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Structural differences between the ready and unready oxidized states of [NiFe] hydrogenases

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An Erratum to this article was published on 10 June 2005

Abstract

[NiFe] hydrogenases catalyze the reversible heterolytic cleavage of molecular hydrogen. Several oxidized, inactive states of these enzymes are known that are distinguishable by their very different activation properties. So far, the structural basis for this difference has not been understood because of lack of relevant crystallographic data. Here, we present the crystal structure of the ready Ni-B state of Desulfovibrio fructosovorans [NiFe] hydrogenase and show it to have a putative μ-hydroxo Ni–Fe bridging ligand at the active site. On the other hand, a new, improved refinement procedure of the X-ray diffraction data obtained for putative unready Ni-A/Ni-SU states resulted in a more elongated electron density for the bridging ligand, suggesting that it is a diatomic species. The slow activation of the Ni-A state, compared with the rapid activation of the Ni-B state, is therefore proposed to result from the different chemical nature of the ligands in the two oxidized species. Our results along with very recent electrochemical studies suggest that the diatomic ligand could be hydro–peroxide.

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Abbreviations

DFT:

Density functional theory

ENDOR:

Electron–nuclear double resonance

EPR:

Electron paramagnetic resonance

ESRF:

European Synchrotron Radiation Facility

EXAFS:

Extended X-ray absorption fine structure

FT:

Fourier transform

PEG:

Poly(ethylene glycol)

TLS:

Translation–libration–screw

References

  1. Adams MWW (1990) Biochim Biophys Acta 1020:115–145

    Google Scholar 

  2. Albracht SPJ (1994) Biochim Biophys Acta 1188:167–204

    CAS  PubMed  Google Scholar 

  3. Frey M, Fontecilla-Camps JC, Volbeda A (2001) In Messerschmidt A, Huber R, Poulos T, Wieghardt K (eds) Handbook of metalloproteins, vol 2. Wiley, Chichester, pp 880–896

  4. Cammack R, Robson R, Frey M (eds) (2001) Hydrogen as a fuel, learning from nature. Taylor & Francis, London

    Google Scholar 

  5. Vignais PM, Billoud B, Meyer J (2001) FEMS Microbiol Rev 25:455–501

    Article  CAS  PubMed  Google Scholar 

  6. Shima S, Lyon EJ, Sordel-Klippert M, Kauss M, Kahnt J, Thauer RK, Steinbach K, Xie X, Verdier L, Griesinger C (2004) Angew Chem 43:2547–2551

    Google Scholar 

  7. Lyon EJ, Shima S, Boecher R, Thauer RK, Grevels FW, Bill E, Roseboom W, Albracht SP (2004) J Am Chem Soc 126:14239–14248

    Google Scholar 

  8. Albracht SPJ, Graf EG, Thauer RK (1982) FEBS Lett 140:311–313

    Google Scholar 

  9. Moura JJG, Moura I, Huynh B-H, Kruger HJ, Teixeira M, DuVarney RC, DerVartanian DV, Xavier AV, Peck HD Jr, LeGall J (1982) Biochem Biophys Res Commun 108:1388–1393

    CAS  PubMed  Google Scholar 

  10. Cammack R, Patil DS, Hatchikian EC, Fernandez VM (1987) Biochim Biophys Acta 912:98–109

    Article  CAS  Google Scholar 

  11. Teixeira M, Moura I, Xavier AV, Huynh B-H, DerVartanian DV, Peck HD Jr, LeGall J, Moura JJG (1985) J Biol Chem 260:8942–8950

    Google Scholar 

  12. Teixeira M, Moura I, Xavier AV, Moura JJG, LeGall J, DerVartanian DV, Peck HD Jr, Huynh B-H (1989) J Biol Chem 264:16435–16450

    CAS  PubMed  Google Scholar 

  13. Fernandez VM, Hatchikian EC, Cammack R (1985) Biochim Biophys Acta 832:69–79

    Article  CAS  Google Scholar 

  14. Fernandez VM, Hatchikian EC, Patil DS, Cammack R (1986) Biochim Biophys Acta 883:145–154

    Google Scholar 

  15. Volbeda A, Garcin E, Piras C, De Lacey AL, Fernandez VM, Hatchikian EC, Frey M, Fontecilla-Camps JC (1996) J Am Chem Soc 118:12989–12996

