Skip to main content
SpringerLink
Log in

High-field EPR, ENDOR and ELDOR on bacterial photosynthetic reaction centers

  • Published:
Applied Magnetic Resonance Aims and scope Submit manuscript

Abstract

We report on recent 95 and 360 GHz high-field electron paramagnetic resonance (EPR), electron-nuclear double resonance (ENDOR) and pulsed electron-electron double resonance (PELDOR) studies of wild-type and mutant reaction centers (RCs) from the photosynthetic bacteriumRhodobacter sphaeroides. Taking advantage of the excellent spectral and temporal resolution of EPR at 95 and 360 GHz, the electron-transfer (ET) cofactors radical ions and spin-correlated radical pairs were characterized by theirg- and hyperfine-tensor components, their anisotropicT 2 relaxation as well as by the dipolar interaction between P •+865 Q •−A radical pairs. The goal of these studies is to better understand the dominant factors determining the specificity and directionality of transmembrane ET processes in photosynthetic RC proteins. In particular, our multifrequency experiments elucidate the subtle cofactor-protein interactions, which are essential for fine-tuning the ET characteristics, e.g., the unidirectionality of the light-induced ET pathways along the A branch of the RC protein. By our high-field techniques, frozen-solution RCs of novel site-specific single and double mutants ofR. sphaeroides were studied to modulate the ET characteristics, e.g., even to the extent that dominant B branch ET prevails. The presented multifrequency EPR work culminates in first 360 GHz ENDOR results from organic nitroxide radicals as well as in first 95 GHz high-field PELDOR results from orientationally selected spin-polarized radical pairs P •+865 Q •−A , which allow to determine the full geometrical structure of the pairs even in frozen-solution RCs.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Feher G.: J. Chem. Soc. Perkin Trans. 211, 1861–1867 (1992)

    Article  Google Scholar 

  2. Blankenship R.E.: Molecular Mechanisms of Photosynthesis. Oxford: Blackwell Science 2002.

    Book  Google Scholar 

  3. Bixon M., Fajer J., Feher G., Freed J.H., Gamliel D., Hoff A.J., Levanon H., Möbius K., Nechushtai R., Norris J.R., Scherz A., Sessler J.L., Stehlik D.: Isr. J. Chem.32, 369–518 (1992)

    Google Scholar 

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

    Article  Google Scholar 

  5. Kirmeier C., Holten D.: Photosynth. Res.13, 225–260 (1987)

    Article  Google Scholar 

  6. Kirmeier C., Bautista J.A., Laible P.D., Hanson D.K., Holten D.: J. Phys. Chem. B109, 24160–24172 (2005)

    Article  Google Scholar 

  7. Paddock M.L., Isaacson R.A., Abresch E.C., Okamura M.Y.: Appl. Magn. Reson.31, 29 (2007)

    Google Scholar 

  8. Jortner J., Bixon M. (eds.): Electron Transfer: from Isolated Molecules to Biomolecules. Advances in Chemical Physics, vols. 106–107. New York: Wiley 1999.

    Google Scholar 

  9. Haffa A.L.M., Lin S., Williams J.C., Bowen B.P., Taguchi A.K.W., Allen J.P., Woodbury N.W.: J. Phys. Chem. B108, 4–7 (2004)

    Article  Google Scholar 

  10. Lancaster C.R.D., Michel H. in: Handbook of Metalloproteins (Messerschmidt A., Huber R., Poulos T., Wieghardt K., eds.), p. 119. Chichester: John Wiley 2001.

    Google Scholar 

  11. Wakeham M., Jones M.: Biochem. Soc. Trans.33, 851–857 (2005)

    Article  Google Scholar 

  12. Haffa A.L.M., Lin S., Williams J.C., Taguchi A.K.W., Allen J.P., Woodbury N.W.: J. Phys. Chem. B107, 12503–12510 (2003)

    Article  Google Scholar 

  13. Paddock M.L., Chang C., Xu Q., Abresch E.C., Axelrod H.L., Feher G., Okamura M.Y.: Biochemistry44, 6920–6928 (2005)

    Article  Google Scholar 

  14. Marcus R.A.: J. Chem. Phys.24, 966–978 (1956)

    Article  ADS  Google Scholar 

  15. Michel-Beyerle M.-E. (ed.): The Reaction Center of Photosynthetic Bacteria: Structure and Dynamics. Berlin: Springer 1996.

