[NiFe]-hydrogenases: Spectroscopic and electrochemical definition of reactions and intermediates

Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences

Volumn 363, Issue 1829, 2005, Pages 937-954

  Armstrong, Fraser A ^a   Albracht, Simon P J ^b  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

Electrochemistry; Energy; Fuel cell; Hydrogen catalysts; Hydrogenases; Spectroscopy

Indexed keywords

EID: 20744457727     PISSN: 1364503X     EISSN: None     Source Type: Journal    
DOI: 10.1098/rsta.2004.1528     Document Type: Review

References (53)

1. Albracht, S. P. J. 1994 Nickel hydrogenases: in search of the active site. Biochim. Biophys. Acta 1188, 167-204.
2. Bagley, K. A., Van Garderen, C. J., Chen, M., Duin, E. C., Albracht, S. P. J. & Woodruff, W. H. 1994 Infrared studies on the interaction of carbon monoxide with divalent nickel in hydrogenase from Chromatium vinosum. Biochemistry 33, 9229-9236.
3. Bagley, K. A., Duin, E. C., Roseboom, W., Albracht, S. P. J. & Woodruff, W. H. 1995 Infrared-detectable groups sense changes in charge density on the nickel center in hydrogenase from Chromatium vinosum. Biochemistry 34, 5527-5535.
4. Bleijlevens, B., Faber, B. W. & Albracht, S. P. J. 2001 The [NiFe] hydrogenase from Allochromatium vinosum studied in EPR-detectable states: H/D exchange experiments that yield new information about the structure of the active site. J. Biol. Inorg. Chem. 6, 763-769.
5. Bleijlevens, B., Buhrke, T., Van der Linden, E., Friedrich, B. & Albracht, S. P. J. 2004a The auxilliary protein HypX confers oxygen tolerance to the soluble [NiFe]-hydrogenase of Ralstonia eutropha by way of a cyanide ligand to nickel. J. Biol. Chem. 279, 46 686-46 691.
6. Bleijlevens, B., Van Broekhuizen, F. A., De Lacey, A. L., Roseboom, W., Fernandez, V. M. & Albracht, S. P. J. 2004b The activation of the [NiFe]-hydrogenase from Allochromatium vinosum. An infrared spectro-electrochemical study. J. Biol. Inorg. Chem. 9, 743-752.
7. 2-sensing hydrogenase from Ralstonia eutropha in its reduced state by HYSCORE and ENDOR spectroscopy. J. Am. Chem. Soc. 125, 13 075-13 083.
8. Cammack, R., Frey, M. & Robson, R. 2001 Hydrogen as a fuel. Learning from nature. New York: Taylor & Francis Inc.
9. Coremans, J. M. C. C., van der Zwaan, J. W. & Albracht, S. P. J. 1992 Distinct redox behaviour of prosthetic groups in ready and unready hydrogenase from Chromatium vinosum. Biochim. Biophys. Acta 1119, 157-168.
10. Davidson, G., Choudhury, S. B., Gu, Z., Bose, K., Roseboom, W., Albracht, S. P. J. & Maroney, M. J. 2000 Structural examination of the nickel site in Chromatium vinosum hydrogenase: redox state oscillations and structural changes accompanying reductive activation and CO binding. Biochemistry 39, 7468-7479.
11. 9 nickel(I) catenate: stabilisation of monovalent nickel by interlocked macrocycles. J. Chem. Soc. Chem. Commun. 760-762.
12. Evans, D. J. & Pickett, C. J. 2003 Chemistry and the hydrogenases. Chem. Soc. Rev. 32, 268-275.
13. Fernandez, V. M., Hatchikian, E. C. & Cammack, R. 1985 Properties and reactivation of two different deactivated forms of Desulfovibrio gigas hydrogenase. Biochim. Biophys. Acta 832, 69-79.
14. Foerster, S., Stein, M., Brecht, M., Ogata, H., Higuchi, Y. & Lubitz, W. 2003 Single crystal EPR studies of the reduced active site of [NiFe] hydrogenase from Desulfovibrio vulgaris Miyazaki F. J. Am. Chem. Soc. 125, 83-93.
15. Garcin, E., Vernede, X., Hatchikian, E. C., Volbeda, A., Frey, M. & Fontecilla-Camps, J. C. 1999 The crystal structure of a reduced [NiFeSe] hydrogenase provides an image of the activated catalytic center. Struct. Fold. Des. 7, 557-566.
16. Georgakaki, I. P., Thomson, L. M., Lyon, E. J., Hall, M. B. & Darensbourg, M. Y. 2003 Fundamental properties of small molecule models of Fe-only hydrogenase: computations relative to the definition of an entatic state in the active site. Coord. Chem. Rev. 238, 255-266.
