Spectroscopic description of an unusual protonated ferryl species in the catalase from Proteus mirabilis and density functional theory calculations on related models. Consequences for the ferryl protonation state in catalase, peroxidase and chloroperoxidase

  • O. Horner
  • J-M. Mouesca
  • P. L. Solari
  • M. Orio
  • J-L. Oddou
  • P. Bonville
  • H. M. Jouve
Original Paper

Abstract

The catalase from Proteus mirabilis peroxide-resistant bacteria is one of the most efficient heme-containing catalases. It forms a relatively stable compound II. We were able to prepare samples of compound II from P. mirabilis catalase enriched in 57Fe and to study them by spectroscopic methods. Two different forms of compound II, namely, low-pH compound II (LpH II) and high-pH compound II (HpH II), have been characterized by Mössbauer, extended X-ray absorption fine structure (EXAFS) and UV-vis absorption spectroscopies. The proportions of the two forms are pH-dependent and the pH conversion between HpH II and LpH II is irreversible. Considering (1) the Mössbauer parameters evaluated for four related models by density functional theory methods, (2) the existence of two different Fe–Oferryl bond lengths (1.80 and 1.66 Å) compatible with our EXAFS data and (3) the pH dependence of the α band to β band intensity ratio in the absorption spectra, we attribute the LpH II compound to a protonated ferryl FeIV–OH complex (Fe–O approximately 1.80 Å), whereas the HpH II compound corresponds to the classic ferryl FeIV=O complex (Fe=O approximately 1.66 Å). The large quadrupole splitting value of LpH II (measured 2.29 mm s−1 vs. computed 2.15 mm s−1) compared with that of HpH II (measured 1.47 mm s−1 vs. computed 1.46 mm s−1) reflects the protonation of the ferryl group. The relevancy and involvement of such (FeIV=O/FeIV–OH) species in the reactivity of catalase, peroxidase and chloroperoxidase are discussed.

Keywords

Catalase compound II Protonated ferryl species Mössbauer spectroscopy Density functional theory calculations Extended X-ray absorption fine structure 

Abbreviations

CPO

Chloroperoxidase

DFT

Density functional theory

DW

Debye–Waller

EPR

Electron paramagnetic resonance

EXAFS

Extended X-ray absorption fine structure

HpH II

High-pH Proteus mirabilis catalase compound II

HRP

Horseradish peroxidase

LpH II

Low-pH Proteus mirabilis catalase compound II

MLC

Micrococcus lysodeikticus catalase

MO

Molecular orbital

PMC

Proteus mirabilis catalase

TMP

Tetramesitylporphyrin

Tris

Tris(hydroxymethyl)aminomethane

Notes

Acknowledgements

N. Genand-Riondet (CEA/Saclay) is gratefully acknowledged for performing the high-field Mössbauer spectroscopy experiments and the European Synchrotron Radiation Facility is gratefully acknowledged for provision of synchrotron radiation. Tony Mattioli (CEA/Saclay) is thanked for resonance Raman measurements. We would like to thank Catherine Bougault (IBS, Grenoble) for helpful discussions and Elizabeth Hewat (IBS, Grenoble) for corrections of the English.

