Hydrogen-induced activation of the [NiFe]-hydrogenase from Allochromatium vinosum as studied by stopped-flow infrared spectroscopy

Biochemistry

Volumn 43, Issue 21, 2004, Pages 6820-6831

  Kurkin, Sergei ^a   George, Simon J ^b   Thorneley, Roger N F ^b   Albracht, Simon P J ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b JOHN INNES CENTRE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMICAL ACTIVATION; DATA REDUCTION; ENZYMES; HYDROGEN; INFRARED SPECTROSCOPY; PHYSIOLOGY; REDUCTION; STOICHIOMETRY;

ACTIVE SITES; PROTONATION; ROOM TEMPERATURE (RT);

BIOCHEMISTRY;

HYDROGEN; HYDROGENASE; HYDROXYL GROUP; IRON; NICKEL;

ALLOCHROMATIUM VINOSUM; ANALYTIC METHOD; ARTICLE; CHROMATIUM; CONCENTRATION (PARAMETERS); ENZYME ACTIVATION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME SUBSTRATE; INFRARED SPECTROSCOPY; NONHUMAN; OXIDATION; PRIORITY JOURNAL; REDUCTION; ROOM TEMPERATURE; STEADY STATE;

BIOCHEMISTRY; CARBON MONOXIDE; CHROMATIACEAE; ENZYME ACTIVATION; HYDROGEN; HYDROGEN-ION CONCENTRATION; HYDROGENASE; KINETICS; OXYGEN; SPECTROSCOPY, FOURIER TRANSFORM INFRARED;

ALLOCHROMATIUM; ALLOCHROMATIUM VINOSUM; CHROMATIUM;

EID: 2542565159     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi049854c     Document Type: Article

References (51)

