Mechanism of hydrogen production in [Fe-Fe]-hydrogenases: A quantum mechanics/molecular mechanics study

International Journal of Hydrogen Energy

Volumn 35, Issue 11, 2010, Pages 5318-5331

  Trohalaki, Steven ^a,b   Pachter, Ruth ^a,b  

^a AIR FORCE RESEARCH LABORATORY   (United States)

^b GENERAL DYNAMICS   (United States)

Author keywords

All iron hydrogenase; Hydrogen production; Hydrogenase mechanism; QM MM

Indexed keywords

ACTIVE SITE; ACTIVE SITE STRUCTURE; CATALYTIC MECHANISMS; CLOSTRIDIUM PASTEURIANUM; DESULFOVIBRIO DESULFURICANS; HIGH ACTIVATION ENERGY; HYDROGENASE MECHANISM; HYDROGENASES; LOWER ENERGIES; METALLOENZYMES; QM/MM; QM/MM METHOD;

ACTIVATION ENERGY; DENSITY FUNCTIONAL THEORY; GAS PRODUCERS; IRON ALLOYS;

HYDROGEN PRODUCTION;

EID: 77955300546     PISSN: 03603199     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijhydene.2010.03.020     Document Type: Article

References (65)

1. R. Cammack, M. Frey, and R.L. Robson Hydrogen as a fuel: learning from nature 2001 Taylor & Francis London and New York
2. M.W.W. Adams The structure and mechanism of iron-hydrogenases Biochim Biophys Acta 1020 1990 115 145
3. 2 production using the green microalga Chlamydomonas reinhardtii in a fully controlled photobioreactor fitted with on-line gas analysis Int J Hydrogen Energy 33 2008 3302 3310
4. J.H. Jo, C.O. Jeon, S.Y. Lee, D.S. Lee, and J.M. Park Molecular characterization and homologous overexpression of [FeFe]-hydrogenase in Clostridium tyrobutyricum JM1 Int J Hydrogen Energy 35 2010 1065 1073
5. F.A. Armstrong, N.A. Belsey, J.A. Cracknell, G. Goldet, A. Parkin, and E. Reisner Dynamic electrochemical investigations of hydrogen oxidation and production by enzymes and implications for future technology Chem Soc Rev 38 2009 36 51
6. 2-photoproducing organisms and processes Biochem Soc Trans 33 2005 70 72
7. K.A. Vincent, A. Parkin, O. Lenz, S.P.J. Albracht, J.C. Fontecilla-Camps, and R. Cammack Electrochemical definitions of O2 sensitivity and oxidative inactivation in hydrogenases J Am Chem Soc 127 2005 18179 18189
8. S.C.E. Tosatto, S. Toppo, D. Carbonera, G.M. Giacometti, and P. Costantini Comparative analysis of [FeFe] hydrogenase from thermotogales indicates the molecular basis of resistance to oxygen inactivation Int J Hydrogen Energy 33 2008 570 578
9. R.C. Roberto, C. Dante, S. Armenta, M. Gutiérrez, and J. Celis Temporal phenomena of hydrogen photobioproduction Int J Hydrogen Energy 29 2008 1219 1226
10. J.W. Peters, W.N. Lanzilotta, B.J. Lemon, and L.C. Seefeldt X-ray crystal structure of the Fe-Only Hydrogenase (CpI) from Clostridium pasteurianium to 1.8 Angstron resolution Science 282 1998 1853 1858
11. Y. Nicolet, B.J. Lemon, J.C. Fontecilla-Camps, and J.W. Peters A novel FeS cluster in Fe-only hydrogenases Trends Biochem Sci 25 2000 138 143
12. Y. Nicolet, C. Piras, P. Legrand, E.C. Hatchikian, and J.C. Fontecilla-Camps Desulfovibrio desulfuricans iron hydrogenase: the structure shows unusual coordination to an active site Fe binuclear center Structure 7 1999 13 23
13. J.W. Peters Structure and mechanism of iron-only hydrogenases Curr Opin Struct Biol 9 1999 670 676
14. Y. Nicolet, A.L. De Lacey, X. Vernede, V.M. Fernandez, E.C. Hatchikian, and J.C. Fontecilla-Camps Crystallographic and FTIR spectroscopic evidence of changes in Fe coordination upon reduction of the active site of the Fe-only hydrogenase from Desulfovibrio desulfuricans J Am Chem Soc 123 2001 1596 1601
15. A. Volbeda, and J.C. Fontecilla-Camps The active site and catalytic mechanism of NiFe hydrogenases Dalton Trans 2003 4030 4038
16. F.A. Armstrong Hydrogenases: active site puzzles and progress Curr Opin Struct Biol 8 2004 133 140
17. Y. Nicolet, C. Cavazza, and J.C. Fontecilla-Camps Fe-only hydrogenases: structure, function and evolution J Inorg Biochem 91 2002 1 8
18. A.S. Pandey, T.V. Harris, L.J. Giles, J.W. Peters, and R.K. Szilagyi Dithiomethylether as a ligand in the hydrogenase H-Cluster J Am Chem Soc 130 2008 11106 11113
19. 14N HYSCORE investigation of the H-cluster of [FeFe] hydrogenase: evidence for a nitrogen in the dithiol bridgew Phys Chem Chem Phys 11 2009 6592 6599
