Theoretical investigation of Q A −· -ligand interactions in bacterial reaction centers ofRhodobacter sphaeroides

  • J. Fritscher
  • T. F. Prisner
  • F. MacMillan


Density functional theory was used to calculate magnetic resonance parameters for the primary stable electron acceptor anion radical (Q A −· ) in its binding site in the bacterial reaction center (bRC) ofRhodobacter sphaeroides. The models used for the calculations of the Q A −· binding pocket included all short-range interactions of the ubiquinone with the protein surroundings in a gradual manner and thus allowed a decomposition and detailed analysis of the different specific interactions. Comparison of the obtained hyperfine and quadrupole couplings with experimental data demonstrates the feasibility and reliability of calculations on such complex biologically relevant systems. With these results, the interpretation of previously published 3-pulse electron spin echo envelope modulation data could be extended and an assignment of the observed double quantum peak to a specific amino acid is proposed. The computations provide evidence for a slightly altered binding site geometry for the QA ground state as investigated by X-ray crystallography with respect to the Q A t-· anion radical state as accessible via EPR spectroscopy. This new geometry leads to improved fits of the W-band correlated-coupled radical pair spectra of Q A −· -P 865 compared to orientation data from the crystal structure. Finally, a correlation of the14N quadrupole parameters of His219 with the hydrogen bond geometry and a comparison with previous systematic studies on the influence of hydrogen bond geometry on quadrupole coupling parameters (J. Fritscher: Phys. Chem. Chem. Phys. 6, 4950–4956, 2004) is presented.