1. Cammack, R., Frey, M., and Robson, R. (2001) Hydrogen as a fuel. Learning from Nature, Taylor & Francis Inc, New York.
2. Adams, M. W. (1990) The structure and mechanism of iron-hydrogenases, Biochim. Biophys. Acta 1020, 115-145.
3. Albracht, S. P. J. (1994) Nickel hydrogenases: in search of the active site, Biochim. Biophys. Acta 1188, 167-204.
4. Vignais, P. M., Billoud, B., and Meyer, J. (2001) Classification and phylogeny of hydrogenases, FEMS Microbiol. Rev. 25, 455-501.
5. 10-Methylenetetrahydromethanopterin dehydrogenase from Methanobacterium thermoautotrophicum has hydrogenase activity, FEBS Lett. 261, 112-116.
6. 2, Arch. Microbiol. 169, 206-210.
7. Lyon, E. J., Shima, S., Buurman, G., Chowdhuri, S., Batschauer, A., Steinbach, K., and Thauer, R. K. (2004) UV-A/blue-light inactivation of the 'metal-free' hydrogenase (Hmd) from methanogenic archaea, Eur. J. Biochem. 271, 195-204.
8. Volbeda, A., Charon, M. H., Piras, C., Hatchikian, E. C., Frey, M., and Fontecilla-Camps, J. C. (1995) Crystal structure of the nickel-iron hydrogenase from Desulfovibrio gigas, Nature 373, 580-587.
9. Volbeda, A., Carcia, E., Piras, C., deLacey, A. L., Fernandez, V. M., Hatchikian, E. C., Frey, M., and Fontecilla-Camps, J. C. (1996) Structure of the [NiFe] hydrogenase active site: Evidence for biologically uncommon Fe ligands, J. Am. Chem. Soc. 118, 12989-12996.
10. Montet, Y., Amara, P., Volbeda, A., Vernede, X., Hatchikian, E. C., Field, M. J., Frey, M., and Fontecilla-Camps, J. C. (1997) Gas access to the active site of Ni-Fe hydrogenases probed by X-ray crystallography and molecular dynamics, Nat. Struct. Biol. 4, 523-526.
11. Higuchi, Y., Yagi, T., and Yasuoka, N. (1997) Unusual ligand structure in Ni-Fe active center and an additional Mg site in hydrogenase revealed by high-resolution X-ray structure analysis, Structure 5, 1671-1680.
12. 2, as revealed by X-ray structure analysis at 1.4 angstrom resolution, Struct. Folding Des. 7, 549-556.
13. Garcin, E., Vernede, X., Hatchikian, E. C., Volbeda, A., Frey, M., and Fontecilla-Camps, J. C. (1999) The crystal structure of a reduced [NiFeSe] hydrogenase provides an image of the activated catalytic center, Struct. Folding Des. 7, 557-566.
14. Matias, P. M., Soares, C. M., Saraiva, L. M., Coelho, R., Morais, J., Le Gall, J., and Carrondo, M. A. (2001) [NiFe] hydrogenase from Desulfovibrio desulfuricans ATCC 27774: gene sequencing, three-dimensional structure determination and refinement at 1.8 Å and modelling studies of its interaction with the tetrahaem cytochrome c3, J. Biol. Inorg. Chem. 6, 63-81.
15. Ogata, H., Mizoguchi, Y., Mizuno, N., Miki, K., Adachi, S., Yasuoka, N., Yagi, T., Yamauchi, O., Hirota, S., and Higuchi, Y. (2002) Structural studies of the carbon monoxide complex of [NiFe]hydrogenase from Desulfovibrio vulgaris Miyazaki F: suggestion for the initial activation site for dihydrogen, J. Am. Chem. Soc. 124, 11628-11635.
16. Volbeda, A., Montet, Y., Vernède, X., Hatchikian, E. C., and Fontecilla-Camps, J. C. (2002) High-resolution crystallographic analysis of Desulfovibrio fructosovorans [NiFe] hydrogenase, Int. J. Hydr. Energy 27, 1449-1461.
17. Bagley, K. A., Duin, E. C., Roseboom, W., Albracht, S. P. J., and 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.
18. Happe, R. P., Roseboom, W., Pierik, A. J., Albracht, S. P. J., and Bagley, K. A. (1997) Biological activation of hydrogen, Nature 385, 126.
19. 2, J. Biol. Chem. 274, 3331-3337.
20. Van der Spek, T. M., Arendsen, A. F., Happe, R. P., Yun, S., Bagley, K. A., Stufkens, D. J., Hagen, W. R., and 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.
21. De Lacey, A. L., Hatchikian, E. C., Volbeda, A., Frey, M., Fontecilla-Camps, J. C., and Fernandez, V. M. (1997) Infrared spectroelectrochemical characterization of the [NiFe] hydrogenase of Desulfovibrio gigas, J. Am. Chem. Soc. 119, 7181-7189.
22. Surerus, K. K., Chen, M., van der Zwaan, J. W., Rusnak, F. M., Kolk, M., Duin, E. C., Albracht, S. P. J., and 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.
23. Gu, Z. J., Dong, J., Allan, C. B., Choudhury, S. B., Franco, R., Moura, J. J. G., LeGall, J., Przybyla, A. E., Roseboom, W., Albracht, S. P. J., Axley, M. J., Scott, R. A., and Maroney, M. J. (1996) Structure of the Ni sites in hydrogenases by X-ray absorption spectroscopy. Species variation and the effects of redox poise, J. Am. Chem. Soc. 118, 11155-11165.
24. Davidson, G., Choudhury, S. B., Gu, Z., Bose, K., Roseboom, W., Albracht, S. P. J., and 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.
25. Huyett, J. E., Carepo, M., Pamplona, A., Franco, R., Moura, I., Moura, J. J. G., and 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.