17. 2 with active [NiFe]-hydrogenase from Allochromatium vinosum. A stopped-flow infrared study. Biochemistry 43, 6808-6819.
18. Happe, R. P., Roseboom, W., Pierik, A. J., Albracht, S. P. J. & Bagley, K. A. 1997 Biological activation of hydrogen. Nature 385, 126.
19. 2 and CO. Eur. J. Biochem. 259, 602-608.
20. 2-activating site of the cytoplasmic NAD-reducing hydrogenase from Ralstonia eutropha. FEBS Lett. 466, 259-263.
21. 2, as revealed by X-ray structure analysis at 1.4 Å resolution. Struct. Fold. Des. 7, 549-556.
22. Huyett, J. E., Carepo, M., Pamplona, A., Franco, R., Moura, I., Moura, J. J. G. & Hoffman, B. M. 1997 Fe-57 Q-band pulsed ENDOR of the hetero-dinuclear site of nickel hydrogenase: comparison of the NiA, NiB, and NiC states. J. Am. Chem. Soc. 119, 9291-9292.
23. Jones, A. K., Sillery, E., Albracht, S. P. J. & Armstrong, F. A. 2002 Direct comparison of the electrocatalytic oxidation of hydrogen by an enzyme and a platinum catalyst. Chem. Commun. 866-867.
24. Jones, A. K., Lamle, S. E., Pershad, H. R., Vincent, K. A., Albracht, S. P. J. & Armstrong, F. A. 2003 Enzyme electrokinetics: electrochemical studies of the anaerobic interconversions between active and inactive states of Allochromatium vinosum [NiFe]-hydrogenase. J. Am. Chem. Soc. 125, 8505-8514.
25. Kurkin, S., George, S. J., Thorneley, R. N. & Albracht, S. P. J. 2004 Hydrogen-induced activation of the [NiFe]-hydrogenase from Allochromatium vinosum as studied by stopped-flow infrared spectroscopy. Biochemistry 43, 6820-6831.
26. Lamle, S. E., Vincent, K. A., Halliwell, L. M., Albracht, S. P. J. & Armstrong, F. A. 2003 Hydrogenase on an electrode: a remarkable heterogeneous catalyst. Dalton Trans. 4152-4157.
27. Lamle, S. E., Albracht, S. P. J. & Armstrong, F. A. 2004 Electrochemical potential-step investigations of the aerobic interconversions of [NiFe]-hydrogenase from Allochromatium vinosum: new insights into the puzzling difference between unready and ready oxidized inactive states. J. Am. Chem. Soc. 126, 14 899-14 909.
28. Lamle, S. E., Albracht, S. P. J., Armstrong, F. A. Submitted. The mechanism of activation of a [NiFe]-hydrogenase by electrons, hydrogen and carbon monoxide.
29. Léger, C., Jones, A. K., Albracht, S. P. J. & Armstrong, F. A. 2002a Effect of a dispersion of interfacial electron transfer rates on steady state catalytic electron transport in [NiFe]-hydrogenase and other enzymes. J. Phys. Chem. B 106, 13 058-13 063.
30. Léger, C., Jones, A. K., Roseboom, W., Albracht, S. P. J. & Armstrong, F. A. 20026 Enzyme electrokinetics: hydrogen evolution and oxidation by Allochromatium vinosum [NiFe]-hydrogenase. Biochemistry 41, 15 736-15 746.
31. Lyon, E. J., Shima, S., Bocher, R., Thauer, R. K., Grevels, F.-W., Bill, E., Roseboom, W. & Albracht, S. P. J. 2004a Carbon monoxide as an intrinsic ligand to iron in the active site of the iron-sulfur cluster free hydrogenase (Hmd) as revealed by infrared spectroscopy. J. Am. Chem. Soc. 126, 14 239-14 248.
32. Lyon, E. J., Shima, S., Buurman, G., Chowdhuri, S., Batschauer, A., Steinbach, K. & Thauer, R. K. 2004b UV-A/blue-light inactivation of the 'metal-free' hydrogenase (Hmd) from methanogenic archaea. Eur. J. Biochem. 271, 195-204.
33. Nicolet, Y., Piras, C., Legrand, P., Hatchikian, C. E. & Fontecilla-Camps, J. C. 1999 Desulfovibrio desulfuricans iron hydrogenase: the structure shows unusual coordination to an active site Fe binuclear center. Struct. Fold. Des. 7, 13-23.
34. Nicolet, Y., De Lacey, A. L., Vernede, X., Fernandez, V. M., Hatchikian, E. C. & Fontecilla-Camps, J. C. 2001 Crystallographic and FTIR spectroscopic evidence of changes in Fe coordination upon reduction of the active site of the Fe-only hydrogenase from Desulfovibrio deaulfuricans. J. Am. Chem. Soc. 123, 1596-1601.
