The crystal structure of the [NiFe] hydrogenase from the photosynthetic bacterium allochromatium vinosum: Characterization of the oxidized enzyme (Ni-A state)

Journal of Molecular Biology

Volumn 402, Issue 2, 2010, Pages 428-444

  Ogata, Hideaki ^a   Kellers, Petra ^a   Lubitz, Wolfgang ^a  

^a MAX PLANCK INSTITUTE FOR CHEMICAL ENERGY CONVERSION   (Germany)

Author keywords

Allochromatium vinosum; Iron sulfur cluster; Ni A state; Photosynthetic purple sulfur bacterium; NiFe hydrogenase

Indexed keywords

CYSTEINE DERIVATIVE; HETERODIMER; IRON; MAGNESIUM ION; METAL ION; NICKEL; NICKEL IRON HYDROGENASE; SULFUR; HYDROGENASE; NICKEL-IRON HYDROGENASE; PROTEIN BINDING; PROTEIN SUBUNIT;

ALLOCHROMATIUM VINOSUM; AMINO ACID SEQUENCE; ARTICLE; CATALYSIS; CRYSTAL STRUCTURE; DESULFOVIBRIO; ELECTRON SPIN RESONANCE; ELECTRON TRANSPORT; ENZYME ACTIVE SITE; ENZYME STRUCTURE; INFRARED SPECTROSCOPY; NONHUMAN; OXIDATION; PHOTOTROPHIC BACTERIUM; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; CHEMICAL STRUCTURE; CHEMISTRY; CHROMATIACEAE; COMPARATIVE STUDY; ENZYMOLOGY; METABOLISM; OXIDATION REDUCTION REACTION; PROTEIN MULTIMERIZATION; PROTEIN QUATERNARY STRUCTURE; PROTEIN SUBUNIT; X RAY CRYSTALLOGRAPHY;

ALLOCHROMATIUM VINOSUM; BACTERIA (MICROORGANISMS); DESULFOVIBRIO; DESULFOVIBRIO SP.; PHOTOBACTERIA;

CATALYTIC DOMAIN; CHROMATIACEAE; CRYSTALLOGRAPHY, X-RAY; DESULFOVIBRIO; ELECTRON SPIN RESONANCE SPECTROSCOPY; HYDROGENASE; MODELS, MOLECULAR; NICKEL; OXIDATION-REDUCTION; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; PROTEIN SUBUNITS; SPECTROSCOPY, FOURIER TRANSFORM INFRARED;

EID: 77956759468     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2010.07.041     Document Type: Article

References (75)

