Crystallographic studies of [NiFe]-hydrogenase mutants: towards consensus structures for the elusive unready oxidized states

  • Anne Volbeda
  • Lydie Martin
  • Elodie Barbier
  • Oscar Gutiérrez-Sanz
  • Antonio L. De Lacey
  • Pierre-Pol Liebgott
  • Sébastien Dementin
  • Marc Rousset
  • Juan C. Fontecilla-Camps
Original Paper

Abstract

Catalytically inactive oxidized O2-sensitive [NiFe]-hydrogenases are characterized by a mixture of the paramagnetic Ni-A and Ni-B states. Upon O2 exposure, enzymes in a partially reduced state preferentially form the unready Ni-A state. Because partial O2 reduction should generate a peroxide intermediate, this species was previously assigned to the elongated Ni–Fe bridging electron density observed for preparations of [NiFe]-hydrogenases known to contain the Ni-A state. However, this proposition has been challenged based on the stability of this state to UV light exposure and the possibility of generating it anaerobically under either chemical or electrochemical oxidizing conditions. Consequently, we have considered alternative structures for the Ni-A species including oxidation of thiolate ligands to either sulfenate or sulfenic acid. Here, we report both new and revised [NiFe]-hydrogenases structures and conclude, taking into account corresponding characterizations by Fourier transform infrared spectroscopy (FTIR), that the Ni-A species contains oxidized cysteine and bridging hydroxide ligands instead of the peroxide ligand we proposed earlier. Our analysis was rendered difficult by the typical formation of mixtures of unready oxidized states that, furthermore, can be reduced by X-ray induced photoelectrons. The present study could be carried out thanks to the use of Desulfovibrio fructosovorans [NiFe]-hydrogenase mutants with special properties. In addition to the Ni-A state, crystallographic results are also reported for two diamagnetic unready states, allowing the proposal of a revised oxidized inactive Ni-SU model and a new structure characterized by a persulfide ion that is assigned to an Ni-‘Sox’ species.

Keywords

Ni–Fe active site Oxygen-sensitivity Ni-A state Ni-SU state Ni-‘Sox’ state 

Abbreviations

Av

Allochromatium vinosum

Df

Desulfovibrio fructosovorans

DvH

Desulfovibrio vulgaris Hildenborough

DvMF

Desulfovibrio vulgaris Miyazaki F

MSR

Methionine sulfoxide reductase

WT

Wild type

Supplementary material

775_2014_1203_MOESM1_ESM.pdf (3.7 mb)
Supplementary material 1 (PDF 3741 kb)

