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

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Abstract

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 t-·A 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.

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References

  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. Schweiger A., Jeschke G.: Principles of Pulse Electron Paramagnetic Resonance. Oxford: Oxford University Press 2001.

    Google Scholar 

  3. Parr R.G., Yang W.: Density-Functional Theory of Atoms and Molecules. New York: Oxford University Press 1989.

    Google Scholar 

  4. Engels B., Eriksson L.A., Lunell S.: Adv. Quantum Chem.27, 297–369 (1996)

    Article  Google Scholar 

  5. Barone V., in: Recent Advances in Density Functional Methods, Part I (Chong D.P., ed.). Singapore: World Scientific Press 1996.

    Google Scholar 

  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. Kaupp M., Malkin V.G., Bühl M. (eds.): Calculation of NMR and EPR Parameters. Weinheim: Wiley-VCH 2004.

    Google Scholar 

  8. Munzarová M., Kaupp M.: J. Phys. Chem. A103, 9966–9983 (1999)

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  11. Koster A.M., Calaminici P., Russo N.: Phys. Rev. A53, 3865–3868 (1996)

    Article  ADS  Google Scholar 

  12. Salzmann R., Kaupp M., McMahon M.T., Oldfield E.: J. Am. Chem. Soc.120, 4771–4783 (1998)

    Article  Google Scholar 

  13. de Luca G., Russo N., Köster A.M., Calaminici P., Jug K.: Mol. Phys.97, 347–354 (1999)

    Article  ADS  Google Scholar 

  14. Bailey W.C.: Chem. Phys.252, 57–66 (2000)

    Article  ADS  Google Scholar 

  15. Sicilia E., de Luca G., Chiodo S., Russo N., Calaminici P., Köster A.M., Jug K.: Mol. Phys.99, 1039–1051 (2001)

    Article  ADS  Google Scholar 

  16. Janowski T., Jaszunski M.: Int. J. Quantum Chem.90, 1083–1090 (2002)

    Article  Google Scholar 

  17. Latosiñska J.N.: Int. J. Quantum Chem.91, 284–296 (2003)

    Article  Google Scholar 

  18. Zhang Y., Gossman W., Oldfield E.: J. Am. Chem. Soc.125, 16387–16396 (2003)

    Article  Google Scholar 

  19. Sinnecker S., Reijerse E., Neese F., Lubitz W.: J. Am. Chem. Soc.126, 3280–3290 (2004)

    Article  Google Scholar 

  20. Stein M., van Lenthe E., Baerends E.J., Lubitz W.: J. Am. Chem. Soc.123, 5839–5840 (2001)

    Article  Google Scholar 

  21. Stein M., Lubitz W.: Phys. Chem. Chem. Phys.3, 2668–2675 (2001)

    Article  Google Scholar 

  22. Wetmore S.D., Smith D.M., Golding B.T., Radom L.: J. Am. Chem. Soc.123, 7963–7972 (2001)

    Article  Google Scholar 

  23. O’Malley P., Collins S.J.: J. Am. Chem. Soc.123, 11042–11046 (2001)

    Article  Google Scholar 

  24. Sinnecker S., Koch W., Lubitz W.: J. Phys. Chem. B106, 5281–5288 (2002)

    Article  Google Scholar 

  25. Jaszewski A.R., Jezierska J.: Chem. Phys. Lett.343, 571–580 (2001)

    Article  ADS  Google Scholar 

  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)

    Article  Google Scholar 

  27. Torrent M., Musaev D.G., Morokuma K., Ke S.-C., Warncke K.J.: J. Phys. Chem. B103, 8618–8627 (1999)

    Article  Google Scholar 

  28. Torrent M., Mansour D., Day E.P., Morokuma K.: J. Phys. Chem. A105, 4546–4557 (2001)

    Article  Google Scholar 

  29. Schiemann O., Fritscher J., Kisseleva N., Sigurdsson S.T., Prisner T.F.: ChemBioChem4, 1057–1065 (2003)

    Article  Google Scholar 

  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)

    Article  Google Scholar 

  31. Schöneboom J.C., Neese F., Thiel W.: J. Am. Chem. Soc.127, 5840–5853 (2005)

    Article  Google Scholar 

  32. Kacprzak S., Kaupp M., MacMillan F.: J. Am. Chem. Soc.128, 5659–5671 (2006)

    Article  Google Scholar 

  33. Crofts A.R., Wraight C.A.: Biochim. Biophys. Acta726, 149–185 (1983)

    Google Scholar 

  34. Nicholls D.G., Ferguson S.J.: Bioenergetics. London: Academic Press 2002.

    Google Scholar 

  35. Lubitz W., Feher G.: Appl. Magn. Reson.17, 1–48 (1999)

    Article  Google Scholar 

  36. Stowell M.H.B., McPhillips T.M., Rees D.C., Soltis S.M., Abresch E., Feher G.: Science276, 812–816 (1997)

    Article  Google Scholar 

  37. Flores M., Isaacson R., Abresch E., Calvo R., Lubitz W., Feher G.: Biophys. J.90, 3356–3362 (2006)

    Article  Google Scholar 

  38. Breton J., Boullais C., Burie J.-R., Nabedryk E., Mioskowski C.: Biochemistry33, 14378–14386 (1994)

    Article  Google Scholar 

  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. Breton J., Nabedryk E.: Biochim. Biophys. Acta1275, 84–90 (1996)