1. Vignais P.M., Billoud B. Occurrence, classification, and biological function of hydrogenases: an overview. Chem. Rev. 2007, 107:4206-4272.
2. Fontecilla-Camps J.C., Volbeda A., Cavazza C., Nicolet Y. Structure/function relationships of [NiFe]- and [FeFe]-hydrogenases. Chem. Rev. 2007, 107:4273-4303.
3. 2 activation. Angew. Chem., Int. Ed. 2009, 48:6457-6460.
4. Peters J.W., Lanzilotta W.N., Lemon B.J., Seefeldt L.C. X-ray crystal structure of the Fe-only hydrogenase (Cpl) from Clostridium pasteurianum to 1.8 Å resolution. Science 1998, 282:1853-1858.
5. Shima S., Pilak O., Vogt S., Schick M., Stagni M.S., Meyer-Klaucke W., et al. The crystal structure of [Fe]-hydrogenase reveals the geometry of the active site. Science 2008, 321:572-575.
6. 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. Struct. Fold. Des. 1999, 7:13-23.
7. Pilak O., Mamat B., Vogt S., Hagemeier C.H., Thauer R.K., Shima S., et al. The crystal structure of the apoenzyme of the iron-sulphur cluster-free hydrogenase. J. Mol. Biol. 2006, 358:798-809.
8. Burgdorf T., Lenz O., Buhrke T., van der Linden E., Jones A.K., Albracht S.P.J., Friedrich B. [NiFe]-hydrogenases of Ralstonia eutropha H16: modular enzymes for oxygen-tolerant biological hydrogen oxidation. J. Mol. Microbiol. Biotechnol. 2005, 10:181-196.
9. Guiral M., Tron P., Aubert C., Gloter A., Iobbi-Nivol C., Giudici-Orticoni M.T. A membrane-bound multienzyme, hydrogen-oxidizing, and sulfur-reducing complex from the hyperthermophilic bacterium Aquifex aeolicus. J. Biol. Chem. 2005, 280:42004-42015.
10. 2 as performed by the membrane-bound [NiFe]-hydrogenase of Ralstonia eutropha. Chem. Phys. Chem. 2010, 11:1107-1119.
11. Higuchi Y., Yagi T., Yasuoka N. Unusual ligand structure in Ni-Fe active center and an additional Mg site in hydrogenase revealed by high resolution X-ray structure analysis. Structure 1997, 5:1671-1680.
12. 2, as revealed by X-ray structure analysis at 1.4 Å resolution. Structure 1999, 7:549-556.
13. 3. J. Biol. Inorg. Chem. 2001, 6:63-81.
14. Montet Y., Amara P., Volbeda A., Vernede X., Hatchikian E.C., Field M.J., et al. Gas access to the active site of Ni-Fe hydrogenases probed by X-ray crystallography and molecular dynamics. Nat. Struct. Biol. 1997, 4:523-526.
15. Ogata H., Mizoguchi Y., Mizuno N., Miki K., Adachi S., Yasuoka N., et al. 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. 2002, 124:11628-11635.
16. Ogata H., Hirota S., Nakahara A., Komori H., Shibata N., Kato T., et al. Activation process of [NiFe] hydrogenase elucidated by high-resolution X-ray analyses: conversion of the ready to the unready state. Structure 2005, 13:1635-1642.
17. Volbeda A., Martin L., Cavazza C., Matho M., Faber B.W., Roseboom W., et al. Structural differences between the ready and unready oxidized states of [NiFe] hydrogenases. J. Biol. Inorg. Chem. 2005, 10:239-249.
18. Volbeda A., Charon M.H., Piras C., Hatchikian E.C., Frey M., Fontecilla-Camps J.C. Crystal structure of the nickel-iron hydrogenase from Desulfovibrio gigas. Nature 1995, 373:580-587.
19. Bagley K.A., Duin E.C., Roseboom W., Albracht S.P.J., Woodruff W.H. Infrared detectable groups sense changes in charge density on the nickel center in hydrogenase from Chromatium vinosum. Biochemistry 1995, 34:5527-5535.
20. 2. J. Biol. Chem. 1999, 274:3331-3337.
21. Ogata H., Lubitz W., Higuchi Y. [NiFe] hydrogenases: structural and spectroscopic studies of the reaction mechanism. Dalton Trans. 2009, 7577-7587.