References

  1. 1.
    Vignais PM, Billoud B (2007) Chem Rev 107:4206–4272. doi:10.1021/cr050196r PubMedCrossRefGoogle Scholar
  2. 2.
    Fritsch J, Scheerer P, Frielingsdorf S, Kroschinsky S, Friedrich B, Lenz O, Spahn CMT (2011) Nature 479:249–252. doi:10.1038/nature10505 PubMedCrossRefGoogle Scholar
  3. 3.
    Shomura Y, Yoon KS, Nishihara H, Higuchi Y (2011) Nature 479:253–256. doi:10.1038/nature10504 PubMedCrossRefGoogle Scholar
  4. 4.
    Volbeda A, Amara P, Darnault C, Mouesca JM, Parkin A, Roessler MM, Armstrong FA, Fontecilla-Camps JC (2012) Proc Natl Acad Sci USA 109:5305–5310. doi:10.1073/pnas.1119806109 PubMedCrossRefPubMedCentralGoogle Scholar
  5. 5.
    Evans RM, Parkin A, Roessler MM, Murphy BJ, Adamson H, Lukey MJ, Sargent F, Volbeda A, Fontecilla-Camps JC, Armstrong FA (2013) J Am Chem Soc 135:2694–2707. doi:10.1021/ja311055d PubMedCrossRefGoogle Scholar
  6. 6.
    Mouesca J-M, Fontecilla-Camps JC, Amara P (2013) Angew Chem Int Ed Engl 52:2002–2006. doi:10.1073/pnas.1302304110 PubMedCrossRefGoogle Scholar
  7. 7.
    Lauterbach L, Lenz O (2013) J Am Chem Soc 135:17897–17905. doi:10.1021/ja408420d PubMedCrossRefGoogle Scholar
  8. 8.
    Volbeda A, Amara P, Iannello M, DeLacey AL, Cavazza C, Fontecilla-Camps JC (2013) Chem Comm 49:7061–7063. doi:10.1039/c3cc43619e PubMedCrossRefGoogle Scholar
  9. 9.
    Fontecilla-Camps JC, Volbeda A, Cavazza C, Nicolet Y (2007) Chem Rev 107:4273–4303. doi:10.1021/cr050195z PubMedCrossRefGoogle Scholar
  10. 10.
    Volbeda A, Martin L, Cavazza C, Matho M, Faber BW, Roseboom W, Albracht SPJ, Garcin E, Rousset M, Fontecilla-Camps JC (2005) J Biol Inorg Chem 10:239–249. doi:10.1007/s00775-005-0632-x PubMedCrossRefGoogle Scholar
  11. 11.
    Fernandez VM, Hatchikian EC, Cammack R (1985) Biochim Biophys Acta 832:69–79. doi:10.1016/0167-4838(85)90175-X CrossRefGoogle Scholar
  12. 12.
    Van Gastel M, Stein M, Brecht M, Schröder O, Lendzian F, Bittl R, Ogata H, Higuchi Y, Lubitz W (2006) J Biol Inorg Chem 11:41–51. doi:10.1007/s00775-005-0048-7 PubMedCrossRefGoogle Scholar
  13. 13.
    Lamle SE, Albracht SPJ, Armstrong FA (2004) J Am Chem Soc 126:14899–14909. doi:10.1021/ja047939v PubMedCrossRefGoogle Scholar
  14. 14.
    Van der Zwaan JW, Coremans JM, Bouwens EC, Albracht SPJ (1990) Biochim Biophys Acta 1041:101–110. doi:10.1016/0167-4838(90)90051-G PubMedCrossRefGoogle Scholar
  15. 15.
    Carepo M, Tierney DL, Brondino CD, Yang TC, Pamplona A, Telser J, Moura I, Moura JJG, Hoffman BM (2002) J Am Chem Soc 124:281–286. doi:10.1021/ja010204v PubMedCrossRefGoogle Scholar
  16. 16.
    Ogata H, Hirota S, Nakahara A, Komori H, Shibata N, Kato T, Kano K, Higuchi Y (2005) Structure 13:1635–1642. doi:10.1016/j.str.2005.07.018 PubMedCrossRefGoogle Scholar
  17. 17.
    Söderhjelm P, Ryde U (2006) J Mol Struct (THEOCHEM) 770:199–219. doi:10.1016/j.theochem.2006.06.008 CrossRefGoogle Scholar
  18. 18.
    Ogata H, Kellers P, Lubitz W (2010) J Mol Biol 420:428–444. doi:10.1016/j.jmb.2010.07.041 CrossRefGoogle Scholar
  19. 19.
    AbouHamdan A, Burlat B, Gutiérrez-Sanz O, Liebgott P-P, Baffert C, De Lacey AL, Rousset M, Guigliarelli B, Léger C, Dementin S (2013) Nat Chem Biol 9:15–17. doi:10.1038/nchembio.1110 CrossRefGoogle Scholar