20. P.E.M. Siegbahn, J.W. Tye, and M.B. Hall Computational studies of [NiFe] and [FeFe] hydrogenases Chem Rev 107 2007 4414 4435
21. M. Bruschi, P. Fantucci, and L.D. Gioia DFT investigation of structural, electronic, and catalytic properties of diiron complexes related to the [2Fe]H subcluster of Fe-Only hydrogenases Inorg Chem 41 2002 1421 1429
22. M. Bruschi, P. Fantucci, and L.D. Gioia Density functional theory investigation of the active site of [Fe]-hydrogenases: effects of redox state and ligand characteristics on structural, electronic, and reactivity properties of complexes related to the [2Fe]H subcluster Inorg Chem 42 2003 4773 4781
23. H cluster of [Fe] hydrogenases. A density functional theory investigation Inorg Chem 45 2006 4109 4118
24. D.J. Evans, and C.J. Pickett Chemistry and the hydrogenases Chem Soc Rev 32 2003 268 275
25. M.Y. Darensbourg, E.J. Lyon, X. Zhao, and I.P. Georgakaki The organometallic active site of [Fe]hydrogenase: models and entatic states Proc Natl Acad Sci U S A 100 2003 3683 3688
26. Z.-P. Liu, and P. Hu A density functional theory study on the active center of Fe-only hydrogenase: characterization and electronic structure of the redox states J Am Chem Soc 124 2002 5175 5182
27. Z.-P. Liu, and P. Hu Mechanism of H2 metabolism on Fe-only hydrogenases J Chem Phys 117 2002 8177 8180
28. H.-J. Fan, and M.B. Hall A capable bridging ligand for Fe-Only hydrogenase: density functional calculations of a low-energy route for heterolytic cleavage and formation of dihydrogen J Am Chem Soc 123 2001 3828 3829
29. C. Greco, M. Bruschi, L.D. Gioia, and U. Ryde A QM/MM investigation of the activation and catalytic mechanism of Fe-Only hydrogenases Inorg Chem 46 2007 5911 5921
30. Y. Montet, P. Amara, A. Volbeda, X. Vernede, C.E. Hatchikian, and M.J. Field Gas access to the active site of Ni-Fe hydrogenases probed by X-ray crystallography and molecular dynamics Nat Struct Biol 4 1997 523 526
31. C.V. Popescu, and E. Münck Electronic structure of the H cluster in [Fe]-hydrogenases J Am Chem Soc 121 1999 7877 7884
32. A.S. Pereira, P. Tavares, I. Moura, J.J.G. Moura, and B.H. Huynh Mossbauer characterization of the iron-sulfur clusters in Desulfovibrio vulgaris hydrogenase J Am Chem Soc 123 2001 2771 2782
33. E.J. Lyon, I.P. Georgakaki, J.H. Reibenspies, and M.Y. Darensbourg Carbon monoxide and cyanide ligands in a classical organometallic complex model for Fe-Only hydrogenase Angew Chem Int Ed English 38 1999 3178 3180
34. Z. Cao, and M.B. Hall Modeling the active sites in metalloenzymes. 3. Density Functional calculations on models for [Fe]-hydrogenase: structures and vibrational frequencies of the observed redox forms and the reaction mechanism at the Diiron active center J Am Chem Soc 123 2001 3734 3742
35. S. Trohalaki, and R. Pachter Mechanism of hydrogen production in [Fe-Fe]-hydrogenase: a density functional theory study Energy Fuels 21 2007 2278
36. H subcluster environment on the properties of key intermediates in the catalytic cycle of [FeFe] hydrogenases: hints for the rational design of synthetic catalysts Angew Chem Int Ed 48 2009 3503 3506
37. E.C. Hatchikian, N. Forget, V.M. Fernandez, R. Williams, and R. Cammack Further characterization of the [Fe]-hydrogenase from Desulfovibrio desulfuricans ATCC 7757 Eur J Biochem 209 1992 357 365
38. Schrodinger, LLC.
39. A.J. Pierik, M. Hulstein, W.R. Hagen, and S.P. Albracht A low-spin iron with CN and CO as intrinsic ligands forms the core of the active site in [Fe]-hydrogenases Eur J Biochem 258 1998 572 578
40. T.M. Van der Spek, A.F. Arendsen, R.P. Happe, S. Yun, K.A. Bagley, and D.J. Stufkens Similarities in the architecture of the active sites of Ni-hydrogenases and Fe-hydrogenases detected by means of infrared spectroscopy Eur J Biochem 237 1996 629 634
41. A.L. De Lacey, C. Stadler, C. Cavazza, E.C. Hatchikian, and V.M. Fernandez FTIR characterization of the active site of the Fe-hydrogenase from desulfovibrio desulfuricans J Am Chem Soc 122 2000 11232 11233
42. R.P. Happe, W. Roseboom, A.J. Pierik, and S.P.J. Albracht Biological activation of hydrogen Nature 385 1997 126 136
