Unraveling the role of the protein environment for [FeFe]-hydrogenase: A new application of coarse-graining

Journal of Physical Chemistry B

Volumn 117, Issue 15, 2013, Pages 4062-4071

  McCullagh, Martin ^a   Voth, Gregory A ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOMIMETICS; ELECTRON TRANSPORT PROPERTIES; ENZYMES; FREE ENERGY; MOLECULAR DYNAMICS; PROTONS;

BIOMIMETIC DEVICES; CONCERTED MECHANISM; COUPLED MECHANISMS; ELECTRON TRANSPORT; ELECTROSTATIC POTENTIALS; HYDROGENASE ENZYMES; RELATIVE FREE ENERGY; REORGANIZATION ENERGIES;

PROTEINS;

EID: 84876488438     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp402441s     Document Type: Article

References (57)

1. Ross, D. Hydrogen storage: The Major Technological Barrier to the Development of Hydrogen Fuel Cell Cars Vacuum 2006, 80, 1084-1089
2. Ahluwalia, R.; Wang, X.; Rousseau, A. Fuel Economy of Hydrogen Fuel Cell Vehicles J. Power Sources 2004, 130, 192-201
3. Granovskii, M.; Dincer, I.; Rosen, M. A. Economic and Environmental Comparison of Conventional, Hybrid, Electric and Hydrogen Fuel Cell Vehicles J. Power Sources 2006, 159, 1186-1193
4. Blankenship, R. E.; Tiede, D. M.; Barber, J.; Brudvig, G. W.; Fleming, G.; Ghirardi, M.; Gunner, M. R.; Junge, W.; Kramer, D. M.; Melis, A. Comparing Photosynthetic and Photovoltaic Efficiencies and Recognizing the Potential for Improvement Science 2011, 332, 805-809
5. Yacoby, I.; Pochekailov, S.; Toporik, H.; Ghirardi, M. L.; King, P. W.; Zhang, S. Photosynthetic Electron Partitioning between [FeFe]-Hydrogenase and Ferredoxin:NADP+-oxidoreductase (FNR) Enzymes in Vitro Proc. Natl. Acad. Sci. U.S.A. 2011, 108, 9396-9401
6. 4 Photoelectrodes for Solar Water Oxidation Energy Environ. Sci. 2011, 4, 5028
7. Lalaurette, E.; Thammannagowda, S.; Mohagheghi, A.; Maness, P.-C.; Logan, B. E. Hydrogen Production from Cellulose in a Two-Stage Process Combining Fermentation and Electrohydrogenesis Int. J. Hydrogen Energy 2009, 34, 6201-6210
8. NREL: Hydrogen and Fuel Cells Research-Hydrogen Production and Delivery. http://www.nrel.gov/hydrogen/proj-production-delivery.html#split (accessed Jul 4, 2012).
9. Frey, M. Hydrogenases: Hydrogen-Activating Enzymes ChemBioChem 2012, 3, 153-160
10. Adams, M. W. The Structure and Mechanism of Iron-hydrogenases Biochim. Biophys. Acta 1990, 1020, 115-145
11. 2-Tolerant Membrane Bound [NiFe] Hydrogenase of R. eutropha H16 by Molecular Modelling Phys. Chem. Chem. Phys. 2011, 13, 16146-16149
12. 2 Toward the Active Site of [NiFe]-Hydrogenase Biophys. J. 2006, 91, 2035-2045
13. Sumner, I.; Voth, G. A. Proton Transport Pathways in [NiFe]-Hydrogenase J. Phys. Chem. B 2012, 116, 2917-2926
14. Smith, D. M. A.; Xiong, Y.; Straatsma, T. P.; Rosso, K. M.; Squier, T. C. Force-Field Development and Molecular Dynamics of [NiFe] Hydrogenase J. Chem. Theory Comput. 2012, 8, 2103-2114
15. Greene, B. L.; Joseph, C. A.; Maroney, M. J.; Dyer, R. B. Direct Evidence of Active-Site Reduction and Photodriven Catalysis in Sensitized Hydrogenase Assemblies J. Am. Chem. Soc. 2012, 134, 11108-11111
16. Wang, P.-H.; Blumberger, J. Mechanistic Insight into the Blocking of CO Diffusion in [NiFe]-Hydrogenase Mutants through Multiscale Simulation Proc. Natl. Acad. Sci. U.S.A. 2012, 109, 6399-6404
17. Stripp, S.; Goldet, G.; Brandmayr, C. How Oxygen Attacks [FeFe] Hydrogenases from Photosynthetic Organisms Proc. Natl. Acad. Sci. U.S.A. 2009, 106, 17331-17336
18. Peters, J. W.; Lanzilotta, W. N.; Lemon, B. J.; Seefeldt, L. C. X-ray Crystal Structure of the Fe-Only Hydrogenase (CpI) from Clostridium pasteurianum to 1.8 Angstrom Resolution Science 1998, 282, 1853-1858
