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Dimanganese catalase—spectroscopic parameters from broken-symmetry density functional theory of the superoxidized MnIII/MnIV state

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Abstract

Broken-symmetry density functional theory was used to study the catalytic center of manganese catalase in the superoxidized MnIII/MnIV state. Heisenberg exchange coupling constants, 55Mn and 14N hyperfine coupling constants (hfcs) and nuclear quadrupole splittings, as well as the electronic g tensors were evaluated for different model systems of the active site after complete geometry optimizations in the high-spin and broken-symmetry states. A comparison of the experimental data with the spectroscopic parameters computed for the models with unprotonated and protonated μ-oxo bridges shows best agreement between theory and experiment for a Mn2(μ-O)2(μ-OAc) core. The calculated Mn–Mn distances and 55Mn hfcs clearly support a dimanganese cluster with unprotonated μ-oxo bridges in the superoxidized state. Furthermore, it is shown that an interchange of the MnIII and MnIV oxidation states in this trapped valence system leads to specific changes in the molecular and electronic structure of the manganese clusters.

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References

  1. Dismukes GC (1996) Chem Rev 96:2909–2926

    Google Scholar 

  2. Wu AJ, Penner-Hahn JE, Pecoraro VL (2004) Chem Rev 104:903–938

    Google Scholar 

  3. Kono Y, Fridovich I (1983) J Biol Chem 258:6015–6019

    Google Scholar 

  4. Barynin VV, Grebenko AI (1986) Dokl Akad Nauk SSSR 286:461–464

    Google Scholar 

  5. Whittaker MM, Barynin VV, Antonyuk SV, Whittaker J (1999) Biochemistry 38:9126–9136

    Google Scholar 

  6. Barynin VV, Whittaker MM, Antonyuk SV, Lamzin VS, Harrison PM, Artymiuk PJ, Whittaker JW (2001) Structure 9:725–738

    Google Scholar 

  7. Antonyuk SV, Melik-Adamyan VR, Popov AN, Lamzin VS, Hempstead PD, Harrison PM, Artymyuk PJ, Barynin VV (2000) Cryst Rep 45:105–116

    Google Scholar 

  8. Waldo GS, Fronko RM, Penner-Hahn JE (1991) Biochemistry 30:10486–10490

    Google Scholar 

  9. Waldo GS, Penner-Hahn JE (1995) Biochemistry 34:1507–1512

    Google Scholar 

  10. Pessiki PJ, Dismukes GC (1994) J Am Chem Soc 116:898–903

    Google Scholar 

  11. Michaud-Soret I, Jacquamet L, Debaecker-Petit N, Le Pape L, Barynin VV, Latour JM (1998) Inorg Chem 37:3874–3876

    Google Scholar 

  12. Kono Y, Fridovich I (1983) J Biol Chem 258:3646–3648

    Google Scholar 

  13. Waldo GS, Yu S, Penner-Hahn JE (1992) J Am Chem Soc 114:5869–5870

    Google Scholar 

  14. Schäfer KO, Bittl R, Lendzian F, Barynin V, Weyhermüller T, Wieghardt K, Lubitz W (2003) J Phys Chem B 107:1242–1250

    Google Scholar 

  15. Fronko RM, Penner-Hahn JE, Bender CJ (1988) J Am Chem Soc 110:7554–7555

    Google Scholar 

  16. Grush MM, Chen J, Stemmler TL, George SJ, Ralston CY, Stibrany RT, Gelasco A, Christou G, Gorun SM, Penner-Hahn JE, Cramer SP (1996) J Am Chem Soc 118:65–69

    Google Scholar 

  17. Stemmler TL, Sossong TM, Goldstein JI, Ash DE, Elgren TE, Krutz DM, Penner-Hahn JE (1997) Biochemistry 36:9847–9858

    Google Scholar 

  18. Stemmler TL, Sturgeon BE, Randall DW, Britt RD, Penner-Hahn JE (1997) J Am Chem Soc 119:9215–9225

    Google Scholar 

  19. Brunold TC, Gamelin DR, Stemmler TL, Mandal SK, Armstrong WH, Penner-Hahn JE, Solomon EI (1998) J Am Chem Soc 120:8724–8738