22. Pandelia M.E., Ogata H., Lubitz W. Intermediates in the catalytic cycle of [NiFe] hydrogenase: functional spectroscopy of the active site. Chem. Phys. Chem. 2010, 11:1127-1140.
23. Leroux F., Dementin S., Burlatt B., Cournac L., Volbeda A., Champ S., et al. Experimental approaches to kinetics of gas diffusion in hydrogenase. Proc. Natl Acad. Sci. USA 2008, 105:11188-11193.
24. Dementin S., Leroux F., Cournac L., De Lacey A.L., Volbeda A., Léger C., et al. Introduction of methionines in the gas channel makes [NiFe] hydrogenase aero-tolerant. J. Am. Chem. Soc. 2009, 131:10156-10164.
25. Menon N.K., Robbins J., DerVartanian M., Patil D., Peck H.D., Menon A.L., et al. Carboxy-terminal processing of the large subunit of [NiFe] hydrogenases. FEBS Lett. 1993, 331:91-95.
26. Garcin E., Vernede X., Hatchikian E.C., Volbeda A., Frey M., Fontecilla-Camps J.C. The crystal structure of a reduced [NiFeSe] hydrogenase provides an image of the activated catalytic center. Structure 1999, 7:557-566.
27. Marques M.C., Coelho R., De Lacey A.L., Pereira I.A., Matias P.M. The three-dimensional structure of [NiFeSe] hydrogenase from Desulfovibrio vulgaris Hildenborough: a hydrogenase without a bridging ligand in the active site in its oxidised, "as-isolated" state. J. Mol. Biol. 2010, 396:893-907.
28. Lubitz W., Reijerse E., van Gastel M. [NiFe] and [FeFe] hydrogenases studied by advanced magnetic resonance techniques. Chem. Rev. 2007, 107:4331-4365.
29. Albracht S.P.J., Kalkman M.L., Slater E.C. Magnetic interaction of nickel(III) and the iron-sulfur cluster in hydrogenase from Chromatium vinosum. Biochim. Biophys. Acta 1983, 724:309-316.
30. Lamle S.E., Albracht S.P.J., Armstrong F.A. Electrochemical potential-step investigations of the aerobic interconversions of [NiFe]-hydrogenase from Allochromatium vinosum: insights into the puzzling difference between unready and ready oxidized inactive states. J. Am. Chem. Soc. 2004, 126:14899-14909.
31. van Gastel M., Stein M., Brecht M., Schröder O., Lendzian F., Bittl R., et al. A single-crystal ENDOR and density functional theory study of the oxidized states of the [NiFe] hydrogenase from Desulfovibrio vulgaris Miyazaki F. J. Biol. Inorg. Chem. 2006, 11:41-51.
32. Albracht S.P.J. Nickel hydrogenases-in search of the active site. Biochim. Biophys. Acta 1994, 1188:167-204.
33. Lubitz W., van Gastel M., Gärtner W. Nickel iron hydrogenases. Met. Ions Life Sci. 2007, 2:279-322.
34. Surerus K.K., Chen M., van der Zwaan J.W., Rusnak F.M., Kolk M., Duin E.C., et al. Further characterization of the spin coupling observed in oxidized hydrogenase from Chromatium vinosum-a Mössbauer and multifrequency EPR study. Biochemistry 1994, 33:4980-4993.
35. Teixeira M., Moura I., Xavier A.V., Moura J.J.G., LeGall J., Dervartanian D.V., et al. Redox intermediates of Desulfovibrio gigas [NiFe] hydrogenase generated under hydrogen-Mössbauer and EPR characterization of the metal centers. J. Biol. Chem. 1989, 264:16435-16450.
36. Albracht S.P.J., van der Zwaan J.W., Fontijn R.D. EPR spectrum at 4, 9 and 35 GHz of hydrogenase from Chromatium vinosum-direct evidence for spin-spin interaction between Ni(III) and the iron-sulfur cluster. Biochim. Biophys. Acta 1984, 766:245-258.
37. Saggu M., Zebger I., Ludwig M., Lenz O., Friedrich B., Hildebrandt P., Lendzian F. Spectroscopic insights into the oxygen-tolerant membrane-associated [NiFe] hydrogenase of Ralstonia eutropha H16. J. Biol. Chem. 2009, 284:16264-16276.
38. Albracht S.P.J., Fontijn R.D., van der Zwaan J.W. Destruction and reconstitution of the activity of hydrogenase from Chromatium vinosum. Biochim. Biophys. Acta 1985, 832:89-97.