19. Fdez Galván, I.; Volbeda, A.; Fontecilla-Camps, J. C.; Field, M. J. A QM/MM Study of Proton Transport Pathways in a [NiFe] Hydrogenase Proteins 2008, 73, 195-203
20. Nicolet, Y.; Piras, C.; Legrand, P.; Hatchikian, C. E.; Fontecilla-Camps, J. C. Desulfovibrio Desulfuricans Iron Hydrogenase: The Structure Shows Unusual Coordination to an Active Site Fe Binuclear Center Structure 1999, 7, 13-23
21. Peters, J. W.; Lanzilotta, W. N.; Lemon, B. J.; Seefeldt, L. C. X-ray Crystal Structure of the Fe-Only Hydrogenase (CpI) from Clostridium pasteurianum to 1.8 Angstrom Resolution Science 1998, 282, 1853-1858
22. Nicolet, Y.; Fontecilla-Camps, J. C. Structure-Function Relationships in [FeFe]-Hydrogenase Active Site Maturation J. Biol. Chem. 2012, 287, 13532-13540
23. Pandey, A. S.; Harris, T. V.; Giles, L. J.; Peters, J. W.; Szilagyi, R. K. Dithiomethylether as a Ligand in the Hydrogenase H-Cluster J. Am. Chem. Soc. 2008, 130, 4533-4540
24. 2 Production using [FeFe]-Hydrogenase Active Site Mimics Dalton Trans. 2011, 40, 12793-12800
25. Teets, T. S.; Nocera, D. G. Photocatalytic Hydrogen Production Chem. Commun. 2011, 47, 9268-9274
26. Matthews, S. L.; Heinekey, D. M. An Oxidized Active Site Model for the FeFe Hydrogenase: Reduction with Hydrogen Gas Inorg. Chem. 2011, 50, 7925-7927
27. 2 Production and Uptake Science 2009, 326, 1384-1387
28. Knörzer, P.; Silakov, A.; Foster, C. E.; Armstrong, F. A.; Lubitz, W.; Happe, T. Importance of the Protein Framework for Catalytic Activity of [FeFe]-Hydrogenases J. Biol. Chem. 2012, 287, 1489-1499
29. De Lacey, A. L.; Fernández, V. M.; Rousset, M.; Cammack, R. Activation and Inactivation of Hydrogenase Function and the Catalytic Cycle: Spectroelectrochemical Studies Chem. Rev. 2007, 107, 4304-4330
30. Mulder, D. W.; Shepard, E. M.; Meuser, J. E.; Joshi, N.; King, P. W.; Posewitz, M. C.; Broderick, J. B.; Peters, J. W. Insights into [FeFe]-Hydrogenase Structure, Mechanism, and Maturation Structure 2011, 19, 1038-1052
31. Zhang, Z.; Lu, L.; Noid, W. G.; Krishna, V.; Pfaendtner, J.; Voth, G. A. A Systematic Methodology for Defining Coarse-Grained Sites in Large Biomolecules Biophys. J. 2008, 95, 5073-5083
32. Zhang, Z.; Voth, G. A. Coarse-Grained Representations of Large Biomolecular Complexes from Low-Resolution Structural Data J. Chem. Theory Comput. 2010, 6, 2990-3002
33. MacKerell, A. D.; Bashford, D.; Bellott; Dunbrack, R. L.; Evanseck, J. D.; Field, M. J.; Fischer, S.; Gao, J.; Guo, H.; Ha, S.; Joseph-McCarthy, D.; Kuchnir, L.; Kuczera, K.; Lau, F. T. K.; Mattos, C.; Michnick, S.; Ngo, T.; Nguyen, D. T.; Prodhom, B.; Reiher, W. E.; Roux, B.; Schlenkrich, M.; Smith, J. C.; Stote, R.; Straub, J.; Watanabe, M.; Wiórkiewicz-Kuczera, J.; Yin, D.; Karplus, M. All-Atom Empirical Potential for Molecular Modeling and Dynamics Studies of Proteins J. Phys. Chem. B 1998, 102, 3586-3616
34. MacKerell, A. D.; Feig, M.; Brooks, C. L. Improved Treatment of the Protein Backbone in Empirical Force Fields J. Am. Chem. Soc. 2004, 126, 698-699
35. Chang, C. H.; Kim, K. Density Functional Theory Calculation of Bonding and Charge Parameters for Molecular Dynamics Studies on [FeFe] Hydrogenases J. Chem. Theory Comput. 2009, 5, 1137-1145
36. Phillips, J. C.; Braun, R.; Wang, W.; Gumbart, J.; Tajkhorshid, E.; Villa, E.; Chipot, C.; Skeel, R. D.; Kalé, L.; Schulten, K. Scalable Molecular Dynamics with NAMD J. Comput. Chem. 2005, 26, 1781-1802