  20. 20.
    De Lacey AL, Hatchikian EC, Volbeda A, Frey M, Fontecilla-Camps JC, Fernandez VM (1997) J Am Chem Soc 119:7181–7189. doi:10.1021/ja963802w CrossRefGoogle Scholar
  21. 21.
    Ravelli RBG, Garman EF (2006) Curr Opin Struct Biol 16:624–629. doi:10.1016/j.sbi.2006.08.001 PubMedCrossRefGoogle Scholar
  22. 22.
    Bleijlevens B, Van Broekhuizen FA, De Lacey AL, Roseboom W, Fernandez VM, Albracht SPJ (2004) J Biol Inorg Chem 9:743–752. doi:10.1007/s00775-004-0570-z PubMedCrossRefGoogle Scholar
  23. 23.
    Vincent KA, Belsey NA, Lubitz W, Armstrong FA (2006) J Am Chem Soc 128:7448–7449. doi:10.1021/ja061732f PubMedCrossRefGoogle Scholar
  24. 24.
    De Lacey AL, Fernández VM, Rousset M, Cavazza C, Hatchikian EC (2003) J Biol Inorg Chem 8:129–134. doi:10.1007/s00775-002-0397-4 CrossRefGoogle Scholar
  25. 25.
    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. doi:10.1073/pnas.95.20.11625 PubMedCrossRefPubMedCentralGoogle Scholar
  26. 26.
    Hatchikian CE, Traore AS, Fernandez VM, Cammack R (1990) Eur J Biochem 187:635–643. doi:10.1111/j.1432-1033.1990.tb15347.x PubMedCrossRefGoogle Scholar
  27. 27.
    Dementin S, Burlat B, De Lacey AL, Pardo A, Adryanczyk-Perrier G, Guigliarelli B, Fernandez VM, Rousset M (2004) J Biol Chem 279:10508–10513. doi:10.1074/jbc.M312716200 PubMedCrossRefGoogle Scholar
  28. 28.
    Leroux F, Dementin S, Burlat B, Cournac L, Volbeda A, Champ S, Martin L, Guigliarelli B, Bertrand P, Fontecilla-Camps JC, Rousset M, Léger C (2008) Proc Natl Acad Sci USA 105:11188–11193. doi:10.1073/pnas.0803689105 PubMedCrossRefPubMedCentralGoogle Scholar
  29. 29.
    Liebgott P-P, Leroux F, Burlat B, Dementin S, Baffert C, Lautier T, Fourmond V, Ceccaldi P, Cavazza C, Meynial-Salles I, Soucaille P, Fontecilla-Camps JC, Guigliarelli B, Bertrand P, Rousset M, Léger C (2010) Nat Chem Biol 6:63–70. doi:10.1038/nchembio.276 PubMedCrossRefGoogle Scholar
  30. 30.
    Vernède X, Fontecilla-Camps JC (1999) J Appl Cryst 32:505–509. doi:10.1107/S0021889899002678 CrossRefGoogle Scholar
  31. 31.
    Kabsch W (2010) Acta Crystallogr Sect D Biol Crystallogr 66:125–132. doi:10.1107/S0907444909047337 CrossRefGoogle Scholar
  32. 32.
    Karplus PA, Diederichs K (2012) Science 336:1030–1033. doi:10.1126/science.1218231 PubMedCrossRefPubMedCentralGoogle Scholar
  33. 33.
    Winn MD, Ballard CC, Cowtan KD, Dodson EJ, Emsley P, Evans PR, Keegan RM, Krissinel EB, Leslie AG, McCoy A, McNicholas SJ, Murshudov GN, Pannu NS, Potterton EA, Powell HR, Read RJ, Vagin A, Wilson KS (2011) Acta Crystallogr Sect D Biol Crystallogr 67:235–242. doi:10.1107/S0907444910045749 CrossRefGoogle Scholar
  34. 34.
    McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ (2007) J Appl Cryst 40:658–674. doi:10.1107/S0021889807021206 CrossRefGoogle Scholar
  35. 35.
    Murshudov GN, Skubák P, Lebedev AA, Pannu NS, Steiner RA, Nicholls RA, Winn MD, Long F, Vagin AA (2011) Acta Crystallogr Sect D Biol Crystallogr 67:355–367. doi:10.1107/S0907444911001314 CrossRefGoogle Scholar
  36. 36.