    Article  CAS  Google Scholar 

  16. De Lacey AL, Hatchikian EC, Volbeda A, Frey M, Fontecilla-Camps JC, Fernandez VM (1997) J Am Chem Soc 119:7181–7189

    Article  Google Scholar 

  17. Volbeda A, Charon MH, Piras C, Hatchikian EC, Frey M, Fontecilla-Camps JC (1995) Nature 373:580–587

    Article  CAS  PubMed  Google Scholar 

  18. Bagley KA, Duin EC, Roseboom W, Albracht SPJ, Woodruff WH (1995) Biochemistry 34:5527–5535

    CAS  PubMed  Google Scholar 

  19. Happe RP, Roseboom W, Pierik AJ, Albracht SPJ, Bagley KA (1997) Nature 385:126

    Article  CAS  PubMed  Google Scholar 

  20. Pierik AJ, Roseboom W, Happe RP, Bagley KA, Albracht SPJ (1999) J Biol Chem 274:3331–3337

    Article  CAS  PubMed  Google Scholar 

  21. Volbeda A, Montet Y, Vernède X, Hatchikian EC, Fontecilla-Camps JC (2002) Int J Hydrogen Energy 27:1449–1461

    Google Scholar 

  22. Higuchi Y, Yagi T, Yasuoka N (1997) Structure 5:1671–1680

    Article  CAS  PubMed  Google Scholar 

  23. Matias PM, Soares CM, Saraiva LM, Coelho R, Morais J, Le Gall J, Carrondo MA (2001) J Biol Inorg Chem 6:63–81

    Article  CAS  PubMed  Google Scholar 

  24. Van der Zwaan JW, Coremans JM, Bouwens EC, Albracht SPJ (1990) Biochim Biophys Acta 1041:101–110

    PubMed  Google Scholar 

  25. Higuchi Y, Ogata H, Miki K, Yasuoka N, Yagi T (1999) Structure 7:549–556

    Article  CAS  PubMed  Google Scholar 

  26. Garcin E, Vernède X, Hatchikian EC, Volbeda A, Frey M, Fontecilla-Camps JC (1999) Structure 7:557–566

    Article  CAS  PubMed  Google Scholar 

  27. Albracht SPJ, Fontijn RD, Van der Zwaan JW (1985) Biochim Biophys Acta 832:89–97

    Google Scholar 

  28. Cypionka H (2000) Annu Rev Microbiol 54:827–848

    Google Scholar 

  29. Hatchikian EC, Traore AS, Fernandez VM, Cammack R (1990) Eur J Biochem 187:635–643

    Google Scholar 

  30. Bleijlevens B, Faber BW, Albracht SPJ (2001) J Biol Inorg Chem 6:763–769

    Article  CAS  PubMed  Google Scholar 

  31. De Lacey AL, Stadler C, Fernandez VM, Hatchikian EC, Fan H-J, Li S, Hall MB (2002) J Biol Inorg Chem 7:318–326

    Article  PubMed  Google Scholar 

  32. Kabsch W (2001) International tables for crystallography. In: Rossmann MG, Arnold E (eds) Crystallography of biological macromolecules, vol F. Kluwer Academic Publishers, Dordrecht, 25.2.9

  33. Navaza J (1994) Acta Cryst A50:157–163

    Google Scholar 

  34. De Lacey AL, Fernandez VM, Rousset M, Cavazza C, Hatchikian EC (2003) J Biol Inorg Chem 8:129–134

    Google Scholar 

  35. Brünger AT, Adams PD, Clore GM, DeLano WL, Gros P, Grosse-Kunstleve RW, Jiang J-S, Kuszewski J, Nilges M, Pannu NS, Read RJ, Rice LM, Simonson T, Warren GL (1998) Acta Cryst D54:905–921

    Google Scholar 

  36. Murshudov GN, Vagin AA, Dodson EJ (1997) Acta Cryst D53:240–255

    Google Scholar 

  37. Winn MD, Isupov MN, Murshudov GN (2001) Acta Cryst D57:122–133

    Google Scholar 

  38. Gu Z, Dong J, Allan CB, Choudhury SB, Franco R, Moura JJG, Moura I, LeGall J, Przybyla AE, Roseboom W, Albracht SPJ, Axley MJ, Scott RA, Maroney MJ (1996) J Am Chem Soc 118:11155–11165

    Article  CAS  Google Scholar 

  39. Davidson G, Choudhury SB, Gu Z, Bose K, Roseboom W, Albracht SPJ, Maroney MJ (2000) Biochemistry 39:7468–7479

    Article  CAS  PubMed  Google Scholar 

  40. Gu W, Jacquamet L, Patil DS, Wang HX, Evans DJ, Millar M, Koch S, Eichhorn DM, Latimer M, Cramer SP (2003) J Inorg Biochem 93:41–51

