Wei Journal of Computational Chemistry, Vol. 26, Issue 16, p. 1781-1802 https://doi.org/10.1002/jcc.20289	journal	January 2005
Cohesin-dockerin recognition in cellulosome assembly: Experiment versus hypothesis Mechaly, Adva; Yaron, Sima; Lamed, Raphael Proteins: Structure, Function, and Genetics, Vol. 39, Issue 2 https://doi.org/10.1002/(SICI)1097-0134(20000501)39:2<170::AID-PROT7>3.0.CO;2-H	journal	May 2000
Collective motions in proteins: A covariance analysis of atomic fluctuations in molecular dynamics and normal mode simulations Ichiye, Toshiko; Karplus, Martin Proteins: Structure, Function, and Genetics, Vol. 11, Issue 3 https://doi.org/10.1002/prot.340110305	journal	November 1991
Species-specificity of the cohesin-dockerin interaction betweenClostridium thermocellum andClostridium cellulolyticum: Prediction of specificity determinants of the dockerin domain Pagès, Sandrine; Bélaïch, Anne; Bélaïch, Jean-Pierre Proteins: Structure, Function, and Genetics, Vol. 29, Issue 4 https://doi.org/10.1002/(SICI)1097-0134(199712)29:4<517::AID-PROT11>3.0.CO;2-P	journal	December 1997
Calculating free energies using average force Darve, Eric; Pohorille, Andrew The Journal of Chemical Physics, Vol. 115, Issue 20 https://doi.org/10.1063/1.1410978	journal	November 2001
Calculation of absolute protein-ligand binding free energy from computer simulations Woo, H. -J.; Roux, B. Proceedings of the National Academy of Sciences, Vol. 102, Issue 19 https://doi.org/10.1073/pnas.0409005102	journal	May 2005
Binding Free Energy Differences in a TCR–Peptide-MHC Complex Induced by a Peptide Mutation: A Simulation Analysis Michielin, Olivier; Karplus, Martin Journal of Molecular Biology, Vol. 324, Issue 3 https://doi.org/10.1016/S0022-2836(02)00880-X	journal	November 2002
The role of the α-helix dipole in protein function and structure Hol, Wim G. J. Progress in Biophysics and Molecular Biology, Vol. 45, Issue 3 https://doi.org/10.1016/0079-6107(85)90001-X	journal	January 1985
Particle mesh Ewald: An N ⋅log( N ) method for Ewald sums in large systems Darden, Tom; York, Darrin; Pedersen, Lee The Journal of Chemical Physics, Vol. 98, Issue 12 https://doi.org/10.1063/1.464397	journal	June 1993
The crystal structure of a type I cohesin domain at 1.7 Å resolution 1 1Edited by D. Rees Tavares, Gisele A.; Béguin, Pierre; Alzari, Pedro M. Journal of Molecular Biology, Vol. 273, Issue 3 https://doi.org/10.1006/jmbi.1997.1326	journal	October 1997
Probing a Model of a GPCR/Ligand Complex in an Explicit Membrane Environment: The Human Cholecystokinin-1 Receptor Hénin, Jérôme; Maigret, Bernard; Tarek, Mounir Biophysical Journal, Vol. 90, Issue 4 https://doi.org/10.1529/biophysj.105.070599	journal	February 2006
The α Helix Dipole: Screened Out? Sengupta, Durba; Behera, Raghu Nath; Smith, Jeremy C. Structure, Vol. 13, Issue 6 https://doi.org/10.1016/j.str.2005.03.010	journal	June 2005
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
Constant pressure molecular dynamics algorithms Martyna, Glenn J.; Tobias, Douglas J.; Klein, Michael L. The Journal of Chemical Physics, Vol. 101, Issue 5 https://doi.org/10.1063/1.467468	journal	September 1994
Computational Alchemy Straatsma, T. P.; McCammon, J. A. Annual Review of Physical Chemistry, Vol. 43, Issue 1 https://doi.org/10.1146/annurev.pc.43.100192.002203	journal	October 1992