    Google Scholar 

  16. Rautter J., Lendzian F., Schulz C., Fetsch A., Kuhn M., Lin X., Williams J.C., Allen J.P., Lubitz W.: Biochemistry34, 8130–8143 (1995)

    Article  Google Scholar 

  17. Plato M., Möbius K., Michel-Beyerle M.-E., Bixon M., Jortner J.: J. Am. Chem. Soc.110, 7279–7285 (1988)

    Article  Google Scholar 

  18. Levanon H., Möbius K.: Annu. Rev. Biophys. Biomol. Struct.26, 495–540 (1997)

    Article  Google Scholar 

  19. Feher G.: Phys. Rev.103, 834–835 (1956)

    Article  ADS  Google Scholar 

  20. Milov A.D., Ponomarev A.B., Tsvertkov Y.D.: Chem. Phys. Lett.110, 67–72 (1984)

    Article  ADS  Google Scholar 

  21. Fuchs M.R., Schleicher E., Schnegg A., Kay C.W.M., Törring J., Bittl R., Bacher A., Richter G., Möbius K., Weber S.: J. Phys. Chem. B106, 885–8890 (2002)

    Article  Google Scholar 

  22. Schnegg A., Kay C.W.M., Schleicher E., Hitomi K., Todo T., Möbius K., Weber S.: Mol. Phys.104, 1627–1633 (2006)

    Article  ADS  Google Scholar 

  23. Feher G., Okamura M.Y. in: The Photosynthetic Bacteria (Clayton R.K., Sistrom W.R., eds.), pp. 349–386. New York: Plenum Press 1978.

    Google Scholar 

  24. Schulz C., Müh F., Beyer A., Jordan R., Schlodder E., Lubitz W. in: Photosynthesis: Mechanisms and Effects (Garab G., ed.), pp. 767–770. Dordrecht: Kluwer 1998.

    Google Scholar 

  25. Paddock M.L., Rongey S.H., Feher G., Okamura M.Y.: Proc. Natl. Acad. Sci. USA86, 6602–6606 (1989)

    Article  ADS  Google Scholar 

  26. Williams J.C., Haffa A.L.M., McCulley J.L., Woodbury N.W., Allen J.P.: Biochemistry40, 15403–15407 (2001)

    Article  Google Scholar 

  27. Debus R.J., Feher G., Okamura M.Y. Biochemistry25, 2276–2287 (1986)

    Article  Google Scholar 

  28. 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 (Michel-Beyerle M.-E., ed.), pp. 353–368. Berlin: Springer 1995.

    Google Scholar 

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

    Article  Google Scholar 

  30. Lubitz W., Abresch E.C., Debus R.J., Isaacson R.A., Okamura M.Y., Feher G.: Biochim. Biophys. Acta808, 464–469 (1985)

    Article  Google Scholar 

  31. Pople J.A., Beveridge D.L.: Approximate Molecular Orbital Theory. New York: McGraw Hill 1970.

    Google Scholar 

  32. Stewart J.J.P.: J. Comput.-Aided Mol. Des.4, 1–105 (1990)

    Article  ADS  Google Scholar 

  33. Ridley J.E., Zerner M.C.: Theor. Chem. Acta32, 111–134 (1973)

    Article  Google Scholar 

  34. Schreckenbach G., Ziegler T.: J. Phys. Chem. A101, 3388–3399 (1997)

    Article  Google Scholar 

  35. Schreckenbach G., Ziegler T.: Theor. Chem. Acc.99, 71–82 (1998)

    Google Scholar 

  36. Patchkovskii S., Ziegler T.: J. Phys. Chem. A105, 5490–5497 (2001)

    Article  Google Scholar 

  37. Malkina O.L., Vaara J., Schimmelpfennig B., Munzarová M.L., Malkin V.G., Kaupp M.: J. Am. Chem. Soc.122, 9206–9218 (2000)

    Article  Google Scholar 

  38. Neese F., Munzarova M.L. in: The Quantum Chemical Calculation of NMR and EPR Properties (Kaupp M., Bühl M., Malkin V., eds.), p. 21. Weinheim: Wiley-VCH 2004.

    Chapter  Google Scholar 

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

    Article  ADS  Google Scholar 

  40. van Lenthe E., Wormer P.E.S., van der Avoird A.: J. Chem. Phys.107, 2488–2498 (1997)

    Article  ADS  Google Scholar 

  41. Neyman K.M., Ganyushin D.I., Matveev A.V., Nashzov V.A.: J. Phys. Chem. A106, 5022–5030 (2002)

    Article  Google Scholar 

  42. te Velde G., Bickelhaupt F.M., Baerends E.T., Fonseca Guerra C.F., van Gisbergen S.J.A., Snijders J.G., Ziegler T.: J. Comput. Chem.22, 931–967 (2001)