39. Brugna-Guiral M., Tron P., Nitschke W., Stetter K.O., Burlat B., Guigliarelli B., et al. [NiFe] hydrogenases from the hyperthermophilic bacterium Aquifex aeolicus: properties, function, and phylogenetics. Extremophiles 2003, 7:145-157.
40. Palagyi-Meszaros L.S., Maroti J., Latinovics D., Balogh T., Klement E., Medzihradszky K.F., et al. Electron-transfer subunits of the NiFe hydrogenases in Thiocapsa roseopersicina BBS. FEBS J. 2009, 276:164-174.
41. 3 catalyzed by hydrogenase with hydrogen. Biochim. Biophys. Acta 1984, 767:288-294.
42. 3 with [NiFe] hydrogenase from Desulfovibrio vulgaris Miyazaki F. Biochemistry 2006, 45:1653-1662.
43. Bagley K.A., Van Garderen C.J., Chen M., Duin E.C., Albracht S.P.J., Woodruff W.H. Infrared studies on the interaction of carbon monoxide with divalent nickel in hydrogenase from Chromatium vinosum. Biochemistry 1994, 33:9229-9236.
44. Gessner C., Stein M., Albracht S.P.J., Lubitz W. Orientation-selected ENDOR of the active center in Chromatium vinosum [NiFe] hydrogenase in the oxidized "ready" state. J. Biol. Inorg. Chem. 1999, 4:379-389.
45. Gu Z.J., Dong J., Allan C.B., Choudhury S.B., Franco R., Moura J.J.G., et al. Structure of the Ni sites in hydrogenases by X-ray absorption spectroscopy. Species variation and the effects of redox poise. J. Am. Chem. Soc. 1996, 118:11155-11165.
46. 13CO on EPR spectra of nickel in hydrogenase from Chromatium vinosum. Biochim. Biophys. Acta 1990, 1041:101-110.
47. Pandelia M.E., Fourmond V., Tron-Infossi P., Lojou E., Bertrand P., Léger C., et al. Membrane-bound hydrogenase I from the hyperthermophilic bacterium Aquifex aeolicus: enzyme activation, redox intermediates and oxygen tolerance. J. Am. Chem. Soc. 2010, 132:6991-7004.
48. Kellers P., Ogata H., Lubitz W. Purification, crystallization and preliminary X-ray analysis of the membrane-bound [NiFe] hydrogenase from Allochromatium vinosum. Acta Crystallogr., Sect. F: Struct. Biol. Cryst. Commun. 2008, 64:719-722.
49. Bleijlevens B., van Broekhuizen F.A., De Lacey A.L., Roseboom W., Fernandez V.M., Albracht S.P.J. The activation of the [NiFe]-hydrogenase from Allochromatium vinosum. An infrared spectro-electrochemical study. J. Biol. Inorg. Chem. 2004, 9:743-752.
50. Long M.N., Liu J.J., Chen Z.F., Bleijlevens B., Roseboom W., Albracht S.P.J. Characterization of a HoxEFUYH type of [NiFe] hydrogenase from Allochromatium vinosum and some EPR and IR properties of the hydrogenase module. J. Biol. Inorg. Chem. 2007, 12:62-78.
51. Devine E., Holmqvist M., Stensjö K., Lindblad P. Diversity and transcription of proteases involved in the maturation of hydrogenases in Nostoc punctiforme ATCC 29133 and Nostoc sp. strain PCC 7120. BMC Microbiol. 2009, 9:53.
52. Dementin S., Burlat B., De Lacey A.L., Pardo A., Adryanczyk-Perrier G., Guigliarelli B., et al. A glutamate is the essential proton transfer gate during the catalytic cycle of the [NiFe] hydrogenase. J. Biol. Chem. 2004, 279:10508-10513.
53. Coremans J.M.C.C., van der Zwaan J.W., Albracht S.P.J. Distinct redox behavior of prosthetic groups in ready and unready hydrogenase from Chromatium vinosum. Biochim. Biophys. Acta 1992, 1119:157-168.
54. 4Ca complex in single crystals of photosystem II: a case study for metalloprotein crystallography. Proc. Natl Acad. Sci. USA 2005, 102:12047-12052.
55. von Sonntag C. Free-Radical-Induced DNA Damage and Its Repair: A Chemical Perspective 2006, Springer-Verlag, Berlin, Germany.
56. r state and its light sensitivity. J. Biol. Inorg. Chem. 2009, 14:1227-1241.