Rhodobacter Sphaeroides Electron Spin Echo Envelope Modulation Spin Density Distribution Electron Paramagnetic Resonance Parameter Electric Field Gradient Tensor 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. 1.
    Weil J.A., Bolton J.R., Wertz J.E.: Electron Paramagnetic Resonance: Elementary Theory and Practical Applications. New York: Wiley 1994.Google Scholar
  2. 2.
    Schweiger A., Jeschke G.: Principles of Pulse Electron Paramagnetic Resonance. Oxford: Oxford University Press 2001.Google Scholar
  3. 3.
    Parr R.G., Yang W.: Density-Functional Theory of Atoms and Molecules. New York: Oxford University Press 1989.Google Scholar
  4. 4.
    Engels B., Eriksson L.A., Lunell S.: Adv. Quantum Chem.27, 297–369 (1996)CrossRefGoogle Scholar
  5. 5.
    Barone V., in: Recent Advances in Density Functional Methods, Part I (Chong D.P., ed.). Singapore: World Scientific Press 1996.Google Scholar
  6. 6.
    Malkin V.G., Malkina O.L., Eriksson L.A., Salahub D.R., in: Modern Density Functional Theory: A Tool for Chemistry (Seminario J.M., Politzer P., eds.). Amsterdam: Elsevier 1995.Google Scholar
  7. 7.
    Kaupp M., Malkin V.G., Bühl M. (eds.): Calculation of NMR and EPR Parameters. Weinheim: Wiley-VCH 2004.Google Scholar
  8. 8.
    Munzarová M., Kaupp M.: J. Phys. Chem. A103, 9966–9983 (1999)CrossRefGoogle Scholar
  9. 9.
    Neese F.: Curr. Opin. Chem. Biol.7, 125–135 (2003)CrossRefGoogle Scholar
  10. 10.
    Sinnecker S., Neese F., Noodleman L., Lubitz W.: J. Am. Chem. Soc.126, 2613–2622 (2004)CrossRefGoogle Scholar
  11. 11.
    Koster A.M., Calaminici P., Russo N.: Phys. Rev. A53, 3865–3868 (1996)CrossRefADSGoogle Scholar
  12. 12.
    Salzmann R., Kaupp M., McMahon M.T., Oldfield E.: J. Am. Chem. Soc.120, 4771–4783 (1998)CrossRefGoogle Scholar
  13. 13.
    de Luca G., Russo N., Köster A.M., Calaminici P., Jug K.: Mol. Phys.97, 347–354 (1999)CrossRefADSGoogle Scholar
  14. 14.
    Bailey W.C.: Chem. Phys.252, 57–66 (2000)CrossRefADSGoogle Scholar
  15. 15.
    Sicilia E., de Luca G., Chiodo S., Russo N., Calaminici P., Köster A.M., Jug K.: Mol. Phys.99, 1039–1051 (2001)CrossRefADSGoogle Scholar
  16. 16.
    Janowski T., Jaszunski M.: Int. J. Quantum Chem.90, 1083–1090 (2002)CrossRefGoogle Scholar
  17. 17.
    Latosiñska J.N.: Int. J. Quantum Chem.91, 284–296 (2003)CrossRefGoogle Scholar
  18. 18.
    Zhang Y., Gossman W., Oldfield E.: J. Am. Chem. Soc.125, 16387–16396 (2003)CrossRefGoogle Scholar
  19. 19.
    Sinnecker S., Reijerse E., Neese F., Lubitz W.: J. Am. Chem. Soc.126, 3280–3290 (2004)CrossRefGoogle Scholar
  20. 20.
    Stein M., van Lenthe E., Baerends E.J., Lubitz W.: J. Am. Chem. Soc.123, 5839–5840 (2001)CrossRefGoogle Scholar
  21. 21.
    Stein M., Lubitz W.: Phys. Chem. Chem. Phys.3, 2668–2675 (2001)CrossRefGoogle Scholar
  22. 22.
    Wetmore S.D., Smith D.M., Golding B.T., Radom L.: J. Am. Chem. Soc.123, 7963–7972 (2001)CrossRefGoogle Scholar
  23. 23.
    O’Malley P., Collins S.J.: J. Am. Chem. Soc.123, 11042–11046 (2001)CrossRefGoogle Scholar
  24. 24.
    Sinnecker S., Koch W., Lubitz W.: J. Phys. Chem. B106, 5281–5288 (2002)CrossRefGoogle Scholar
  25. 25.
    Jaszewski A.R., Jezierska J.: Chem. Phys. Lett.343, 571–580 (2001)CrossRefADSGoogle Scholar
  26. 26.
    van Gastel M., Coremans J.W.A., Sommerdijk H., van Hemert M.C., Groenen E.J.J. J. Am. Chem. Soc.124, 2035–2041 (2002)CrossRefGoogle Scholar
  27. 27.
    Torrent M., Musaev D.G., Morokuma K., Ke S.-C., Warncke K.J.: J. Phys. Chem. B103, 8618–8627 (1999)CrossRefGoogle Scholar