35. 2 value. Biochemistry 38, 8992-8999.
36. Peters, J. W., Lanzilotta, W. N., Lemon, B. J. & Seefeldt, L. C. 1998 X-ray crystal structure of the Fe-only hydrogenase (CpI) from Clostridium pasteurianum to 1.8 angstrom resolution. Science 282, 1853-1858.
37. Pierik, A. J., Hulstein, M., Hagen, W. R. & Albracht, S. P. J. 1998 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, 572-578.
38. 2. J. Biol. Chem. 274, 3331-3337.
39. Ratnasamy, P. 2005 Novel benign catalysts for oxidizing hydrocarbons. Phil. Trans. R. Soc. A. (doi:10.1098/rsta.2004.1538).
40. Rousset, M., Montet, Y., Guigliarelli, B., Forget, N., Asso, M., Bertrand, P., Fontecilla-Camps, J. C. & Hatchikian, E. C. 1998 [3Fe-4S] to [4Fe-4S] cluster conversion in Desulfovibrio fructosovorans [NiFe] hydrogenase by site-directed mutagenesis. Proc. Natl Acad. Sci. USA 95, 11625-11630.
41. Shima, S. et al. 2004 The cofactor of the iron-sulfur cluster free hydrogenase Hmd: structure of the light-inactivation product. Angew. Chem. Int. Ed. Engl. 43, 2547-2551.
42. Surerus, K. K., Chen, M., van der Zwaan, J. W., Rusnak, F. M., Kolk, M., Duin, E. C., Albracht, S. P. J. & Münck, E. 1994 Further characterization of the spin coupling observed in oxidized hydrogenase from Chromatium vinosum. A Mössbauer and multifrequency EPR study. Biochemistry 33, 4980-4993.
43. Teixeira, M., Moura, I., Xavier, A. V., Moura, J. J. G., LeGall, J., DerVartanian, D. V., Peck, H. D., Jr & Huynh, B. H. 1989 Redox intermediates of Desulfovibrio gigas [NiFe] hydrogenase generated under hydrogen. Mössbauer and EPR characterization of the metal centers. J. Biol. Chem. 264, 16 435-16 450.
44. Thauer, R. K. 1998 Biochemistry of methanogenesis: a tribute to Marory Stephenson. Microbiology 144, 2377-2406.
45. Van der Linden, E., Burgdorf, T., Bernhard, M., Bleijlevens, B., Friedrich, B. & Albracht, S. P. J. 2004a The soluble [NiFe]-hydrogenase from Ralstonia eutropha contains four cyanides in its active site, one of which is responsible for the insensitivity towards oxygen. J. Biol. Inorg. Chem. 9, 616-626.
46. +-reducing [NiFe]-hydrogenase from Ralstonia eutropha. Eur. J. Biochem. 271, 801-808.
47. Van der Spek, T. M., Arendsen, A. F., Happe, R. P., Yun, S., Bagley, K. A., Stufkens, D. J., Hagen, W. R. & Albracht, S. P. J. 1996 Similarities in the architecture of the active sites of Ni-hydrogenases and Fe-hydrogenases detected by means of infrared spectroscopy. Eur. J. Biochem. 237, 629-634.
48. Van der Zwaan, J. W., Albracht, S. P. J., Fontijn, R. D. & Slater, E. C. 1985 Monovalent nickel in hydrogenase from Chromatium vinosum. Light sensitivity and evidence for direct interaction with hydrogen. FEBS Lett. 179, 271-277.
49. 13CO on EPR spectra of nickel in hydrogenase from Chromatium vinosum. Biochim. Biophys. Acta 1041, 101-110.
50. Vignais, P. M., Billoud, B. & Meyer, J. 2001 Classification and phylogeny of hydrogenases. FEMS Microbiol. Rev. 25, 455-501.
51. Volbeda, A., Charon, M. H., Piras, C., Hatchikian, E. C., Frey, M. & Fontecilla-Camps, J. C. 1995 Crystal structure of the nickel-iron hydrogenase from Desulfovibrio gigas. Nature 373, 580-587.
52. Volbeda, A., Garcia, E., Piras, C., De Lacey, A. L., Fernandez, V. M., Hatchikian, E. C., Frey, M. & Fontecilla-Camps, J. C. 1996 Structure of the [NiFe] hydrogenase active site: evidence for biologically uncommon Fe ligands. J. Am. Chem. Soc. 118, 12 989-12 996.
53. Volbeda, A., Martin, L., Cavazza, C., Matho, M., Faber, B. W., Roseboom, W., Albracht, S. P. J., Garcin, E., Rousset, M., Fontecilla-Camps, J. C. In press. Structural basis for the different activation properties of the ready and unready oxidized states of [NiFe]-hydrogenases.