Diiron Azadithiolates as Models for the [FeFe]-Hydrogenase Active Site and Paradigm for the Role of the Second Coordination Sphere

Accounts of Chemical Research

Volumn 48, Issue 7, 2015, Pages 2107-2116

  Rauchfuss, Thomas B ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HETEROCYCLIC COMPOUND; HYDROGENASE; IRON DERIVATIVE; IRON HYDROGENASE; IRON SULFUR PROTEIN; THIOL DERIVATIVE;

CHEMICAL STRUCTURE; CHEMISTRY; CONFORMATION; ENZYME ACTIVE SITE; METABOLISM; STEREOISOMERISM;

AZA COMPOUNDS; CATALYTIC DOMAIN; HYDROGENASE; IRON COMPOUNDS; IRON-SULFUR PROTEINS; MODELS, MOLECULAR; MOLECULAR CONFORMATION; STEREOISOMERISM; SULFHYDRYL COMPOUNDS;

EID: 84937419398     PISSN: 00014842     EISSN: 15204898     Source Type: Journal    
DOI: 10.1021/acs.accounts.5b00177     Document Type: Article

References (67)

1. Fontecilla-Camps, J. C.; Volbeda, A.; Cavazza, C.; Nicolet, Y. Structure/Function Relationships of [NiFe]- and [FeFe]-Hydrogenases Chem. Rev. 2007, 107, 4273-4303
2. Lubitz, W.; Ogata, H.; Rüdiger, O.; Reijerse, E. Hydrogenases Chem. Rev. 2014, 114, 4081-4148
3. Peters, J. W.; Schut, G. J.; Boyd, E. S.; Mulder, D. W.; Shepard, E. M.; Broderick, J. B.; King, P. W.; Adams, M. W. W. [FeFe]- and [NiFe]-hydrogenase Diversity, Mechanism, and Maturation Biochim. Biophys. Acta, Mol. Cell Res. 2014, 1853, 1350-1369
4. Bioinspired Catalysis; Schollhammer, P.; Weigand, W., Eds.; Wiley-VCH: Weinheim, 2014.
5. Mulder, D. W.; Ratzloff, M. W.; Bruschi, M.; Greco, C.; Koonce, E.; Peters, J. W.; King, P. W. Investigations on the Role of Proton-Coupled Electron Transfer in Hydrogen Activation by [FeFe]-Hydrogenase J. Am. Chem. Soc. 2014, 136, 15394-15402
6. Mulder, D. W.; Ratzloff, M. W.; Shepard, E. M.; Byer, A. S.; Noone, S. M.; Peters, J. W.; Broderick, J. B.; King, P. W. EPR and FTIR Analysis of the Mechanism of H2 Activation by [FeFe]-Hydrogenase HydA1 from Chlamydomonas reinhardtii J. Am. Chem. Soc. 2013, 135, 6921-6929
7. Tard, C.; Pickett, C. J. Structural and Functional Analogues of the Active Sites of the [Fe]-, [NiFe]-, and [FeFe]-Hydrogenases Chem. Rev. 2009, 109, 2245-2274
8. Schmidt, M.; Contakes, S. M.; Rauchfuss, T. B. First Generation Analogues of the Binuclear Site in the Fe-Only Hydrogenases: Fe2(μ-SR)2(CO)4(CN)22- J. Am. Chem. Soc. 1999, 121, 9736-9737
9. Le Cloirec, A.; Davies, S. C.; Evans, D. J.; Hughes, D. L.; Pickett, C. J.; Best, S. P.; Borg, S. A Di-Iron Dithiolate Possessing Structural Elements of the Carbonyl/Cyanide Sub-Site of the H-Centre of Fe-Only Hydrogenase Chem. Commun. 1999, 2285-2286
10. Lyon, E. J.; Georgakaki, I. P.; Reibenspies, J. H.; Darensbourg, M. Y. Carbon Monoxide and Cyanide Ligands in a Classical Organometallic Complex Model for Fe-Only Hydrogenase Angew. Chem., Int. Ed. 1999, 38, 3178-3180
11. Matthews, S. L.; Heinekey, D. M. A Carbonyl-Rich Bridging Hydride Complex Relevant to the Fe-Fe Hydrogenase Active Site Inorg. Chem. 2010, 49, 9746-9748
12. Mack, A. E.; Rauchfuss, T. B. (1,3-Propanedithiolato)hexacarbonyldiiron and Cyanide Derivatives Inorg. Synth. 2011, 35, 142-147