43. Friesner RA. Advances in protein chemistry, vol. 72, Peptide solvation and H-bonds; 2006. pp. 80-99.
44. D.M. Phillip, and R.A. Friesner Mixed ab initio QMrMM modeling using frozen orbitals and tests with alanine dipeptide and tetrapeptide J Comput Chem 20 1999 1468 1494
45. R.B. Murphy, D.M. Philipp, and R.A. Friesner A mixed quantum mechanics/molecular mechanics (QM/MM) method for large-scale modeling of chemistry in protein environments J Comput Chem 21 2000 1442 1457
46. M. Baik, B.F. Gherman, R.A. Friesner, and S.J. Lippard Hydroxylation of methane by non-heme diiron enzymes: molecular orbital analysis of the C-H bond activation by reactive intermediate Q J Am Chem Soc 124 2002 14608 14615
47. Wirstam M, Lippard SJ, Friesner RA. Reversible dioxygen binding to hemerythrin. 125; 2003, 3980-3987.
48. R.A. Friesner, M. Baik, V. Guallar, B.F. Gherman, M. Wirstam, and R.B. Murphy How iron-containing proteins control dioxygen chemistry: a detailed atomic level description via accurate quantum chemical and mixed quantum mechanics/molecular mechanics calculations Coordin Chem Rev 238-239 2003 267 290
49. V. Guallar, M. Baik, S.J. Lippard, and R.A. Friesner Peripheral heme substituents control the hydrogen-atom abstraction chemistry in cytochromes P450 Proc Natl Acad Sci U S A 100 2003 6998 7002
50. M. Baik, M. Newcomb, R.A. Friesner, and S.J. Lippard Mechanistic studies on the hydroxylation of methane by methane monooxygenase Chem Rev 103 2003 2385 2419
51. M. Baik, R.A. Friesner, and S.J. Lippard Theoretical study of cisplatin binding to purine bases: why does cisplatin prefer guanine over adenine as substrate? J Am Chem Soc 125 2003 14082 14092
52. V. Guallar, M. Jacobson, A. McDermott, and R.A. Friesner Computational modeling of the catalytic reaction in triosephosphate isomerase J Mol Biol 337 2004 227 239
53. B.F. Gherman, S.D. Goldberg, V.W. Cornish, and R.A. Friesner Mixed quantum mechanical/molecular mechanical (QM/MM) study of the deacylation reaction in a penicillin binding protein (PBP) versus in a class C β-Lactamase J Am Chem Soc 126 2004 7652 7664
54. V. Guallar, and R.A. Friesner Cytochrome P450CAM enzymatic catalysis cycle: a quantum mechanics/molecular mechanics study J Am Chem Soc 126 2004 8501 8508
55. B.F. Gherman, M. Baik, S.J. Lippard, and R.A. Friesner Dioxygen activation in methane monooxygenase: a theoretical study J Am Chem Soc 126 2004 2978 2990
56. B.F. Gherman, S.J. Lippard, and A. Friesner Richard Substrate hydroxylation in methane monooxygenase: quantitative modeling via mixed quantum mechanics/molecular mechanics techniques J Am Chem Soc 127 2005 1025 1037
57. Guallar V, Jarzecki AA, Friesner RA, Spiro TG. Modeling of ligation-induced helix/loop displacements in myoglobin: toward an understanding of hemoglobin allostery. 128; 2006, 5427-5435.
58. D. Rinaldo, D.M. Philipp, S.J. Lippard, and R.A. Friesner Intermediates in dioxygen activation by methane monooxygenase: a QM/MM study J Am Chem Soc 129 2007 3135 3147
59. T.O. Fischmann, A. Hruza, J.S. Duca, L. Ramanathan, T. Mayhood, and W.T. Windsor Structure-guided discovery of cyclin-dependent kinase inhibitors Biopolymers 89 2008 372 379
60. S.D. Bembenek, J.M. Keith, M.A. Letavic, R. Apodaca, A.J. Barbier, and L. Dvorak Lead identification of acetylcholinesterase inhibitors-histamine H3 receptor antagonists from molecular modeling Bioorg Med Chem 16 2008 2968 2973
61. T. Zhou, Y. Mo, Z. Zhou, and K.R. Tsai Density functional study on dihydrogen activation at the H cluster in Fe-Only hydrogenases Inorg Chem 44 2005 4941 4946
62. C.H. Chang, and K. Kim Density functional theory calculation of bonding and charge parameters for molecular dynamics studies on [FeFe] hydrogenases J Chem Theory Comput 5 2009 1137 1145
63. H subcluster Inorg Chem 43 2004 3733 3741
64. I.P. Georgakaki, L.M. Thomson, E.J. Lyon, M.B. Hall, and M.Y. Darensbourg Fundamental properties of small molecule models of Fe-Only hydrogenase: computations relative to the definition of an entatic state in the active site Coordin Chem Rev 238-239 2003 255 266
65. H. Kessler Detection of hindered rotation and inversion by NMR Spectroscopy Angew Chem Int Ed 9 1970 219 235