    Google Scholar 

  20. Hureau C, Blondin G, Cesario M, Un S (2003) J Am Chem Soc 125:11637–11645

    Google Scholar 

  21. Yano J, Sauer K, Girerd JJ, Yachandra VK (2004) J Am Chem Soc 126:7486–7495

    Google Scholar 

  22. DeGrado WF, Di Costanzo L, Geremia S, Lombardi A, Pavone V, Randaccio L (2003) Angew Chem Int Ed 42:417–420

    Google Scholar 

  23. Triller MU, Hsieh WY, Pecoraro VL, Rompel A, Krebs B (2002) Inorg Chem 41:5544–5554

    Google Scholar 

  24. Zhang JJ, Luo QH, Duan CY, Wang ZL, Mei YH (2001) J Inorg Biochem 86:573–579

    Google Scholar 

  25. Neese F (2003) Curr Opin Chem Biol 7:125–135

    Google Scholar 

  26. Lovell T, Himo F, Han WG, Noodleman L (2003) Coord Chem Rev 238:211–232

    Google Scholar 

  27. Noodleman L, Lovell T, Han WG, Li J, Himo F (2004) Chem Rev 104:459–508

    Google Scholar 

  28. Koch W, Holthausen MC (2000) A chemist’s guide to density functional theory. Wiley-VCH, Weinheim

    Google Scholar 

  29. Hohenberg P, Kohn W (1964) Phys Rev B 136:864

    Google Scholar 

  30. Kohn W, Sham LJ (1965) Phys Rev 140:1133

    Google Scholar 

  31. Bencini A, Gatteschi D (1990) EPR of exchange coupled systems. Springer-Verlag, Berlin

    Google Scholar 

  32. Noodleman L, Davidson ER (1986) Chem Phys 109:131–143

    Google Scholar 

  33. Noodleman L (1981) J Chem Phys 74:5737–5743

    Google Scholar 

  34. Illas F, Moreira IDR, de Graaf C, Barone V (2000) Theor Chem Acc 104:265–272

    Google Scholar 

  35. Zheng M, Khangulov SV, Dismukes GC, Barynin VV (1994) Inorg Chem 33:382–387

    Google Scholar 

  36. Delfs CD, Stranger R (2001) Inorg Chem 40:3061–3076

    Google Scholar 

  37. Barone V, Bencini A, Gatteschi D, Totti F (2002) Chem Eur J 8:5019–5027

    Google Scholar 

  38. Petrie S, Mukhopadhyay S, Armstrong WH, Stranger R (2004) Phys Chem 6:4871–4877

    Google Scholar 

  39. Delfs CD, Stranger R (2000) Inorg Chem 39:491–495

    Google Scholar 

  40. McGrady JE, Stranger R (1997) J Am Chem Soc 119:8512–8522

    Google Scholar 

  41. Zhao XG, Richardson WH, Chen JL, Li J, Noodleman L, Tsai HL, Hendrickson DN (1997) Inorg Chem 36:1198–1217

    Google Scholar 

  42. Sinnecker S, Neese F, Noodleman L, Lubitz W (2004) J Am Chem Soc 126:2613–2622

    Google Scholar 

  43. Siegbahn PEM (2002) Curr Opin Chem Biol 6:227–235

    Google Scholar 

  44. Siegbahn PEM (2001) J Comput Chem 22:1634–1645

    Google Scholar 

  45. Siegbahn PEM (2001) Theor Chem Acc 105:197–206

    Google Scholar 

  46. Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, Weissig H, Shindyalov IN, Bourne PE (2000) Nucleic Acids Res 28:235–242

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  48. Perdew JP (1986) Phys Rev B 34:7406

    Google Scholar 

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

    Article  Google Scholar 

  50. Schäfer A, Huber C, Ahlrichs R (1994) J Chem Phys 100:5829–5835

    Article  Google Scholar 

  51. Schäfer A, Horn H, Ahlrichs R (1992) J Chem Phys 97:2571–2577

    Article  Google Scholar 

  52. Eichkorn K, Weigend F, Treutler O, Ahlrichs R (1997) Theor Chem Acc 97:119–124

    Google Scholar 

  53. Eichkorn K, Treutler O, Ohm H, Häser M, Ahlrichs R (1995) Chem Phys Lett 242:652–660

    Google Scholar 

  54. Eichkorn K, Treutler O, Ohm H, Häser M, Ahlrichs R (1995) Chem Phys Lett 240:283–289

    Article  CAS  Google Scholar 

  55. Stephens PJ, Devlin FJ, Chabalowski CF, Frisch MJ (1994) J Phys Chem 98:11623–11627

    CAS  Google Scholar 

  56. Becke AD (1993) J Chem Phys 98:5648–5652

    Article  CAS  Google Scholar 

  57. Lee CT, Yang WT, Parr RG (1988) Phys Rev B 37:785–789

    Article  CAS  Google Scholar 

  58. Neese F (2002) Inorg Chim Acta 337:181–192

    Google Scholar 

  59. Barone V (1996) In: Chong DP (ed) Recent advances in density functional methods. World Scientific Publication Company, Singapore, p 287