Supplementary material

775_2006_203_MOESM1_ESM.doc (688 kb)
Supplementary material: Reference UV-visible spectra of PMC resting state, compound I and compound II (Fig. S1); Mössbauer spectra of as-isolated 57Fe catalase from P. mirabilis at 4.2 K in a magnetic field of 50 mT and 7.0 T applied parallel to the γ-beam (Fig. S2); Mössbauer spectrum of compound I in 57Fe catalase from P. mirabilis at 40 K in a magnetic field of 3T applied parallel to the γ-beam (Fig. S3); Mössbauer spectrum of compound II in 57Fe catalase from P. mirabilis at 150 K in a magnetic field of 7.0 T applied parallel to the γ-beam (Fig. S4);comparison between the visible absorption spectra of compound II samples used for EXAFS and Mössbauer measurements (Fig. S5); experimental EXAFS of PMC compound II from P. mirabilis at pH 8.0 with results of the EXAFS analysis considering two distinct iron–oxo contributions (Fig. S6); projection of the minimization function on the (R–Fe=O, R–Fe–OH) plane, i.e. contour plot (regions enclosed by squares correspond to the 95% confidence interval) (Fig. S7); linear correlation between the computed quadrupole splitting ΔEQ and the computed electronic density at the iron nucleus ρ(Fe), by using all six FeIV=O models of compound II at high pH and four possible FeIV–OH models of compound II at low pH (Figure S8); optimized coordinates for the models 1, 1ter, 2, 2ter, 3, 3bis and 4 (Table S1 a–g); structural parameters and quadrupole splitting in case of the alternative protonation of the axial Tyrosine residue (here without cation) (Table S2); repartition of the iron spin population (%) among the d atomic orbitals for the models 1 to 4. Summation per spin (∑dαβ) and total iron spin populations (∑dα−∑dβ) (Table S3); mononuclear iron biomolecules and complexes used for establishing the linear correlation between experimentally measured isomer shifts at 4.2 K and experimentally measured quadrupole splitting at 4.2 K (Table S4). (DOC 687 kb)

References

  1. 1.
    Hauptmann N, Cadenas E (1997) In: Scandalios JG (eds) Oxidative stress and the molecular biology of antioxidant defenses. Cold Spring Harbor Laboratory Press, New York, pp 1–20Google Scholar
  2. 2.
    Schriner SE, Linford NJ, Martin GM, Treuting P, Ogburn CE, Emond M, Coskun PE, Ladiges W, Wolf N, Van Remmen H, Wallace DC, Rabinovitch PS (2005) Science 308:1909–1911PubMedCrossRefGoogle Scholar
  3. 3.
    Jang BC, Paik JH, Kim SP, Shin DH, Song DK, Park JG, Suh MH, Park JW, Suh SI (2005) Cell Signal 17:625–633PubMedCrossRefGoogle Scholar
  4. 4.
    Nicholls P, Fita I, Loewen PC (2001) Adv Inorg Biochem 51:51–106Google Scholar
  5. 5.
    Lardinois OM, Mestdagh MM, Rouxhet PG (1996) Biochim Biophys Acta 1295:222–238PubMedGoogle Scholar
  6. 6.
    Lardinois OM (1995) Free Radical Res 22:251–274Google Scholar
  7. 7.
    Kirkman HN, Rolfo M, Ferraris AM, Gaetani GF (1999) J Biol Chem 274:13908–13914PubMedCrossRefGoogle Scholar
  8. 8.
    Andreoletti P, Gambarelli S, Sainz G, Stojanoff V, White C, Desfonds G, Gagnon J, Gaillard J, Jouve HM (2001) Biochemistry 40:13734–13743PubMedCrossRefGoogle Scholar
  9. 9.
    Jones P (2001) J Biol Chem 276:13791–13796PubMedGoogle Scholar
  10. 10.
    Conradie J, Swarts JC, Ghosh A (2004) J Phys Chem B 108:452–456CrossRefGoogle Scholar
  11. 11.
    Conradie J, Wasbotten I, Ghosh A (2006) J Inorg Biochem 100:502–506PubMedCrossRefGoogle Scholar
  12. 12.
    Rovira C, Fita I (2003) J Phys Chem B 107:5300–5305CrossRefGoogle Scholar
  13. 13.
    Rovira C (2005) ChemPhysChem 6:1820–1826PubMedCrossRefGoogle Scholar
  14. 14.
    Green MT, Dawson JH, Gray HB (2004) Science 304:1653–1656PubMedCrossRefGoogle Scholar
  15. 15.
    Hersleth HP, Ryde U, Rydberg P, Gorbitz CH, Andersson KK (2006) J Inorg Biochem 100:460–476PubMedCrossRefGoogle Scholar
  16. 16.
    Rydberg P, Sigfridsson E, Ryde U (2004) J Biol Inorg Chem 9:203–223PubMedCrossRefGoogle Scholar
  17. 17.
    Silaghi-Dumitrescu R (2004) J Biol Inorg Chem 9:471–476PubMedCrossRefGoogle Scholar
  18. 18.
    Green MT (2006) J Am Chem Soc 128:1902–1906PubMedCrossRefGoogle Scholar
  19. 19.
    Behan RK, Green MT (2006) J Inorg Biochem 100:448–459PubMedCrossRefGoogle Scholar
  20. 20.
    Terner J, Palaniappan V, Gold A, Weiss R, Fitzgerald MM, Sullivan AM, Hosten CM (2006) J Inorg Biochem 100:480–501PubMedCrossRefGoogle Scholar
  21. 21.
    Switala J, Loewen PC (2002) Arch Biochem Biophys 401:145–154PubMedCrossRefGoogle Scholar
  22. 22.
    Jouve HM, Beaumont F, Léger I, Foray J, Pelmont J (1989) Biochem Cell Biol 67:271–277Google Scholar
  23. 23.
    Gouet P, Jouve HM, Dideberg O (1995) J Mol Biol 249:933–954PubMedCrossRefGoogle Scholar
  24. 24.
    Gouet P, Jouve HM, Williams PA, Andersson I, Andreoletti P, Nussaume L, Hajdu J (1996) Nat Struct Biol 3:951–956PubMedCrossRefGoogle Scholar
  25. 25.
    Andreoletti P, Pernoud A, Sainz G, Gouet P, Jouve HM (2003) Acta Crystallogr D Biol Crystallogr 59:2163–2168PubMedCrossRefGoogle Scholar
  26. 26.
    Horner O, Oddou J-L, Mouesca J-M, Jouve HM (2006) J Inorg Biochem 100:477–479PubMedCrossRefGoogle Scholar
  27. 27.
    Stone KL, Hoffart LM, Behan RK, Krebs C, Green MT (2006) J Am Chem Soc 128:6147–6153PubMedCrossRefGoogle Scholar
  28. 28.
    Sauret G, Jouve H, Pelmont J (1979) Can J Microbiol 25:312–320PubMedCrossRefGoogle Scholar
  29. 29.
    Jouve H, Sauret G, Laboure AM, Pelmont J (1979) Can J Microbiol 25:302–311PubMedGoogle Scholar
  30. 30.
    Andreoletti P, Sainz G, Jaquinod M, Gagnon J, Jouve HM (2003) Proteins 50:261–271PubMedCrossRefGoogle Scholar
  31. 31.
    Rieske JS, Lipton SH, Baum H, Silman HI (1967) J Biol Chem 242:4888–4896PubMedGoogle Scholar
  32. 32.
    Ivancich A, Jouve HM, Sartor B, Gaillard J (1997) Biochemistry 36:9356–9364PubMedCrossRefGoogle Scholar
  33. 33.
    Jeandey Ch, Horner O, Oddou J-L, Jeandey C (2003) Meas Sci Technol 14:629–632CrossRefGoogle Scholar
  34. 34.
    Horner O, Mouesca JM, Oddou JL, Jeandey C, Niviere V, Mattioli TA, Mathe C, Fontecave M, Maldivi P, Bonville P, Halfen JA, Latour JM (2004) Biochemistry 43:8815–8825PubMedCrossRefGoogle Scholar
  35. 35.
    Filipponi A, Di Cicco A (2000) Task Q 4:575–669Google Scholar
  36. 36.
    Murshudov GN, Grebenko AI, Brannigan JA, Antson AA, Barynin VV, Dodson GG, Dauter Z, Wilson KS, Melik-Adamyan WR (2002) Acta Crystallogr D Biol Crystallogr 58:1972–1982PubMedCrossRefGoogle Scholar
  37. 37.
    Filipponi A, Di Cicco A, Natoli CR (1995) Phys Rev B Condens Matter 52:15122–15134PubMedGoogle Scholar
  38. 38.
    Filipponi A, Di Cicco A (1995) Phys Rev B Condens Matter 52:15135–15149PubMedGoogle Scholar
  39. 39.
    Borghi E, Solari PL (2005) J Synchrotron Radiat 12:102–110PubMedCrossRefGoogle Scholar
  40. 40.
    Borghi E, Solari PL, Beltramini M, Bubacco L, Di Muro P, Salvato B (2002) Biophys J 82:3254–3268PubMedCrossRefGoogle Scholar
  41. 41.
    Baerends EJ, Ellis DE, Ros P (1973) Chem Phys 2:41–45CrossRefGoogle Scholar
  42. 42.
    Baerends EJ, Ros P (1973) Chem Phys 2:52–59CrossRefGoogle Scholar
  43. 43.
    Baerends EJ, Ros P (1978) Int J Quantum Chem Quantum Chem Symp 12:169–190Google Scholar
  44. 44.
    Bickelhaupt FM, Baerends EJ, Ravenek W (1990) Inorg Chem 29:350–354CrossRefGoogle Scholar
  45. 45.
    TeVelde G, Baerends EJ (1992) J Comput Phys 99:84–98CrossRefGoogle Scholar
  46. 46.
    Ziegler T (1991) Chem Rev 91:651–667CrossRefGoogle Scholar
  47. 47.
    Vosko SH, Wilk L, Nusair M (1980) Can J Phys 58:1200CrossRefGoogle Scholar
  48. 48.
    Painter GS (1981) Phys Rev B 24:4264–4270CrossRefGoogle Scholar
  49. 49.
    Becke AD (1988) Phys Rev A 38:3098–3100PubMedCrossRefGoogle Scholar
  50. 50.
    Perdew JP (1986) Phys Rev B 33:8822–8824CrossRefGoogle Scholar
  51. 51.
    Groves JT, Quinn RQ, Mc Murry TJ, Nakamura M, Lang G, Boso B (1985) J Am Chem Soc 107:354–360CrossRefGoogle Scholar
  52. 52.
    Zimmermann R, Ritter G, Spiering H, Nagy D (1974) J Phys C 6:439–442Google Scholar
  53. 53.
    Sitter AJ, Reczek CM, Terner J (1985) J Biol Chem 260:7515–7522PubMedGoogle Scholar
  54. 54.
    Chuang WJ, Heldt J, Van Wart HE (1989) J Biol Chem 264:14209–14215PubMedGoogle Scholar
  55. 55.
    Schulz CE, Devaney PW, Winkler H, Debrunner PG, Doan N, Chiang R, Rutter R, Hager LP (1979) FEBS Lett 103:102–105PubMedCrossRefGoogle Scholar
  56. 56.
    Schulz CE, Rutter R, Sage JT, Debrunner PG, Hager LP (1984) Biochemistry 23:4743–4754PubMedCrossRefGoogle Scholar
  57. 57.
    Oosterhuis WT, Lang G (1973) J Chem Phys 58:4757–4765CrossRefGoogle Scholar
  58. 58.
    Münck E (2000) In: Que LJr (ed) Physical methods in bioinorganic chemistry—spectroscopy and magnetism. University Science Books, chap 6Google Scholar
  59. 59.
    Rutter R, Hager LP, Dhonau H, Hendrich M, Valentine M, Debrunner P (1984) Biochemistry 23:6809–6816PubMedCrossRefGoogle Scholar
  60. 60.
    Leising RA, Brennan BA, Que L Jr, Fox BG, Münck E (1991) J Am Chem Soc 113:3988–3990CrossRefGoogle Scholar
  61. 61.
    Rohde JU, In JH, Lim MH, Brennessel WW, Bukowski MR, Stubna A, Munck E, Nam W, Que L Jr (2003) Science 299:1037–1039PubMedCrossRefGoogle Scholar
  62. 62.
    Egawa T, Proshlyakov DA, Miki H, Makino R, Ogura T, Kitagawa T, Ishimura Y (2001) J Biol Inorg Chem 6:46–54PubMedCrossRefGoogle Scholar
  63. 63.
    Chang CS, Yamazaki I, Sinclair R, Khalid S, Powers L (1993) Biochemistry 32:923–928PubMedCrossRefGoogle Scholar
  64. 64.
    Dunford HB (1999) Heme peroxidases. Wiley, New YorkGoogle Scholar
  65. 65.
    Rosa A, Ricciardi G, Baerends EJ, van Gisbergen SJA (2001) J Phys Chem A 105:3311–3327CrossRefGoogle Scholar
  66. 66.
    Gouterman M (1978) In: Dolphin D (ed) The porphyrins, vol 3. Academic, New York, pp 1–165Google Scholar
  67. 67.
    Penner-Hahn JE, Eble KS, McMurry TJ, Renner M, Balch AL, Groves JT, Dawson JH, Hodgson KO (1986) J Am Chem Soc 108:7819–7825CrossRefGoogle Scholar
  68. 68.
    Chance M, Powers L, Kumar C, Chance B (1986) Biochemistry 25:1259–1265PubMedCrossRefGoogle Scholar
  69. 69.
    Chance M, Powers L, Poulos T, Chance B (1986) Biochemistry 25:1266–1270PubMedCrossRefGoogle Scholar
  70. 70.
    Stern EA (2001) J Synchrotron Radiat 8:49–54PubMedCrossRefGoogle Scholar
  71. 71.
    Sastri CV, Park MJ, Ohta T, Jackson TA, Stubna A, Seo MS, Lee J, Kim J, Kitagawa T, Munck E, Que L Jr, Nam W (2005) J Am Chem Soc 127:12494–12495PubMedCrossRefGoogle Scholar
  72. 72.
    Bukowski MR, Koehntop KD, Stubna A, Bominaar EL, Halfen JA, Munck E, Nam W, Que L Jr (2005) Science 310:1000–1002PubMedCrossRefGoogle Scholar
  73. 73.
    Lang G, Spartalian K, Yonetani T (1976) Biochim Biophys Acta 451:250–258PubMedGoogle Scholar
  74. 74.
    Schulz CE, Chiang R, Debrunner PG (1979) J Phys 40:C2 534–C2 536Google Scholar
  75. 75.
    Hashimoto S, Tatsuno Y, Kitagawa T (1986) Proc Natl Acad Sci USA 83:2417–2421PubMedCrossRefGoogle Scholar
  76. 76.
    Ivancich A, Mattioli TA, Un S (1999) J Am Chem Soc 121:5743–5753CrossRefGoogle Scholar
  77. 77.
    Proshlyakov DA, Ogura T, Shinzawa-Itoh K, Yoshikawa S, Kitagawa T (1996) Biochemistry 35:8580–8586PubMedCrossRefGoogle Scholar
  78. 78.
    Jouve HM, Tessier S, Pelmont J (1983) Can J Biochem Cell Biol 61:8–14PubMedCrossRefGoogle Scholar

Copyright information

© SBIC 2007

Authors and Affiliations

  • O. Horner
    • 1
  • J-M. Mouesca
    • 2
  • P. L. Solari
    • 3
    • 6
  • M. Orio
    • 2
  • J-L. Oddou
    • 1
  • P. Bonville
    • 4
  • H. M. Jouve
    • 5
  1. 1.Laboratoire de Physicochimie des Métaux en BiologieUMR CEA/CNRS/Université Joseph Fourier 5155Grenoble Cedex 9France
  2. 2.Département de Recherche Fondamentale sur la Matière Condensée, Laboratoire de Résonances Magnétiques, Service de Chimie Inorganique et BiologiqueUMR CEA/Université Joseph Fourier E3Grenoble Cedex 9France
  3. 3.European Synchrotron Radiation FacilityGrenobleFrance
  4. 4.Département de Recherches sur l’Etat CondenséService de Physique de l’Etat CondenséGif-sur-Yvette CedexFrance
  5. 5.Institut de Biologie Structurale Jean-Pierre EbelUMR CEA/CNRS/Université Joseph Fourier 5075Grenoble Cedex 1France
  6. 6.Synchrotron SoleilGif-sur-Yvette CedexFrance

Personalised recommendations