    Article  Google Scholar 

  41. Ermler U., Fritzsch G., Buchanan S.K., Michel H.: Structure2, 925–936 (1994)

    Article  Google Scholar 

  42. Fritzsch G., Koepke J., Diem R., Kuglstatter A., Baciou L.: Acta Crystallogr. D58, 1660–1663 (2002)

    Article  Google Scholar 

  43. Bittl R., Zech S.G.: J. Phys. Chem. B101, 1429–1436 (1997)

    Article  Google Scholar 

  44. Prisner T.F., van der Est A., Bittl R., Lubitz W., Stehlik D., Möbius K.: Chem. Phys.194, 361–370 (1995)

    Article  Google Scholar 

  45. Himo F., Babcock G.T., Eriksson L.A.: J. Phys. Chem. A103, 3745–3749 (1999)

    Article  Google Scholar 

  46. Hutter M.C., Hughes J.M., Reimers J.R., Hush N.S.: J. Phys. Chem. B103, 4906–4915 (1999)

    Article  Google Scholar 

  47. O’Malley P.: Chem. Phys. Lett.285, 99–104 (1998)

    Article  ADS  Google Scholar 

  48. Nonella M.: J. Phys. Chem. B102, 4217–4225 (1998)

    Article  Google Scholar 

  49. Boesch S.E., Wheeler R.A.: J. Phys. Chem. A101, 5799–5804 (1997)

    Article  Google Scholar 

  50. Burie J.-R., Boullais C., Nonella M., Mioskowski C., Nabedryk E., Breton J.: J. Phys. Chem. B101, 6607–6617 (1997)

    Article  Google Scholar 

  51. Nonella M., Mathias G., Eichinger M., Tavan P.: J. Phys. Chem. B107, 316–322 (2003)

    Article  Google Scholar 

  52. O’Malley P.J.: Chem. Phys. Lett.379, 277–281 (2003)

    Article  ADS  Google Scholar 

  53. Kacprzak S., Kaupp M.: J. Phys. Chem. B108, 2464–2469 (2004)

    Article  Google Scholar 

  54. Harriman J.E.: Theoretical Foundations of Electron Spin Resonance. New York: Academic Press 1978.

    Google Scholar 

  55. Weltner W.: Magnetic Atoms and Molecules. New York: Dover Publications 1983.

    Google Scholar 

  56. Lucken E.A.C.: Nuclear Quadrupole Coupling Constants. New York: Academic Press 1969.

    Google Scholar 

  57. Gordy W.: Theory and Applications of Electron Spin Resonance. New York: Wiley 1980.

    Google Scholar 

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

    Article  ADS  Google Scholar 

  59. Bishop D.M., Cheung L.M.: Phys. Rev. A20, 381–384 (1979)

    Article  ADS  Google Scholar 

  60. Pyykkö P.: Mol. Phys.99, 1617–1629 (2001)

    Article  ADS  Google Scholar 

  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. Becke A.D.: J. Chem. Phys.98, 5648–5652 (1993)

    Article  ADS  Google Scholar 

  63. Perdew J.P.: Physica B172, 1–6 (1991)

    Article  ADS  Google Scholar 

  64. Perdew J.P., Wang Y.: Phys. Rev. B45, 13244–13249 (1992)

    Article  ADS  Google Scholar 

  65. Stewart J.J.P.: J. Comput. Chem.10, 209–220 (1989)

    Article  Google Scholar 

  66. Stewart J.J.P.: J. Comput. Chem.10, 221–264 (1989)

    Article  Google Scholar 

  67. O’Malley P.: J. Phys. Chem. A102, 248–253 (1998)

    Article  Google Scholar 

  68. O’Malley P.: J. Am. Chem. Soc.120, 5093–5097 (1998)

    Article  Google Scholar 

  69. Kaupp M.: Biochemistry41, 2895–2900 (2002)

    Article  Google Scholar 

  70. Salikhov K.M., Bock C.H., Stehlik D.: Appl. Magn. Reson.1, 195–211 (1990)

    Article  Google Scholar 

  71. Lendzian F., Rautter J., Käß H., Gardiner A., Lubitz W.: Ber. Bunsenges. Phys. Chem.100, 2036–2040 (1996)

    Google Scholar 

  72. Spoyalov A.P., Hulsebosch R.J., Shochat S., Gast P., Hoff A.J.: Chem. Phys. Lett.263, 715–720 (1996)

    Article  ADS  Google Scholar 

  73. Flores M., Isaacson R., Abresch E., Calvo R., Lubitz W., Feher G.: Biophys. J.90, 3356–3362 (2006)

    Article  Google Scholar 

  74. Rohrer M., MacMillan F., Prisner T.F., Gardiner A., Möbius K., Lubitz W.: J. Phys. Chem. B102, 4648–4657 (1998)

    Article  Google Scholar 

  75. Fritscher J.: Phys. Chem. Chem. Phys.6, 4950–4956 (2004)

    Article  Google Scholar 

  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. Eriksson L.A., Himo F., Siegbahn P.E.M., Babcock G.T.: J. Phys. Chem. A101, 9496–9504 (1997)

    Article  Google Scholar 

  78. Mattar S.M., Emwas A.H., Stephens A.D.: Chem. Phys. Lett.363, 152–160 (2002)

    Article  ADS  Google Scholar 

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Authors and Affiliations

  1. Institut für Physikalische und Theoretische Chemie and Center for Biomolecular Magnetic Resonance, J. W. Goethe-Universität, Max-von-Laue-Straße 7, 60438, Frankfurt am Main, Germany

    J. Fritscher, T. F. Prisner & F. MacMillan

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  1. J. Fritscher
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  2. T. F. Prisner
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  3. F. MacMillan
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Fritscher, J., Prisner, T.F. & MacMillan, F. Theoretical investigation of Q −·A -ligand interactions in bacterial reaction centers ofRhodobacter sphaeroides . Appl. Magn. Reson. 30, 251–268 (2006). https://doi.org/10.1007/BF03166200

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  • DOI: https://doi.org/10.1007/BF03166200

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