  28. 28.
    Torrent M., Mansour D., Day E.P., Morokuma K.: J. Phys. Chem. A105, 4546–4557 (2001)CrossRefGoogle Scholar
  29. 29.
    Schiemann O., Fritscher J., Kisseleva N., Sigurdsson S.T., Prisner T.F.: ChemBioChem4, 1057–1065 (2003)CrossRefGoogle Scholar
  30. 30.
    Fritscher J., Artin E., Wnuk S., Bar G., Robblee J.H., Kacprzak S., Kaupp M., Griffin R.G., Bennati M., Stubbe J.: J. Am. Chem. Soc.127, 7729–7738 (2005)CrossRefGoogle Scholar
  31. 31.
    Schöneboom J.C., Neese F., Thiel W.: J. Am. Chem. Soc.127, 5840–5853 (2005)CrossRefGoogle Scholar
  32. 32.
    Kacprzak S., Kaupp M., MacMillan F.: J. Am. Chem. Soc.128, 5659–5671 (2006)CrossRefGoogle Scholar
  33. 33.
    Crofts A.R., Wraight C.A.: Biochim. Biophys. Acta726, 149–185 (1983)Google Scholar
  34. 34.
    Nicholls D.G., Ferguson S.J.: Bioenergetics. London: Academic Press 2002.Google Scholar
  35. 35.
    Lubitz W., Feher G.: Appl. Magn. Reson.17, 1–48 (1999)CrossRefGoogle Scholar
  36. 36.
    Stowell M.H.B., McPhillips T.M., Rees D.C., Soltis S.M., Abresch E., Feher G.: Science276, 812–816 (1997)CrossRefGoogle Scholar
  37. 37.
    Flores M., Isaacson R., Abresch E., Calvo R., Lubitz W., Feher G.: Biophys. J.90, 3356–3362 (2006)CrossRefGoogle Scholar
  38. 38.
    Breton J., Boullais C., Burie J.-R., Nabedryk E., Mioskowski C.: Biochemistry33, 14378–14386 (1994)CrossRefGoogle Scholar
  39. 39.
    Brudler R., de Groot H.J.M., van Liemt W.B.S., Steggerda W.F., Esmeijer R., Gast P., Ho A.J., Lugtenburg J., Gerwert K.: EMBO J.13, 5523–5530 (1994)Google Scholar
  40. 40.
    Breton J., Nabedryk E.: Biochim. Biophys. Acta1275, 84–90 (1996)CrossRefGoogle Scholar
  41. 41.
    Ermler U., Fritzsch G., Buchanan S.K., Michel H.: Structure2, 925–936 (1994)CrossRefGoogle Scholar
  42. 42.
    Fritzsch G., Koepke J., Diem R., Kuglstatter A., Baciou L.: Acta Crystallogr. D58, 1660–1663 (2002)CrossRefGoogle Scholar
  43. 43.
    Bittl R., Zech S.G.: J. Phys. Chem. B101, 1429–1436 (1997)CrossRefGoogle Scholar
  44. 44.
    Prisner T.F., van der Est A., Bittl R., Lubitz W., Stehlik D., Möbius K.: Chem. Phys.194, 361–370 (1995)CrossRefGoogle Scholar
  45. 45.
    Himo F., Babcock G.T., Eriksson L.A.: J. Phys. Chem. A103, 3745–3749 (1999)CrossRefGoogle Scholar
  46. 46.
    Hutter M.C., Hughes J.M., Reimers J.R., Hush N.S.: J. Phys. Chem. B103, 4906–4915 (1999)CrossRefGoogle Scholar
  47. 47.
    O’Malley P.: Chem. Phys. Lett.285, 99–104 (1998)CrossRefADSGoogle Scholar
  48. 48.
    Nonella M.: J. Phys. Chem. B102, 4217–4225 (1998)CrossRefGoogle Scholar
  49. 49.
    Boesch S.E., Wheeler R.A.: J. Phys. Chem. A101, 5799–5804 (1997)CrossRefGoogle Scholar
  50. 50.
    Burie J.-R., Boullais C., Nonella M., Mioskowski C., Nabedryk E., Breton J.: J. Phys. Chem. B101, 6607–6617 (1997)CrossRefGoogle Scholar
  51. 51.
    Nonella M., Mathias G., Eichinger M., Tavan P.: J. Phys. Chem. B107, 316–322 (2003)CrossRefGoogle Scholar
  52. 52.
    O’Malley P.J.: Chem. Phys. Lett.379, 277–281 (2003)CrossRefADSGoogle Scholar
  53. 53.
    Kacprzak S., Kaupp M.: J. Phys. Chem. B108, 2464–2469 (2004)CrossRefGoogle Scholar
  54. 54.
    Harriman J.E.: Theoretical Foundations of Electron Spin Resonance. New York: Academic Press 1978.Google Scholar
  55. 55.
    Weltner W.: Magnetic Atoms and Molecules. New York: Dover Publications 1983.Google Scholar
  56. 56.
    Lucken E.A.C.: Nuclear Quadrupole Coupling Constants. New York: Academic Press 1969.Google Scholar