13. Boyke, C. A. Ph.D. Thesis, University Illinois, Urbana-Champaign, 2006.
14. Manor, B. C.; Ringenberg, M. R.; Rauchfuss, T. B. Borane-Protected Cyanides as Surrogates of H-Bonded Cyanides in [FeFe]-Hydrogenase Active Site Models Inorg. Chem. 2014, 53, 7241-7247
15. Fontecilla-Camps, J. C.; Amara, P.; Cavazza, C.; Nicolet, Y.; Volbeda, A. Structure-function relationships of anaerobic gas-processing metalloenzymes Nature 2009, 460, 814-822
16. Bruschi, M.; Greco, C.; Kaukonen, M.; Fantucci, P.; Ryde, U.; De Gioia, L. Influence of the [2Fe]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. 2009, 48, 3503-3506
17. Tschierlei, S.; Ott, S.; Lomoth, R. Spectroscopically Characterized Intermediates of Catalytic H2 Formation by [FeFe] Hydrogenase Models Energy Environ. Sci. 2011, 4, 2340-2352
18. Felton, G. A. N.; Mebi, C. A.; Petro, B. J.; Vannucci, A. K.; Evans, D. H.; Glass, R. S.; Lichtenberger, D. L. Review of Electrochemical Studies of Complexes Containing the Fe2S2 Core Characteristic of [FeFe]-Hydrogenases Including Catalysis by These Complexes of the Reduction of Acids to Form Dihydrogen J. Organomet. Chem. 2009, 694, 2681-2699
19. Gloaguen, F.; Rauchfuss, T. B. Small Molecule Mimics of Hydrogenase: Hydrides and Redox Chem. Soc. Rev. 2009, 38, 100-108
20. Chernev, P.; Lambertz, C.; Bruenje, A.; Leidel, N.; Sigfridsson, K. G. V.; Kositzki, R.; Hsieh, C.-H.; Yao, S.; Schiwon, R.; Driess, M.; Limberg, C.; Happe, T.; Haumann, M. Hydride Binding to the Active Site of [FeFe]-Hydrogenase Inorg. Chem. 2014, 53, 12164-12177
21. Barton, B. E.; Rauchfuss, T. B. Terminal Hydride in [FeFe]-Hydrogenase Model Has Lower Potential for H2 Production Than the Isomeric Bridging Hydride Inorg. Chem. 2008, 47, 2261-2263
22. van der Vlugt, J. I.; Rauchfuss, T. B.; Whaley, C. M.; Wilson, S. R. Characterization of a Diferrous Terminal Hydride Mechanistically Relevant to the Fe-Only Hydrogenases J. Am. Chem. Soc. 2005, 127, 16012-16013
23. Zaffaroni, R.; Rauchfuss, T. B.; Gray, D. L.; De Gioia, L.; Zampella, G. Terminal vs Bridging Hydrides of Diiron Dithiolates: Protonation of Fe2(dithiolate)(CO)2(PMe3)4 J. Am. Chem. Soc. 2012, 134, 19260-19269
24. Liu, C.; Peck, J. N. T.; Wright, J. A.; Pickett, C. J.; Hall, M. B. Density Functional Calculations on Protonation of the [FeFe]-Hydrogenase Model Complex Fe2(μ-pdt)(CO)4(PMe3)2 and Subsequent Isomerization Pathways Eur. J. Inorg. Chem. 2011, 1080-1093
25. Knoerzer, 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
26. Finkelmann, A. R.; Stiebritz, M. T.; Reiher, M. Inaccessibility of the μ-Hydride Species in [FeFe] Hydrogenases Chem. Sci. 2014, 5, 215-221
27. Zaffaroni, R.; Rauchfuss, T. B.; Fuller, A.; De Gioia, L.; Zampella, G. Contrasting Protonation Behavior of Diphosphido vs Dithiolato Diiron(I) Carbonyl Complexes Organometallics 2013, 32, 232-238