    Article  Google Scholar 

  43. Fuchs M.R., Schnegg A., Platto M., Schulz C., Müh F., Lubitz W., Möbius K.: Chem. Phys.294, 371–384 (2003)

    Article  Google Scholar 

  44. Becke A.D.: Phys. Rev. A38, 3098–3100 (1988)

    Article  ADS  Google Scholar 

  45. Lee C., Yang W., Parr R.G.: Phys. Rev. B37, 785–789 (1988)

    Article  ADS  Google Scholar 

  46. Savitsky A., Kühn M., Duché D., Möbius K., Steinhoff H.J.: J. Phys. Chem. B108, 9541–9548 (2004)

    Article  Google Scholar 

  47. Möbius K., Savitsky A., Fuchs M. in: Very High Frequency (VHF) ESR/EPR. Biological Magnetic Resonance, vol. 22 (Grinberg O., Berliner L.J., eds.) pp. 45–93. New York: Kluwer Academic/Plenum 2004.

    Google Scholar 

  48. Möbius K., Savitsky A., Schnegg A., Plato M., Fuhs M.: Phys. Chem. Chem. Phys.7, 19–42 (2005)

    Article  Google Scholar 

  49. Prisner T.F., Rohrer M., Möbius K.: Appl. Magn. Reson.7, 167–183 (1994)

    Article  Google Scholar 

  50. Burghaus O., Rohrer M., Götzinger T., Plato M., Möbius K.: Meas. Sci. Technol.3, 765–774 (1992)

    Article  ADS  Google Scholar 

  51. Klette R., Törring J.T., Plato M., Möbius K., Bönigk B., Lubitz W.: J. Phys. Chem.97, 2015–2020 (1993)

    Article  Google Scholar 

  52. Fuhs M., Schnegg A., Prisner T., Köhne I., Hanley J., Rutherford A.W., Möbius K.: Biochim. Biophys. Acta1556, 81–88 (2002)

    Article  Google Scholar 

  53. Dubinskii A.A., Grishin Y.A., Savitsky A.N., Möbius K.: Appl. Magn. Reson.22, 369–386 (2002)

    Google Scholar 

  54. Fuchs M.R., Prisner T.F., Möbius K.: Rev. Sci. Instrum.70, 3681–3863 (1999)

    Article  ADS  Google Scholar 

  55. Smith G.M., Riedi P.C. in: Electron Paramagnetic Resonance, vol. 17 (Gilbert B.C., Davies M.J., McLauchland K.A., eds.), pp. 164–204. Specialist Perodical Reports. Cambridge: Royal Society of Chemistry 2000.

    Chapter  Google Scholar 

  56. Disselhorst J.A.J.M., Vandermeer H., Poluektov O.G., Schmidt J.: J. Magn. Reson. A115, 183–188 (1995)

    Article  Google Scholar 

  57. Rohrer M., Plato M., MacMillan F., Grishin Y., Lubitz W., Möbius K.: J. Magn. Reson. A116, 59–66 (1995)

    Article  Google Scholar 

  58. Brunel L.-C., van Tol J., Angerhofer A., Hill S., Krzystek J., Maniero A.L. in: Very High Frequency (VHF) ESR/EPR. Biological Magnetic Resonance, vol. 22 (Grinberg O., Berliner L.J., eds.), pp. 465–505. New York: Kluwer Academic/Plenum 2004.

    Google Scholar 

  59. Lendzian F., Huber M., Isaacson R.A., Endeward B., Plato M., Bönigk B., Möbius K., Lubitz W., Feher G.: Biochim. Biophys. Acta1183, 139–160 (1993)

    Article  Google Scholar 

  60. Burghaus O., Plato M., Rohrer M., Möbius K., MacMillan F., Lubitz W.: J. Phys. Chem.97, 7639–7647 (1993)

    Article  Google Scholar 

  61. Hoff A.J., Deisenhofer J.: Phys. Rep.287, 1–247 (1997)

    Article  ADS  Google Scholar 

  62. Huber M.: Photosynth. Res.52, 1–26 (1997)

    Article  ADS  Google Scholar 

  63. Lubitz W., Lendzian F., Bittl R.: Acc. Chem. Res.35, 313–320 (2002)

    Article  Google Scholar 

  64. Ivancich A., Artz K., Williams J.C., Allen J.P., Mattioli T.-A.: Biochemistry37, 11812–11820 (1998)

    Article  Google Scholar 

  65. Huber M., Törring J.T.: Chem. Phys.194, 379–385 (1995)

    Article  ADS  Google Scholar 

  66. Huber M., Törring J.T., Plato M., Finck U., Lubitz W., Feick R., Schenck C.C., Möbius K.: J. Sol. Energy Mater. Sol. Cells38, 119–126 (1995)