GROMACS: Fast, flexible, and free Van Der Spoel, David; Lindahl, Erik; Hess, Berk Journal of Computational Chemistry, Vol. 26, Issue 16 https://doi.org/10.1002/jcc.20291	journal	January 2005
Free energy calculations: Applications to chemical and biochemical phenomena Kollman, Peter. Chemical Reviews, Vol. 93, Issue 7 https://doi.org/10.1021/cr00023a004	journal	November 1993
On the calculation of absolute macromolecular binding free energies Luo, Hengbin; Sharp, Kim Proceedings of the National Academy of Sciences, Vol. 99, Issue 16 https://doi.org/10.1073/pnas.162365999	journal	July 2002
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
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
Cellulosome assembly revealed by the crystal structure of the cohesin-dockerin complex Carvalho, A. L.; Dias, F. M. V.; Prates, J. A. M. Proceedings of the National Academy of Sciences, Vol. 100, Issue 24 https://doi.org/10.1073/pnas.1936124100	journal	November 2003
Overcoming free energy barriers using unconstrained molecular dynamics simulations Hénin, Jérôme; Chipot, Christophe The Journal of Chemical Physics, Vol. 121, Issue 7 https://doi.org/10.1063/1.1773132	journal	August 2004
Assessing the efficiency of free energy calculation methods Rodriguez-Gomez, David; Darve, Eric; Pohorille, Andrew The Journal of Chemical Physics, Vol. 120, Issue 8 https://doi.org/10.1063/1.1642607	journal	February 2004
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
Effect of Solvent on Collective Motions in Globular Protein Hayward, S.; Kitao, Akio; Hirata, Fumio Journal of Molecular Biology, Vol. 234, Issue 4 https://doi.org/10.1006/jmbi.1993.1671	journal	December 1993
Secondary Structure and Calcium-Induced Folding of the Clostridium thermocellum Dockerin Domain Determined by NMR Spectroscopy Lytle, Betsy L.; Volkman, Brian F.; Westler, William M. Archives of Biochemistry and Biophysics, Vol. 379, Issue 2 https://doi.org/10.1006/abbi.2000.1882	journal	July 2000
Organization and distribution of the cellulosome in Clostridium thermocellum. Bayer, E. A.; Setter, E.; Lamed, R. Journal of Bacteriology, Vol. 163, Issue 2 https://doi.org/10.1128/JB.163.2.552-559.1985	journal	January 1985
Analysis of a 10-ns Molecular Dynamics Simulation of Mouse Acetylcholinesterase Tai, Kaihsu; Shen, Tongye; Börjesson, Ulf Biophysical Journal, Vol. 81, Issue 2 https://doi.org/10.1016/S0006-3495(01)75736-0	journal	August 2001
Structural Basis of Cellulosome Efficiency Explored by Small Angle X-ray Scattering Hammel, Michal; Fierobe, Henri-Pierre; Czjzek, Mirjam Journal of Biological Chemistry, Vol. 280, Issue 46 https://doi.org/10.1074/jbc.M503168200	journal	September 2005
Duplicated Dockerin Subdomains of Clostridium thermocellum Endoglucanase CelD Bind to a Cohesin Domain of the Scaffolding Protein CipA with Distinct Thermodynamic Parameters and a Negative Cooperativity ^† Schaeffer, Francis; Matuschek, Markus; Guglielmi, Gérard Biochemistry, Vol. 41, Issue 7 https://doi.org/10.1021/bi011853m	journal	February 2002

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AQUEOUS SOLUTIONS
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COMPUTERIZED SIMULATION
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Building a Foundation for Structure-Based Cellulosome Design for Cellulosic Ethanol: Insight into Cohesin-Dockerin Complexation from Computer Simulation

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