28. Kramarz, K. W.; Norton, J. R. Slow Proton Transfer Reactions in Organometallic and Bioinorganic Chemistry Prog. Inorg. Chem. 1994, 42, 1-65
29. Ogata, H.; Nishikawa, K.; Lubitz, W. Hydrogens detected by subatomic resolution protein crystallography in a NiFe hydrogenase Nature 2015, 520, 571-574
30. Hoffman, B. M.; Lukoyanov, D.; Dean, D. R.; Seefeldt, L. C. Nitrogenase: A Draft Mechanism Acc. Chem. Res. 2013, 46, 587-595
31. Barton, B. E.; Zampella, G.; Justice, A. K.; De Gioia, L.; Rauchfuss, T. B.; Wilson, S. R. Isomerization of the Hydride Complexes [HFe2(SR)2(PR3)x(CO)6- x]+ (x = 2, 3, 4) Relevant to the Active Site Models for the [FeFe]-Hydrogenases Dalton Trans. 2010, 39, 3011-3019
32. Singleton, M. L.; Bhuvanesh, N.; Reibenspies, J. H.; Darensbourg, M. Y. Synthetic Support of De Novo Design: Sterically Bulky [FeFe]-Hydrogenase Models Angew. Chem., Int. Ed. 2008, 47, 9492-9495
33. Zampella, G.; Fantucci, P.; De Gioia, L. DFT Characterization of the Reaction Pathways for Terminal- to μ-Hydride Isomerisation in Synthetic Models of the [FeFe]-Hydrogenase Active Site Chem. Commun. 2010, 8824-8826
34. Gloaguen, F.; Lawrence, J. D.; Schmidt, M.; Wilson, S. R.; Rauchfuss, T. B. Synthetic and Structural Studies on [Fe2(SR)2(CN)x(CO)6- x]x - as Active Site Models for Fe-Only Hydrogenases J. Am. Chem. Soc. 2001, 123, 12518-12527
35. Wang, W.; Nilges, M. J.; Rauchfuss, T. B.; Stein, M. Isolation of a Mixed Valence Diiron Hydride: Evidence for a Spectator Hydride in Hydrogen Evolution Catalysis J. Am. Chem. Soc. 2013, 135, 3633-3639
36. Angamuthu, R.; Chen, C.-S.; Cochrane, T. R.; Gray, D. L.; Schilter, D.; Ulloa, O. A.; Rauchfuss, T. B. N-Substituted Derivatives of the Azadithiolate Cofactor from the [FeFe]-Hydrogenases: Stability and Complexation Inorg. Chem. 2015, 54, 000
37. Giolando, D. M.; Rauchfuss, T. B. Alkylidenebis(perthiolates): A New Class of Organosulfur Ligands Prepared from (RC5H4)2TiS5 Organometallics 2002, 3, 487-489
38. Stanley, J. L.; Rauchfuss, T. B.; Wilson, S. R. Studies on the Condensation Pathway to and Properties of Diiron Azadithiolate Carbonyls Organometallics 2007, 26, 1907-1911
39. Lawrence, J. D.; Li, H.; Rauchfuss, T. B.; Bénard, M.; Rohmer, M.-M. Diiron Azadithiolates as Models for the Iron-only Hydrogenase Active Site: Synthesis, Structure, and Stereoelectronics Angew. Chem., Int. Ed. 2001, 40, 1768-1771
40. Lawrence, J. D.; Li, H.; Rauchfuss, T. B. Beyond Fe-Only Hydrogenases: N -Functionalized 2-Aza-1,3-dithiolates Fe2[(SCH2)2NR](CO)x (x = 5, 6) Chem. Commun. 2001, 1482-1483
41. Li, H.; Rauchfuss, T. B. Iron Carbonyl Sulfides, Formaldehyde, and Amines Condense To Give the Proposed Azadithiolate Cofactor of the Fe-Only Hydrogenases J. Am. Chem. Soc. 2002, 124, 726-727