  57. 57.
    Gordy W.: Theory and Applications of Electron Spin Resonance. New York: Wiley 1980.Google Scholar
  58. 58.
    Tokman M., Sundholm D., Pyykkö P., Olsen J.: Chem. Phys. Lett.265, 60–64 (1997)CrossRefADSGoogle Scholar
  59. 59.
    Bishop D.M., Cheung L.M.: Phys. Rev. A20, 381–384 (1979)CrossRefADSGoogle Scholar
  60. 60.
    Pyykkö P.: Mol. Phys.99, 1617–1629 (2001)CrossRefADSGoogle Scholar
  61. 61.
    Frisch M.J., Trucks G.W., Schlegel H.B., Scuseria G.E., Robb M.A., Cheeseman J.R., Zakrzewski V.G., Montgomery J.A. Jr., Stratmann R.E., Burant J.C., Dapprich S., Millam J.M., Daniels A.D., Kudin K.N., Strain M.C., Farkas O., Tomasi J., Barone V., Cossi M., Cammi R., Mennucci B., Pomelli C., Adamo C., Clifford S., Ochterski J., Petersson G.A., Ayala P.Y., Cui Q., Morokuma K., Salvador P., Dannenberg J.J., Malick D.K., Rabuck A.D., Raghavachari K., Foresman J.B., Cioslowski J., Ortiz J.V., Baboul A.G., Stefanov B.B., Liu G., Liashenko A., Piskorz P., Komaromi I., Gomperts R., Martin R.L., Fox D.J., Keith T., Al-Laham M.A., Peng C.Y., Nanayakkara A., Challacombe M., Gill P.M.W., Johnson B.G., Chen W., Wong M.W., Andres J.L., Gonzalez C., Head-Gordon M., Replogle E.S., Pople J.A.: Gaussian 98 (Revision A.11). Pittsburgh, Pa.: Gaussian, Inc. 2001.Google Scholar
  62. 62.
    Becke A.D.: J. Chem. Phys.98, 5648–5652 (1993)CrossRefADSGoogle Scholar
  63. 63.
    Perdew J.P.: Physica B172, 1–6 (1991)CrossRefADSGoogle Scholar
  64. 64.
    Perdew J.P., Wang Y.: Phys. Rev. B45, 13244–13249 (1992)CrossRefADSGoogle Scholar
  65. 65.
    Stewart J.J.P.: J. Comput. Chem.10, 209–220 (1989)CrossRefGoogle Scholar
  66. 66.
    Stewart J.J.P.: J. Comput. Chem.10, 221–264 (1989)CrossRefGoogle Scholar
  67. 67.
    O’Malley P.: J. Phys. Chem. A102, 248–253 (1998)CrossRefGoogle Scholar
  68. 68.
    O’Malley P.: J. Am. Chem. Soc.120, 5093–5097 (1998)CrossRefGoogle Scholar
  69. 69.
    Kaupp M.: Biochemistry41, 2895–2900 (2002)CrossRefGoogle Scholar
  70. 70.
    Salikhov K.M., Bock C.H., Stehlik D.: Appl. Magn. Reson.1, 195–211 (1990)CrossRefGoogle Scholar
  71. 71.
    Lendzian F., Rautter J., Käß H., Gardiner A., Lubitz W.: Ber. Bunsenges. Phys. Chem.100, 2036–2040 (1996)Google Scholar
  72. 72.
    Spoyalov A.P., Hulsebosch R.J., Shochat S., Gast P., Hoff A.J.: Chem. Phys. Lett.263, 715–720 (1996)CrossRefADSGoogle Scholar
  73. 73.
    Flores M., Isaacson R., Abresch E., Calvo R., Lubitz W., Feher G.: Biophys. J.90, 3356–3362 (2006)CrossRefGoogle Scholar
  74. 74.
    Rohrer M., MacMillan F., Prisner T.F., Gardiner A., Möbius K., Lubitz W.: J. Phys. Chem. B102, 4648–4657 (1998)CrossRefGoogle Scholar
  75. 75.
    Fritscher J.: Phys. Chem. Chem. Phys.6, 4950–4956 (2004)CrossRefGoogle Scholar
  76. 76.
    Isaacson R.A., Abresch E.C., Lendzian F., Boullais C., Paddock M.L., Mioskowski C., Lubitz W., Feher G., in: The Reaction Center of Photosynthetic Bacteria: Structure and Dynamics (Michel-Beyerle M.-E., ed.). Berlin: Springer 1996.Google Scholar
  77. 77.
    Eriksson L.A., Himo F., Siegbahn P.E.M., Babcock G.T.: J. Phys. Chem. A101, 9496–9504 (1997)CrossRefGoogle Scholar
  78. 78.
    Mattar S.M., Emwas A.H., Stephens A.D.: Chem. Phys. Lett.363, 152–160 (2002)CrossRefADSGoogle Scholar

Copyright information

© Springer 2006

Authors and Affiliations

  1. 1.Institut für Physikalische und Theoretische Chemie and Center for Biomolecular Magnetic ResonanceJ. W. Goethe-UniversitätFrankfurt am MainGermany

Personalised recommendations