  60. Mouesca JM, Chen JL, Noodleman L, Bashford D, Case DA (1994) J Am Chem Soc 116:11898–11914

    Google Scholar 

  61. Neese F (2004) J Phys Chem Solids 65:781–785

    Google Scholar 

  62. Neese F (2003) J Chem Phys 118:3939–3948

    Google Scholar 

  63. Weltner W Jr (1983) Magnetic atoms and molecules. Dover Publications Inc., New York

    Google Scholar 

  64. Tokman M, Sundholm D, Pyykko P, Olsen J (1997) Chem Phys Lett 265:60–64

    Google Scholar 

  65. Neese F (2001) J Chem Phys 115:11080–11096

    Google Scholar 

  66. Koseki S, Schmidt MW, Gordon MS (1998) J Phys Chem A 102:10430–10435

    Google Scholar 

  67. Koseki S, Gordon MS, Schmidt MW, Matsunaga N (1995) J Phys Chem 99:12764–12772

    Google Scholar 

  68. Koseki S, Schmidt MW, Gordon MS (1992) J Phys Chem 96:10768–10772

    Google Scholar 

  69. Neese F (2004) ORCA—an ab initio, density functional and semiempirical program package, Version 2.3. Max-Planck-Institut für Bioanorganische Chemie, Mülheim an der Ruhr

    Google Scholar 

  70. Mukhopadhyay S, Mandal SK, Bhaduri S, Armstrong WH (2004) Chem Rev 104:3981–4026

    Google Scholar 

  71. Baldwin MJ, Stemmler TL, Riggs-Gelasco PJ, Kirk ML, Penner-Hahn JE, Pecoraro VL (1994) J Am Chem Soc 116:11349–11356

    Google Scholar 

  72. Brunold TC, Gamelin DR, Solomon EI (2000) J Am Chem Soc 122:8511–8523

    Article  CAS  Google Scholar 

  73. Schäfer KO, Bittl R, Zweygart W, Lendzian F, Haselhorst G, Weyhermüller T, Wieghardt K, Lubitz W (1998) J Am Chem Soc 120:13104–13120

    Google Scholar 

  74. Wieghardt K, Bossek U, Zsolnai L, Huttner G, Blondin G, Girerd JJ, Babonneau F (1987) J Chem Soc Chem Commun 651–653

  75. Schäfer KO (2002) Exchange coupled manganese complexes: model systems for the active centres of redoxproteins investigated with EPR techniques. Dissertation, Technische Universität Berlin, Germany

    Google Scholar 

  76. Randall DW, Sturgeon BE, Ball JA, Lorigan GA, Chan MK, Klein MP, Armstrong WH, Britt RD (1995) J Am Chem Soc 117:11780–11789

    Google Scholar 

  77. Haddy A, Waldo GS, Sands RH, Penner-Hahn JE (1994) Inorg Chem 33:2677–2682

    Google Scholar 

  78. Dikanov SA, Tsvetkov ID, Khangulov SV, Goldfeld MG (1988) Dokl Akad Nauk SSSR 302:1255–1257

    Google Scholar 

  79. Ivancich A, Barynin VV, Zimmermann JL (1995) Biochemistry 34:6628–6639

    Google Scholar 

  80. Schmitt EA, Noodleman L, Baerends EJ, Hendrickson DN (1992) J Am Chem Soc 114:6109–6119

    Google Scholar 

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Acknowledgements

The authors are grateful to L. Noodleman for helpful discussions concerning the bs approach. This work was supported by the priority programs SPP 1137 “Molecular magnetism” (F.N.) and SPP 1051 “High-field EPR in biology, chemistry and physics” (W.L.) of the DFG, and by the Max-Planck-Gesellschaft.

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  1. Max-Planck-Institut für Bioanorganische Chemie, Stiftstrasse 34–36, Mülheim an der Ruhr, 45470, Germany

    Sebastian Sinnecker, Frank Neese & Wolfgang Lubitz

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  1. Sebastian Sinnecker
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Correspondence to Wolfgang Lubitz.

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Sinnecker, S., Neese, F. & Lubitz, W. Dimanganese catalase—spectroscopic parameters from broken-symmetry density functional theory of the superoxidized MnIII/MnIV state. J Biol Inorg Chem 10, 231–238 (2005). https://doi.org/10.1007/s00775-005-0633-9

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