    Google Scholar 

  41. Darensbourg DJ, Reibenspies JH, Lai C-H, Lee W-Z, Darensbourg MY (1997) J Am Chem Soc 119:7903–7904

    Google Scholar 

  42. Roussel A, Cambillau C (1991) The turbo-frodo graphics package. In: Silicon graphics geometry partners directory, Silicon Graphics Corporation, Mountain View, CA, pp 81

  43. Garcin E (1998) Thése doctorate, Université Joseph Fourier, Grenoble

  44. Montet Y (1998) Thése doctorate, Université Joseph Fourier, Grenoble

  45. Rousset M, Montet Y, Guigliarelli B, Forget N, Asso M, Bertrand P, Fontecilla-Camps JC, Hatchikian EC (1998) Proc Natl Acad Sci USA 95:11625–11630

    Google Scholar 

  46. Chabrière E, Volbeda A, Fontecilla-Camps JC, Roth M, Charon MH (1999) Acta Cryst D55:1546–1554

    Google Scholar 

  47. Montet Y, Amara P, Volbeda A, Vernede X, Hatchikian EC, Field MJ, Frey M, Fontecilla-Camps JC (1997) Nat Struct Biol 4:523–526

    CAS  PubMed  Google Scholar 

  48. Dole F, Fourner A, Magro V, Hatchikian EC, Bertrand P, Guigliarelli B (1997) Biochemistry 36:7847–7854

    Article  CAS  PubMed  Google Scholar 

  49. Kurkin S, George SJ, Thorneley RN, Albracht SP (2004) Biochemistry 43:6820–6831

    Article  CAS  PubMed  Google Scholar 

  50. Weik M, Ravelli RBG, Kryger G, McSweeney S, Raves ML, Harel M, Gros P, Silman I, Kroon J, Sussman JL (2000) Proc Natl Acad Sci USA 97:623–628

    Google Scholar 

  51. Burmeister WP (2000) Acta Cryst D56:328–341

    Google Scholar 

  52. Stein M, Van Lenthe E, Baerends EJ, Lubitz W (2001) J Am Chem Soc 123:5839–5840

    CAS  PubMed  Google Scholar 

  53. Stadler C, De Lacey AL, Montet Y, Volbeda A, Fontecilla-Camps JC, Conesa JC, Fernandez VM (2002) Inorg Chem 41:4424–4434

    Article  CAS  PubMed  Google Scholar 

  54. Niu S, Thomson LM, Hall MB (1999) J Am Chem Soc 121:4000–4007

    Article  CAS  Google Scholar 

  55. De Gioia L, Fantucci P, Guigliarelli B, Bertrand P (1999) Inorg Chem 38:2658–2662

    Article  Google Scholar 

  56. Salerno JC (1988) In: Lancaster JR Jr (ed) The bioinorganic chemistry of nickel, VCH, Weinheim, FRG, pp 53–71

  57. Geßner C, Trofanchuk O, Kawagoe K, Higuchi Y, Yasuoka N, Lubitz W (1996) Chem Phys Lett 256:518–524

    Google Scholar 

  58. Trofanchuk O, Stein M, Geßner C, Lendzian F, Higuchi Y, Lubitz W (2000) J Biol Inorg Chem 5:36–44

    Google Scholar 

  59. Surerus KK, Chen M, van der Zwaan JW, Rusnak FM, Kolk M, Duin EC, Albracht SPJ, Münck E (1994) Biochemistry 33:4980–4993

    CAS  PubMed  Google Scholar 

  60. George SJ, Kurkin S, Thorneley RN, Albracht, SP (2004) Biochemistry 43:6808–6819

    Article  CAS  PubMed  Google Scholar 

  61. Lamle SE, Albracht SPJ, Armstrong FA (2004) J Am Chem Soc 126:14899–14909

    Google Scholar 

  62. Fujita K, Schenker R, Gu W, Brunold TC, Cramer SP, Riordan CG (2004) Inorg Chem 43:3324–3326

    Google Scholar 

  63. Carepo M, Tierney DL, Brondino CD, Yang TC, Pamplona A, Telser J, Moura I, Moura JJ, Hoffman BM (2002) J Am Chem Soc 124:281–286