37. Kalé, L.; Skeel, R.; Bhandarkar, M.; Brunner, R.; Gursoy, A.; Krawetz, N.; Phillips, J.; Shinozaki, A.; Varadarajan, K.; Schulten, K. NAMD2: Greater Scalability for Parallel Molecular Dynamics J. Comput. Phys. 1999, 151, 283-312
38. Zhang, Z.; Lu, L.; Noid, W. G.; Krishna, V.; Pfaendtner, J.; Voth, G. A. A Systematic Methodology for Defining Coarse-Grained Sites in Large Biomolecules Biophys. J. 2008, 95, 5073-5083
39. Sinitskiy, A. V.; Saunders, M. G.; Voth, G. A. Optimal Number of Coarse-Grained Sites in Different Components of Large Biomolecular Complexes J. Phys. Chem. B 2012, 116, 8363-8374
40. Marcus, R. A.; Sutin, N. Electron Transfers in Chemistry and Biology Biochim. Biophys. Acta 1985, 811, 265-322
41. Small, D. W.; Matyushov, D. V.; Voth, G. A. The Theory of Electron Transfer Reactions: What May Be Missing? J. Am. Chem. Soc. 2003, 125, 7470-7478
42. Matyushov, D. V.; Voth, G. A. Modeling the Free Energy Surfaces of Electron Transfer in Condensed Phases J. Chem. Phys. 2000, 113, 5413-5424
43. Reed, S. K.; Madden, P. A.; Papadopoulos, A. Electrochemical Charge Transfer at a Metallic Electrode: A Simulation Study J. Chem. Phys. 2008, 128, 124701
44. Heck, A.; Woiczikowski, P. B.; Kubař, T.; Giese, B.; Elstner, M.; Steinbrecher, T. B. Charge Transfer in Model Peptides: Obtaining Marcus Parameters from Molecular Simulation J. Phys. Chem. B 2012, 116, 2284-2293
45. King, G.; Warshel, A. Investigation of the Free Energy Functions for Electron Transfer Reactions J. Chem. Phys. 1990, 93, 8682
46. Greco, C.; Bruschi, M.; De Gioia, L.; Ryde, U. A QM/MM Investigation of the Activation and Catalytic Mechanism of Fe-Only Hydrogenases Inorg. Chem. 2007, 46, 5911-5921
47. Chang, C. H. Computational Chemical Analysis of [FeFe] Hydrogenase H-Cluster Analogues to Discern Catalytically Relevant Features of the Natural Diatomic Ligand Configuration J. Phys. Chem. A 2011, 115, 8691-8704
48. Siegbahn, P. E. M.; Tye, J. W.; Hall, M. B. Computational Studies of [NiFe] and [FeFe] Hydrogenases Chem. Rev. 2007, 107, 4414-4435
49. Basu, G.; Kitao, A.; Kuki, A.; Go, N. Protein Electron Transfer Reorganization Energy Spectrum from Normal Mode Analysis. 1. Theory J. Phys. Chem. B 1998, 102, 2076-2084
50. Arcangeli, C.; Bizzarri, A. R.; Cannistraro, S. Concerted Motions in Copper Plastocyanin and Azurin: An Essential Dynamics Study Biophys. Chem. 2001, 90, 45-56
51. Gray, H. B.; Winkler, J. R. Electron Transfer in Proteins Annu. Rev. Biochem. 1996, 65, 537-361
52. Dementin, S.; Burlat, B.; Fourmond, V.; Leroux, F.; Liebgott, P.-P.; Abou Hamdan, A.; Léger, C.; Rousset, M.; Guigliarelli, B.; Bertrand, P. Rates of Intra- and Intermolecular Electron Transfers in Hydrogenase Deduced from Steady-State Activity Measurements J. Am. Chem. Soc. 2011, 133, 10211-10221
53. Zarzycki, P.; Kerisit, S.; Rosso, K. Computational Methods for Intramolecular Electron Transfer in a Ferrous-Ferric iron Complex J. Colloid Interface Sci. 2011, 361, 293-306
54. Blumberger, J. Free Energies for Biological Electron Transfer from QM/MM Calculation: Method, Application and Critical Assessment Phys. Chem. Chem. Phys. 2008, 10, 5651-5667
55. LeBard, D. N.; Matyushov, D. V. Glassy Protein Dynamics and Gigantic Solvent Reorganization Energy of Plastocyanin J. Phys. Chem. B 2008, 112, 5218-5227
56. Jorgensen, W. L.; Chandrasekhar, J.; Madura, J. D.; Impey, R. W.; Klein, M. L. Comparison of Simple Potential Functions for Simulating Liquid Water J. Chem. Phys. 1983, 79, 926-935
57. Cornish, A. J.; Gartner, K.; Yang, H.; Peters, J. W.; Hegg, E. L. Mechanism of Proton Transfer in [FeFe]-Hydrogenase from Clostridium pasteurianum J. Biol. Chem. 2011, 286, 38341-38347