57. Goenka Agrawal A., van Gastel M., Gärtner W., Lubitz W. Hydrogen bonding affects the [NiFe] active site of Desulfovibrio vulgaris Miyazaki F hydrogenase: a hyperfine sublevel correlation spectroscopy and density functional theory study. J. Phys. Chem. B 2006, 110:8142-8150.
58. Higuchi Y., Yagi T. Liberation of hydrogen sulfide during the catalytic action of Desulfovibrio hydrogenase under the atmosphere of hydrogen. Biochem. Biophys. Res. Commun. 1999, 255:295-299.
59. Vincent K.A., Belsey N.A., Lubitz W., Armstrong F.A. Rapid and reversible reactions of [NiFe]-hydrogenases with sulfide. J. Am. Chem. Soc. 2006, 128:7448-7449.
60. Galvan I.F., Volbeda A., Fontecilla-Camps J.C., Field M.J. A QM/MM study of proton transport pathways in a [NiFe] hydrogenase. Proteins: Struct., Funct., Bioinform. 2008, 73:195-203.
61. Teixeira V.H., Soares C.M., Baptista A.M. Proton pathways in a [NiFe]-hydrogenase: a theoretical study. Proteins: Struct., Funct., Bioinform. 2008, 70:1010-1022.
62. Cammack R., Rao K.K., Serra J., Llama M.J. The redox properties of the iron-sulfur cluster in hydrogenase from Chromatium vinosum, strain-D. Biochimie 1986, 68:93-96.
63. Pandelia, M. E. (2009). [NiFe] hydrogenases from Desulfovibrio vulgaris Miyazaki F and Aquifex aeolicus studied by FTIR, EPR and electrochemical techniques: redox intermediates, O2/CO sensitivity and light-induced effects. Dissertation, Technische Universität Berlin.
64. van Gastel M., Fichtner C., Neese F., Lubitz W. EPR experiments to elucidate the structure of the ready and unready states of the [NiFe] hydrogenase of Desulfovibrio vulgaris Miyazaki F. Biochem. Soc. Trans. 2005, 33:7-11.
65. Saggu M., Teutloff C., Ludwig M., Brecht M., Pandelia M.E., Lenz O., et al. Comparison of the membrane-bound [NiFe] hydrogenases from R. eutropha H16 and D. vulgaris Miyazaki F in the oxidized ready state by pulsed EPR. Phys. Chem. Chem. Phys. 2010, 12:2139-2148.
66. Kellers, P. (2008). Strukturelle und funktionelle Charakterisierung der [NiFe]-Hydrogenase aus Allochromatium vinosum. Dissertation, Heinrich-Heine-Universität Düsseldorf.
67. Leslie A.G.W. Recent changes to the MOSFLM package for processing film and image plate data. Joint CCP4 + ESF-EAMCB Newsletter on Protein Crystallography 1992, 26.
68. Kabsch W. Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J. Appl. Crystallogr. 1993, 26:795-800.
69. Collaborative Computational Project No.4 The CCP4 Suite: programs for protein crystallography. Acta Crystallogr., Sect. D: Biol. Crystallogr. 1994, 50:760-763.
70. Vagin A., Teplyakov A. MOLREP: an automated program for molecular replacement. J. Appl. Crystallogr. 1997, 30:1022-1025.
71. Emsley P., Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr., Sect. D: Biol. Crystallogr. 2004, 60:2126-2132.
72. Vagin A.A., Steiner R.A., Lebedev A.A., Potterton L., McNicholas S., Long F., Murshudov G.N. REFMAC5 dictionary: organization of prior chemical knowledge and guidelines for its use. Acta Crystallogr., Sect. D: Biol. Crystallogr. 2004, 60:2184-2195.
73. Lovell S.C., Davis I.W., Arendall W.B., de Bakker P.I.W., Word J.M., Prisant M.G., et al. Structure validation by Calpha geometry: phi, psi and Cbeta deviation. Proteins: Struct., Funct., Genet. 2003, 50:437-450.
74. Petrey D., Honig B. GRASP2: visualization, surface properties, and electrostatics of macromolecular structures and sequences. Methods Enzymol. 2003, 374:492-509.
75. Delano W.L. The PyMOL Molecular Graphics System 2002, DeLano Scientific, Palo Alto, CA, http://www.pymol.org.