    Article  Google Scholar 

  67. Artz K., Williams J.C., Allen J.P., Lendzian F., Rautter J., Lubitz W.: Proc. Natl. Acad. Sci. USA94, 13582–13587 (1997)

    Article  ADS  Google Scholar 

  68. Müh F., Lendzian F., Roy M., Williams J.C., Allen J.P., Lubitz W.: J. Phys. Chem. B106, 3226–3236 (2002)

    Article  Google Scholar 

  69. Möbius K., Biehl R. in: Multiple Electron Resonance Spectroscopy (Dorio M.M., Freed J.H., eds.), pp. 475–508. New York: Plenum 1979.

    Google Scholar 

  70. Gessner C., Lendzian F., Bönigk B., Plato M., Möbius K., Lubitz W.: Appl. Magn. Reson.3, 763–777 (1992)

    Google Scholar 

  71. Lin X., Murchinson H.A., Nagarajan V., Parson W.W., Allen J.P., Williams J.C.: Proc. Natl. Acad. Sci. USA91, 10265–10269 (1994)

    Article  ADS  Google Scholar 

  72. Wang W., Belford R.L., Clarkson R.B., Davis P.H., Forrer J., Nilges M.J., Timken M.D., Walczak T., Thurnauer M.C., Norris J.R., Morris A.L., Zhang Y.: Appl. Magn. Reson.6, 195–215 (1994)

    Article  Google Scholar 

  73. Huber M., Isaacson R.A., Abresh E.C., Gaul D., Schenck C.C., Feher G.: Biochim. Biophys. Acta1273, 108–128 (1996)

    Article  Google Scholar 

  74. Chirino A.J., Lous E.J., Huber M., Allen J.P., Schenck C.C., Paddock M.L., Feher G., Rees D.C.: Biochemistry33, 4584–4593 (1994)

    Article  Google Scholar 

  75. Fajer J., Borg D.C., Forman A., Dolphin D., Felton R.H.: J. Am. Chem. Soc.95, 2739–2741 (1973)

    Article  Google Scholar 

  76. McDowell L.M., Gaul D., Kimaier C., Holten D., Schenck C.C.: Biochemistry30, 8315–8322 (1991)

    Article  Google Scholar 

  77. Bratt P.J., Ringus E., Hassan A., van Tol H., Maniero A.-L., Brunel L.-C., Rohrer M., Bubenzer-Hange C., Scheer H., Angerhofer A.: J. Phys. Chem. B103, 10973–10982 (1999)

    Article  Google Scholar 

  78. Gulin V.I., Dikanov S.A., Tsvetkov Y.D., Evelo R.G., Hoff A.J.: Pure Appl. Chem.64, 903–906 (1992)

    Article  Google Scholar 

  79. Plato M., Möbius K.: Chem. Phys.197, 289–295 (1995)

    Article  ADS  Google Scholar 

  80. Müh F., Bibikova M., Lendzian F., Oesterhelt D., Lubitz W. in: Photosynthesis: Mechanisms and Effects (Garab G., ed.), pp. 763–766. Dordrecht: Kluwer 1998.

    Google Scholar 

  81. Müh F., Bibikova M., Schlodder E., Oesterhelt D., Lubitz W.: Biochim. Biophys. Acta1459, 191–201 (2000)

    Article  Google Scholar 

  82. Atherton N.M.: Principles of Electron Spin Resonance. New York: Ellis Horwood 1993.

    Google Scholar 

  83. Isaacson R., Lendzian F., Abresch E., Lubitz W., Feher G.: Biophys. J.69, 311–322 (1995)

    Article  ADS  Google Scholar 

  84. Rohrer M., Gast P., Möbius K., Prisner T.F.: Chem. Phys. Lett.259, 523–530 (1996)

    Article  ADS  Google Scholar 

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

    Article  Google Scholar 

  86. Burghaus O., Toth-Kischkat A., Klette R., Möbius K.: J. Magn. Reson.80, 383–388 (1988)

    Google Scholar 

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

    Article  Google Scholar 

  88. Stehlik D., Möbius K.: Annu. Rev. Phys. Chem.48, 745–784 (1997)

    Article  Google Scholar 

  89. Weber S. in: Electron Paramagnetic Resonance, vol. 17 (Gilbert B.C., Davies M.J., McLauchlan K.A., eds.), pp. 43–77. Specialist Periodical Reports. Cambridge: Royal Society of Chemistry 2000.

    Chapter  Google Scholar 

  90. Lubitz W. in: Electron Paramagnetic Resonance, vol. 19 (Gilbert B.C., