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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

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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.

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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

References

  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 1–20

    Google Scholar 

  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 308:1909–1911

    Article  PubMed  CAS  Google Scholar 

  3. Jang BC, Paik JH, Kim SP, Shin DH, Song DK, Park JG, Suh MH, Park JW, Suh SI (2005) Cell Signal 17:625–633

    Article  PubMed  CAS  Google Scholar 

  4. Nicholls P, Fita I, Loewen PC (2001) Adv Inorg Biochem 51:51–106

    CAS  Google Scholar 

  5. Lardinois OM, Mestdagh MM, Rouxhet PG (1996) Biochim Biophys Acta 1295:222–238

    PubMed  Google Scholar 

  6. Lardinois OM (1995) Free Radical Res 22:251–274

    CAS  Google Scholar 

  7. Kirkman HN, Rolfo M, Ferraris AM, Gaetani GF (1999) J Biol Chem 274:13908–13914

    Article  PubMed  CAS  Google Scholar 

  8. Andreoletti P, Gambarelli S, Sainz G, Stojanoff V, White C, Desfonds G, Gagnon J, Gaillard J, Jouve HM (2001) Biochemistry 40:13734–13743

    Article  PubMed  CAS  Google Scholar 

  9. Jones P (2001) J Biol Chem 276:13791–13796

    PubMed  CAS  Google Scholar 

  10. Conradie J, Swarts JC, Ghosh A (2004) J Phys Chem B 108:452–456

    Article  CAS  Google Scholar 

  11. Conradie J, Wasbotten I, Ghosh A (2006) J Inorg Biochem 100:502–506

    Article  PubMed  CAS  Google Scholar 

  12. Rovira C, Fita I (2003) J Phys Chem B 107:5300–5305

    Article  CAS  Google Scholar 

  13. Rovira C (2005) ChemPhysChem 6:1820–1826

    Article  PubMed  CAS  Google Scholar 

  14. Green MT, Dawson JH, Gray HB (2004) Science 304:1653–1656

    Article  PubMed  CAS  Google Scholar 

  15. Hersleth HP, Ryde U, Rydberg P, Gorbitz CH, Andersson KK (2006) J Inorg Biochem 100:460–476

    Article  PubMed  CAS  Google Scholar 

  16. Rydberg P, Sigfridsson E, Ryde U (2004) J Biol Inorg Chem 9:203–223

    Article  PubMed  CAS  Google Scholar 

  17. Silaghi-Dumitrescu R (2004) J Biol Inorg Chem 9:471–476

    Article  PubMed  CAS  Google Scholar 

  18. Green MT (2006) J Am Chem Soc 128:1902–1906

    Article  PubMed  CAS  Google Scholar 

  19. Behan RK, Green MT (2006) J Inorg Biochem 100:448–459

    Article  PubMed  CAS  Google Scholar 

  20. Terner J, Palaniappan V, Gold A, Weiss R, Fitzgerald MM, Sullivan AM, Hosten CM (2006) J Inorg Biochem 100:480–501

    Article  PubMed  CAS  Google Scholar 

  21. Switala J, Loewen PC (2002) Arch Biochem Biophys 401:145–154

    Article  PubMed  CAS  Google Scholar 

  22. Jouve HM, Beaumont F, Léger I, Foray J, Pelmont J (1989) Biochem Cell Biol 67:271–277

    CAS  Google Scholar 

  23. Gouet P, Jouve HM, Dideberg O (1995) J Mol Biol 249:933–954

    Article  PubMed  CAS  Google Scholar 

  24. Gouet P, Jouve HM, Williams PA, Andersson I, Andreoletti P, Nussaume L, Hajdu J (1996) Nat Struct Biol 3:951–956

    Article  PubMed  CAS  Google Scholar 

  25. Andreoletti P, Pernoud A, Sainz G, Gouet P, Jouve HM (2003) Acta Crystallogr D Biol Crystallogr 59:2163–2168

    Article  PubMed  CAS  Google Scholar 

  26. Horner O, Oddou J-L, Mouesca J-M, Jouve HM (2006) J Inorg Biochem 100:477–479

    Article  PubMed  CAS  Google Scholar 

  27. Stone KL, Hoffart LM, Behan RK, Krebs C, Green MT (2006) J Am Chem Soc 128:6147–6153

    Article  PubMed  CAS  Google Scholar 

  28. Sauret G, Jouve H, Pelmont J (1979) Can J Microbiol 25:312–320

    Article  PubMed  CAS  Google Scholar 

  29. Jouve H, Sauret G, Laboure AM, Pelmont J (1979) Can J Microbiol 25:302–311

    PubMed  CAS  Google Scholar 

  30. Andreoletti P, Sainz G, Jaquinod M, Gagnon J, Jouve HM (2003) Proteins 50:261–271

    Article  PubMed  CAS  Google Scholar 

  31. Rieske JS, Lipton SH, Baum H, Silman HI (1967) J Biol Chem 242:4888–4896

    PubMed  CAS  Google Scholar 

  32. Ivancich A, Jouve HM, Sartor B, Gaillard J (1997) Biochemistry 36:9356–9364

    Article  PubMed  CAS  Google Scholar 

  33. Jeandey Ch, Horner O, Oddou J-L, Jeandey C (2003) Meas Sci Technol 14:629–632

    Article  Google Scholar 

  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 43:8815–8825

    Article  PubMed  CAS  Google Scholar 

  35. Filipponi A, Di Cicco A (2000) Task Q 4:575–669

    Google Scholar 

  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 58:1972–1982

    Article  PubMed  CAS  Google Scholar 

  37. Filipponi A, Di Cicco A, Natoli CR (1995) Phys Rev B Condens Matter 52:15122–15134

    PubMed  CAS  Google Scholar 

  38. Filipponi A, Di Cicco A (1995) Phys Rev B Condens Matter 52:15135–15149

    PubMed  CAS  Google Scholar 

  39. Borghi E, Solari PL (2005) J Synchrotron Radiat 12:102–110

    Article  PubMed  CAS  Google Scholar 

  40. Borghi E, Solari PL, Beltramini M, Bubacco L, Di Muro P, Salvato B (2002) Biophys J 82:3254–3268

    Article  PubMed  CAS  Google Scholar 

  41. Baerends EJ, Ellis DE, Ros P (1973) Chem Phys 2:41–45

    Article  CAS  Google Scholar 

  42. Baerends EJ, Ros P (1973) Chem Phys 2:52–59

    Article  CAS  Google Scholar 

  43. Baerends EJ, Ros P (1978) Int J Quantum Chem Quantum Chem Symp 12:169–190

    CAS  Google Scholar 

  44. Bickelhaupt FM, Baerends EJ, Ravenek W (1990) Inorg Chem 29:350–354

    Article  CAS  Google Scholar 

  45. TeVelde G, Baerends EJ (1992) J Comput Phys 99:84–98

    Article  CAS  Google Scholar 

  46. Ziegler T (1991) Chem Rev 91:651–667

    Article  CAS  Google Scholar 

  47. Vosko SH, Wilk L, Nusair M (1980) Can J Phys 58:1200

    Article  CAS  Google Scholar 

  48. Painter GS (1981) Phys Rev B 24:4264–4270

    Article  CAS  Google Scholar 

  49. Becke AD (1988) Phys Rev A 38:3098–3100

    Article  PubMed  CAS  Google Scholar 

  50. Perdew JP (1986) Phys Rev B 33:8822–8824

    Article  Google Scholar 

  51. Groves JT, Quinn RQ, Mc Murry TJ, Nakamura M, Lang G, Boso B (1985) J Am Chem Soc 107:354–360

    Article  CAS  Google Scholar 

  52. Zimmermann R, Ritter G, Spiering H, Nagy D (1974) J Phys C 6:439–442

    Google Scholar 

  53. Sitter AJ, Reczek CM, Terner J (1985) J Biol Chem 260:7515–7522

    PubMed  CAS  Google Scholar 

  54. Chuang WJ, Heldt J, Van Wart HE (1989) J Biol Chem 264:14209–14215

    PubMed  CAS  Google Scholar 

  55. Schulz CE, Devaney PW, Winkler H, Debrunner PG, Doan N, Chiang R, Rutter R, Hager LP (1979) FEBS Lett 103:102–105

    Article  PubMed  CAS  Google Scholar 

  56. Schulz CE, Rutter R, Sage JT, Debrunner PG, Hager LP (1984) Biochemistry 23:4743–4754

    Article  PubMed  CAS  Google Scholar 

  57. Oosterhuis WT, Lang G (1973) J Chem Phys 58:4757–4765

    Article  CAS  Google Scholar 

  58. Münck E (2000) In: Que LJr (ed) Physical methods in bioinorganic chemistry—spectroscopy and magnetism. University Science Books, chap 6

  59. Rutter R, Hager LP, Dhonau H, Hendrich M, Valentine M, Debrunner P (1984) Biochemistry 23:6809–6816

    Article  PubMed  CAS  Google Scholar 

  60. Leising RA, Brennan BA, Que L Jr, Fox BG, Münck E (1991) J Am Chem Soc 113:3988–3990

    Article  CAS  Google Scholar 

  61. Rohde JU, In JH, Lim MH, Brennessel WW, Bukowski MR, Stubna A, Munck E, Nam W, Que L Jr (2003) Science 299:1037–1039

    Article  PubMed  CAS  Google Scholar 

  62. Egawa T, Proshlyakov DA, Miki H, Makino R, Ogura T, Kitagawa T, Ishimura Y (2001) J Biol Inorg Chem 6:46–54

    Article  PubMed  CAS  Google Scholar 

  63. Chang CS, Yamazaki I, Sinclair R, Khalid S, Powers L (1993) Biochemistry 32:923–928

    Article  PubMed  CAS  Google Scholar 

  64. Dunford HB (1999) Heme peroxidases. Wiley, New York

  65. Rosa A, Ricciardi G, Baerends EJ, van Gisbergen SJA (2001) J Phys Chem A 105:3311–3327

    Article  CAS  Google Scholar 

  66. Gouterman M (1978) In: Dolphin D (ed) The porphyrins, vol 3. Academic, New York, pp 1–165

  67. Penner-Hahn JE, Eble KS, McMurry TJ, Renner M, Balch AL, Groves JT, Dawson JH, Hodgson KO (1986) J Am Chem Soc 108:7819–7825

    Article  CAS  Google Scholar 

  68. Chance M, Powers L, Kumar C, Chance B (1986) Biochemistry 25:1259–1265

    Article  PubMed  CAS  Google Scholar 

  69. Chance M, Powers L, Poulos T, Chance B (1986) Biochemistry 25:1266–1270

    Article  PubMed  CAS  Google Scholar 

  70. Stern EA (2001) J Synchrotron Radiat 8:49–54

    Article  PubMed  CAS  Google Scholar 

  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 127:12494–12495

    Article  PubMed  CAS  Google Scholar 

  72. Bukowski MR, Koehntop KD, Stubna A, Bominaar EL, Halfen JA, Munck E, Nam W, Que L Jr (2005) Science 310:1000–1002

    Article  PubMed  CAS  Google Scholar 

  73. Lang G, Spartalian K, Yonetani T (1976) Biochim Biophys Acta 451:250–258

    CAS  PubMed  Google Scholar 

  74. Schulz CE, Chiang R, Debrunner PG (1979) J Phys 40:C2 534–C2 536

    Google Scholar 

  75. Hashimoto S, Tatsuno Y, Kitagawa T (1986) Proc Natl Acad Sci USA 83:2417–2421

    Article  PubMed  CAS  Google Scholar 

  76. Ivancich A, Mattioli TA, Un S (1999) J Am Chem Soc 121:5743–5753

    Article  CAS  Google Scholar 

  77. Proshlyakov DA, Ogura T, Shinzawa-Itoh K, Yoshikawa S, Kitagawa T (1996) Biochemistry 35:8580–8586

    Article  PubMed  CAS  Google Scholar 

  78. Jouve HM, Tessier S, Pelmont J (1983) Can J Biochem Cell Biol 61:8–14

    Article  PubMed  CAS  Google Scholar 

Download references

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.

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Author notes

  1. P. L. Solari

    Present address: Synchrotron Soleil, Saint Aubin, BP 48, 91192, Gif-sur-Yvette Cedex, France

Authors and Affiliations

  1. Laboratoire de Physicochimie des Métaux en Biologie, UMR CEA/CNRS/Université Joseph Fourier 5155, CEA/Grenoble, 38054, Grenoble Cedex 9, France

    O. Horner & J-L. Oddou

  2. Département de Recherche Fondamentale sur la Matière Condensée, Laboratoire de Résonances Magnétiques, Service de Chimie Inorganique et Biologique, UMR CEA/Université Joseph Fourier E3, CEA/Grenoble, 38054, Grenoble Cedex 9, France

    J-M. Mouesca & M. Orio

  3. European Synchrotron Radiation Facility, 6 rue Jules Horowitz, 38000, Grenoble, France

    P. L. Solari

  4. Département de Recherches sur l’Etat Condensé, Service de Physique de l’Etat Condensé, les Atomes et les Molécules, CEA/Saclay, 91191, Gif-sur-Yvette Cedex, France

    P. Bonville

  5. Institut de Biologie Structurale Jean-Pierre Ebel, UMR CEA/CNRS/Université Joseph Fourier 5075, 41 rue Jules Horowitz, 38027, Grenoble Cedex 1, France

    H. M. Jouve

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  1. O. Horner
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  2. J-M. Mouesca
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Correspondence to H. M. Jouve.

Electronic supplementary material

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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)

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Horner, O., Mouesca, JM., Solari, P.L. et al. 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. J Biol Inorg Chem 12, 509–525 (2007). https://doi.org/10.1007/s00775-006-0203-9

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