42. Berggren, G.; Adamska, A.; Lambertz, C.; Simmons, T. R.; Esselborn, J.; Atta, M.; Gambarelli, S.; Mouesca, J. M.; Reijerse, E.; Lubitz, W.; Happe, T.; Artero, V.; Fontecave, M. Biomimetic Assembly and Activation of [FeFe]-Hydrogenases Nature 2013, 499, 66-69
43. Esselborn, J.; Lambertz, C.; Adamska-Venkatesh, A.; Simmons, T.; Berggren, G.; Noth, J.; Siebel, J.; Hemschemeier, A.; Artero, V.; Reijerse, E.; Fontecave, M.; Lubitz, W.; Happe, T. Spontaneous Activation of [FeFe]-Hydrogenases by an Inorganic [2Fe] Active Site Mimic Nat. Chem. Biol. 2013, 9, 607-609
44. Adamska-Venkatesh, A.; Simmons, T. R.; Siebel, J. F.; Artero, V.; Fontecave, M.; Reijerse, E.; Lubitz, W. Artificially Maturated [FeFe] Hydrogenase from Chlamydomonas reinhardtii: a HYSCORE and ENDOR Study of a Non-Natural H-Cluster Phys. Chem. Chem. Phys. 2015, 17, 5421-5430
45. Carroll, M. E.; Barton, B. E.; Rauchfuss, T. B.; Carroll, P. J. Synthetic Models for the Active Site of the [FeFe]-Hydrogenase: Catalytic Proton Reduction and the Structure of the Doubly Protonated Intermediate J. Am. Chem. Soc. 2012, 134, 18843-18852
46. Stanley, J. L.; Heiden, Z. M.; Rauchfuss, T. B.; Wilson, S. R.; De Gioia, L.; Zampella, G. Desymmetrized Diiron Azadithiolato Carbonyls: A Step Toward Modeling the Iron-Only Hydrogenases Organometallics 2007, 27, 119-125
47. Eilers, G.; Schwartz, L.; Stein, M.; Zampella, G.; de Gioia, L.; Ott, S.; Lomoth, R. Ligand versus Metal Protonation of an Iron Hydrogenase Active Site Mimic Chem.-Eur. J. 2007, 13, 7075-7084
48. Barton, B. E.; Olsen, M. T.; Rauchfuss, T. B. Aza- and Oxadithiolates Are Probable Proton Relays in Functional Models for the [FeFe]-Hydrogenases J. Am. Chem. Soc. 2008, 130, 16834-16835
49. Custelcean, R.; Jackson, J. E. Dihydrogen Bonding: Structures, Energetics, and Dynamics Chem. Rev. 2001, 101, 1963-1980
50. Liu, T.; DuBois, D. L.; Bullock, R. M. An Iron Complex with Pendent Amines as a Molecular Electrocatalyst for Oxidation of Hydrogen Nat. Chem. 2013, 5, 228-233
51. Olsen, M. T.; Rauchfuss, T. B.; Wilson, S. R. Role of the Azadithiolate Cofactor in Models for [FeFe]-Hydrogenase: Novel Structures and Catalytic Implications J. Am. Chem. Soc. 2010, 132, 17733-17740
52. Justice, A. K.; Zampella, G.; De Gioia, L.; Rauchfuss, T. B.; van der Vlugt, J. I.; Wilson, S. R. Chelate Control of Diiron(I) Dithiolates Relevant to the [Fe-Fe]-Hydrogenase Active Site Inorg. Chem. 2007, 46, 1655-1664
53. Rakowski DuBois, M.; DuBois, D. L. The Roles of the First And Second Coordination Spheres in the Design of Molecular Catalysts for H2 Production and Oxidation Chem. Soc. Rev. 2009, 38, 62-72
54. Huynh, M. T.; Wang, W.; Rauchfuss, T. B.; Hammes-Schiffer, S. Computational Investigation of [FeFe]-Hydrogenase Models: Characterization of Singly and Doubly Protonated Intermediates and Mechanistic Insights Inorg. Chem. 2014, 53, 10301-10311