26. George, S. J., Ashby, G. A., Wharton, C. W., and Thorneley, R. N. F. (1997) Time-resolved binding of carbon monoxide to nitrogenase monitored by stopped-flow infrared spectroscopy, J. Am. Chem. Soc. 119, 6450-6451.
27. Thorneley, R. N. F., and George, S. J. (2000) Time-resolved infrared spectroscopy of functioning nitrogenase, in Nitrogen Fixation in Bacteria: Cellular and Molecular Biology (Triplett, E., Ed.) pp 81-99, Horizon Scientific Press, Wymondham, UK.
28. Muthusamy, M., Ambundo, E. A., George, S. J., Lippard, S. J., and Thorneley, R. N. F. (2003) Stopped-Flow Fourier Transform Infrared Spectroscopy of Nitromethane Oxidation by the Diiron(IV) Intermediate of Methane Monooxygenase, J. Am. Chem. Soc. 125, 11150-11151.
29. Coremans, J. M. C. C., van der Zwaan, J. W., and 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.
30. 2 with active [NiFe]-hydrogenase from Allochromatium vinosum. A stopped-flow infrared study, Biochemistry 43, 6808-6819.
31. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilising the principle of protein-dye binding, Anal. Biochem. 100, 201-220.
32. Bleijlevens, B., Faber, B. W., and 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.
33. White, A. J., Drabble, K., and Wharton, C. W. (1995) A stopped-flow apparatus for infrared-spectroscopy of aqueous-solutions, Biochem. J. 306, 843-849.
34. George, S. J., Allen, J. W. A., Ferguson, S. J., and Thorneley, R. N. F. (2000) Time-resolved infrared spectroscopy reveals a stable ferric heme-NO intermediate in the reaction of Paracoccus pantotrophus cytochrome cdl nitrite reductase with nitrite, J. Biol. Chem. 275, 33231-33237.
35. Kurkin, S., Meuer, J., Koch, J., Hedderich, R., and Albracht, S. P. J. (2002) The membrane-bound [NiFe]-hydrogenase (Ech) from Methanosarcina barkeri: unusual properties of the iron-sulphur clusters, Eur. J. Biochem. 269, 6101-6111.
36. Fernandez, V. M., Hatchikian, E. C., and Cammack, R. (1985) Properties and reactivation of two different deactivated forms of Desulfovibrio gigas hydrogenase, Biochim. Biophys. Acta 832, 69-79.
37. Fernandez, V. M., Rao, K. K., Fernandez, M. A., and Cammack, R. (1986) Activation and deactivation of the membrane-bound hydrogenase from Desulfovibrio desulfuricans, Norway strain, Biochimie 68, 43-48.
38. 13CO on EPR spectra of nickel in hydrogenase from Chromatium vinosum, Biochim. Biophys. Acta 1041, 101-110.
39. Cammack, R., Patil, D., Aquirre, R., and Hatchikian, E. C. (1982) Redox properties of the esr-detectable nickel in hydrogenase from Desulfovibrio gigas, FEBS Lett. 142, 289-292.
40. Teixeira, M., Moura, I., Xavier, A. V., Moura, J. J. G., LeGall, J., DerVartanian, D. V., Peck, H. D., Jr., and 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, 16435-16450.
41. Bleijlevens, B. (2002) Activation and sensing of hydrogen in nature, Ph.D. Thesis, University of Amsterdam, Amsterdam.
42. Bagley, K. A., Van Garderen, C. J., Chen, M., Duin, E. C., Albracht, S. P. J., and Woodruff, W. H. (1994) Infrared studies on the interaction of carbon monoxide with divalent nickel in hydrogenase from Chromatium vinosum, Biochemistry 33, 9229-9236.
43. Bleijlevens, B. (2001) The hydrogen-consumption activity of the [NiFe] hydrogenase of Allochromatium vinosum in different redox states, in Hydrogen as a Fuel. Learning from Nature (Cammack, R., Frey, M., and Robson, R., Eds.) pp 82-84, Taylor & Francis, London.
44. Van der Zwaan, J. W., Albracht, S. P. J., Fontijn, R. D., and 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.
45. 2 and hydrogenase, Biochim. Biophys. Acta 1119, 148-156.
46. Barondeau, D. P., Roberts, L. M., and Lindahl, P. A. (1994) Stability of the Ni-C state and oxidative titrations of Desulfovibrio-gigas hydrogenase monitored by EPR and electronic absorption spectroscopies, J. Am. Chem. Soc. 116, 3442-3448.
47. Cammack, R., Patil, D. S., Hatchikian, E. C., and Fernández, V. M. (1987) Nickel and iron-sulphur centres in Desulfovibrio gigas hydrogenase: ESR spectra, redox properties and interactions, Biochim. Biophys. Acta 912, 98-109.
48. Foerster, S., Stein, M., Brecht, M., Ogata, H., Higuchi, Y., and 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.
49. 2-sensing hydrogenase from Ralstonia eutropha in its reduced state by HYSCORE and ENDOR spectroscopy, J. Am. Chem. Soc. 125, 13075-13083.
50. Tran-Betcke, A., Warnecke, U., Bocker, C., Zaborosch, C., and Friedrich, B. (1990) Cloning and nucleotide sequences of the genes for the subunits of NAD-reducing hydrogenase of Alcaligenes eutrophus H16, J. Bacteriol. 172, 2920-2929.
51. Jones, A. K., Lamle, S. E., Pershad, H. R., Vincent, K. A., Albracht, S. P. J., and 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.