    Article  CAS  PubMed  Google Scholar 

  64. Claiborne A, Yeh JI, Mallet TC, Luba J, Crane EJ, Charrier C, Parsonage D (1999) Biochemistry 38:15407–15416

    Google Scholar 

  65. Claiborne A, Mallet TC, Yeh JI, Luba J, Parsonage D (2001) Adv Protein Chem 58:215–276

    Google Scholar 

  66. Kumar M, Colpas GJ, Day RO, Maroney MJ (1989) J Am Chem Soc 111:8323–8325

    Google Scholar 

  67. Farmer PJ, Verpeaux J-N, Amatore C, Darensbourg MY, Musie, G (1994) J Am Chem Soc 116:9355–9356

    Google Scholar 

  68. Huang W, Jia J, Cummings J, Nelson M, Schneider G, Lindqvist Y (1997) Structure 5:691–699

    Article  CAS  PubMed  Google Scholar 

  69. Farmer PJ, Reibenspies JH, Lindahl PA, Darensbourg MY (1993) J Am Chem Soc 115:4665–4674

    Google Scholar 

  70. Buonomo RM, Font I, Maguire MJ, Reibenspies JH, Tuntulani T, Darensbourg M (1995) J Am Chem Soc 117:963–973

    Google Scholar 

  71. Eremenko IL, Berke H (1994) Organometallics 13:244–25

    Google Scholar 

  72. Bleijlevens B, Van Broekhuizen FA, De Lacey AL, Roseboom W, Fernandez VM, Albracht SPJ (2004) J Biol Inorg Chem 9:743–753

    Google Scholar 

  73. Dementin S, Burlat B, De Lacey AL, Pardo A, Adryanczyk-Perrier G, Guigliarelli B, Fernandez VM, Rousset M (2004) J Biol Chem 179:1508–1513

    Google Scholar 

  74. Jones AK, Lamle SE, Pershad HR, Vincent KA, Albracht SPJ, Armstrong FA (2003) J Am Chem Soc 125:8505–8514

    Article  CAS  PubMed  Google Scholar 

  75. Howlin B, Butler SA, Moss DS, Harris GW, Driessen HPC (1993) J Appl Cryst 26:622–624

    Google Scholar 

  76. Collaborative Computational Project, Number 4 (1994) Acta Cryst D50:760–763

    Google Scholar 

  77. Kraulis PJ (1991) J Appl Crystallogr 24:946–950

    Article  Google Scholar 

  78. Lawrence MC, Bourke P (2000) J Appl Crystallogr 33:990–991

    Article  CAS  Google Scholar 

  79. Merrit EA, Bacon DJ (1997) Methods Enzymol 277:520–524

    Google Scholar 

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Acknowledgements

We thank Claude Hatchikian for providing us with aerobically purified enzyme preparations, Yaël Montet for initial crystallographic analyses of the S499A mutant of D. fructosovorans hydrogenase, Jacques Gaillard for performing EPR measurements of the anaerobically purified enzyme, Dominique Bourgeois for use of his “cryo-bench” to perform UV/vis measurements of crystals, Andy Thompson, Gordon Leonard and Julien Lescar for their help with data collection at the ESRF and Patricia Amara and Fraser Armstrong for helpful discussions. This work was supported by the CEA, the CNRS and the European Union BIOTECH Program, grant BIO4-98-0280. Atomic coordinates and structure factors have been deposited in the Protein Data Bank, with deposition codes IYQY (crystal A1), IYQN (crystal A2) and IYRQ (Ni-B state).

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Authors and Affiliations

  1. Laboratoire de Cristallographie et de Cristallogenèse des Protèines, Institut de Biologie Structurale J.P. Ebel (CEA-CNRS-UJF), 41 rue Jules Horowitz, 38027, Grenoble Cédex 1, France

    Anne Volbeda, Lydie Martin, Christine Cavazza, Michaël Matho, Elsa Garcin & Juan C. Fontecilla-Camps

  2. Biochemistry, Swammerdam Institute for Life Sciences, University of Amsterdam, Plantage Muidergracht 12, 1018 TV, Amsterdam, The Netherlands

    Bart W. Faber, Winfried Roseboom & Simon P. J. Albracht

  3. Unité de Bioénergétique et Ingénierie des Protéines, Institut de Biologie Structurale et Microbiologie, CNRS, 31 chemin Joseph Aiguier, Marseille Cédex 20, France

    Marc Rousset

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  1. Anne Volbeda
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  2. Lydie Martin
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  3. Christine Cavazza
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  4. Michaël Matho
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  10. Juan C. Fontecilla-Camps
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Correspondence to Anne Volbeda or Juan C. Fontecilla-Camps.

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An erratum to this article can be found at http://dx.doi.org/10.1007/s00775-005-0663-3

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Volbeda, A., Martin, L., Cavazza, C. et al. Structural differences between the ready and unready oxidized states of [NiFe] hydrogenases. J Biol Inorg Chem 10, 239–249 (2005). https://doi.org/10.1007/s00775-005-0632-x

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