55. Fourmond, V.; Jacques, P.-A.; Fontecave, M.; Artero, V. H2 Evolution and Molecular Electrocatalysts: Determination of Overpotentials and Effect of Homoconjugation Inorg. Chem. 2010, 49, 10338-10347
56. Thomas, C. M.; Liu, T.; Hall, M. B.; Darensbourg, M. Y. Series of Mixed Valent Fe(II)Fe(I) Complexes That Model the Hox State of [FeFe]Hydrogenase: Redox Properties, Density-Functional Theory Investigation, and Reactivities with Extrinsic CO Inorg. Chem. 2008, 47, 7009-7024
57. Justice, A. K.; De Gioia, L.; Nilges, M. J.; Rauchfuss, T. B.; Wilson, S. R.; Zampella, G. Redox and Structural Properties of Mixed-Valence Models for the Active Site of the [FeFe]-Hydrogenase: Progress and Challenges Inorg. Chem. 2008, 47, 7405-7414
58. Olsen, M. T.; Barton, B. E.; Rauchfuss, T. B. Hydrogen Activation by Biomimetic Diiron Dithiolates Inorg. Chem. 2009, 48, 7507-7509
59. Tilset, M.; Fjeldahl, I.; Hamon, J.-R.; Hamon, P.; Toupet, L.; Saillard, J.-Y.; Costuas, K.; Haynes, A. Theoretical, Thermodynamic, Spectroscopic, and Structural Studies of the Consequences of One-Electron Oxidation on the Fe-X Bonds in 17- and 18-Electron Cp∗Fe(dppe)X Complexes (X = F, Cl, Br, I, H, CH3) J. Am. Chem. Soc. 2001, 123, 9984-10000
60. Camara, J. M.; Rauchfuss, T. B. Mild Redox Complementation Enables H2 Activation by [FeFe]-Hydrogenase Models J. Am. Chem. Soc. 2011, 133, 8098-8101
61. Tard, C.; Liu, X.; Ibrahim, S. K.; Bruschi, M.; De Gioia, L.; Davies, S. C.; Yang, X.; Wang, L.-S.; Sawers, G.; Pickett, C. J. Synthesis of the H-Cluster Framework of Iron-only Hydrogenase Nature 2005, 433, 610-614
62. Camara, J. M.; Rauchfuss, T. B. Combining Acid-Base, Redox and Substrate Binding Functionalities to Give a Complete Model for the [FeFe]-Hydrogenase Nat. Chem. 2012, 4, 26-30
63. Munery, S.; Capon, J.-F.; De Gioia, L.; Elleouet, C.; Greco, C.; Pétillon, F. Y.; Schollhammer, P.; Talarmin, J.; Zampella, G. New FeI-FeI Complex Featuring a Rotated Conformation Related to [2 Fe]H Subsite of the [Fe-Fe] Hydrogenase Chem.-Eur. J. 2013, 19, 15458-15461
64. Wang, W.; Rauchfuss, T. B.; Moore, C. E.; Rheingold, A. L.; De Gioia, L.; Zampella, G. Crystallographic Characterization of a Fully Rotated, Basic Diiron Dithiolate: Model for the Hred State? Chem.-Eur. J. 2013, 19, 15476-15479
65. Darmon, J. M.; Kumar, N.; Hulley, E. B.; Weiss, C. J.; Raugei, S.; Bullock, R. M.; Helm, M. L. Increasing the Rate of Hydrogen Oxidation Without Increasing the Overpotential: A Bioinspired Iron Molecular Electrocatalyst with an Outer Coordination Sphere Proton Relay Chem. Sci. 2015, 6, 2737-2745
66. Crabtree, R. H. Multifunctional Ligands in Transition Metal Catalysis New J. Chem. 2011, 35, 18-23
67. Lansing, J. C.; Camara, J. M.; Gray, D. E.; Rauchfuss, T. B. Hydrogen Production Catalyzed by Bidirectional, Biomimetic Models of the [FeFe]-Hydrogenase Active Site Organometallics 2014, 33, 5897-5906