    Emsley P, Lohkamp B, Scott WG, Cowtan K (2010) Acta Crystallogr Sect D Biol Crystallogr 66:486–501. doi:10.1107/S0907444910007493 CrossRefGoogle Scholar
  37. 37.
    De Lacey AL, Fernández VM, Rousset M, Cammack R (2007) Chem Rev 107:4304–4330. doi:10.1021/cr0501947 PubMedCrossRefGoogle Scholar
  38. 38.
    Van Gastel M (2010) Appl Magn Reson 37:207–218. doi:10.1007/s00723-009-0044-0 CrossRefGoogle Scholar
  39. 39.
    Wood PM (1988) Biochem J 253:287–289PubMedPubMedCentralGoogle Scholar
  40. 40.
    Volbeda A, Montet Y, Vernède X, Hatchikian EC, Fontecilla-Camps JC (2002) Int J Hydrogen Energy 27:1449–1461. doi:10.1016/S0360-3199(02)00072-1 CrossRefGoogle Scholar
  41. 41.
    Kumar M, Colpas GJ, Day RO, Maroney MJ (1989) J Am Chem Soc 111:8323–8325. doi:10.1021/ja00203a068 CrossRefGoogle Scholar
  42. 42.
    Farmer PJ, Verpeaux J-N, Amatore C, Darensbourg MY, Musie G (1994) J Am Chem Soc 116:9355–9356. doi:10.1021/ja00099a073 CrossRefGoogle Scholar
  43. 43.
    Marques MC, Coelho R, Pereira IAC, Matias PM (2013) Int J Hydrogen Energy 38:8664–8682. doi:10.1016/j.ijhydene.2013.04.132 CrossRefGoogle Scholar
  44. 44.
    Pandelia M-E, Ogata H, Lubitz W (2010) Chem Phys Chem 11:1127–1140. doi:10.1002/cphc.200900950 PubMedGoogle Scholar
  45. 45.
    Claiborne A, Yeh JI, Mallet TC, Luba J, Crane EJ, Charrier V, Parsonage D (1999) Biochemistry 38:15407–15416. doi:10.1021/bi992025k PubMedCrossRefGoogle Scholar
  46. 46.
    Boschi-Muller S, Gand A, Branlant G (2008) Arch Biochem Biophys 474:266–273. doi:10.1016/j.abb.2008.02.007 PubMedCrossRefGoogle Scholar
  47. 47.
    Tarrago L, Laugier E, Zaffagnini M, Marchand CH, Le Maréchal P, Lemaire SD, Rey P (2010) J Biol Chem 285:14964–14972. doi:10.1074/jbc.M110.108373 PubMedCrossRefPubMedCentralGoogle Scholar
  48. 48.
    Nagahara N, Katayama A (2005) J Biol Chem 280:34569–34576. doi:10.1074/jbc.M505643200 PubMedCrossRefGoogle Scholar
  49. 49.
    Liebgott P-P, de Lacey AL, Burlat B, Cournac L, Richaud P, Brugna M, Fernandez VM, Guigliarelli B, Rousset M, Léger C, Dementin S (2011) J Am Chem Soc 133:986–997. doi:10.1021/ja108787s PubMedCrossRefGoogle Scholar
  50. 50.
    Marques MC, Coelho R, De Lacey AL, Pereira IAC, Matias PM (2010) J Mol Biol 396:893–907. doi:10.1016/j.jmb.2009.12.013 PubMedCrossRefGoogle Scholar
  51. 51.
    Brunger AT (2010) Nature 355:473–475. doi:10.1038/355472a0 Google Scholar

Copyright information

© SBIC 2014

Authors and Affiliations

  • Anne Volbeda
    • 1
    • 2
    • 3
  • Lydie Martin
    • 1
    • 2
    • 3
  • Elodie Barbier
    • 1
    • 2
    • 3
    • 6
  • Oscar Gutiérrez-Sanz
    • 4
  • Antonio L. De Lacey
    • 4
  • Pierre-Pol Liebgott
    • 5
    • 7
  • Sébastien Dementin
    • 5
  • Marc Rousset
    • 5
    • 8
  • Juan C. Fontecilla-Camps
    • 1
    • 2
    • 3
  1. 1.University Grenoble Alpes, IBSGrenobleFrance
  2. 2.CEA, IBSGrenobleFrance
  3. 3.CNRS, IBSGrenobleFrance
  4. 4.Instituto de Catálisis y Petroleoquímica, CSICMadridSpain
  5. 5.Aix-Marseille Université, CNRS, IMMMarseilleFrance
  6. 6.CEA, MINATECGrenobleFrance
  7. 7.Aix-Marseille Université, CNRS/INSU, MIOMarseilleFrance
  8. 8.Consulate General of FranceChicagoUSA

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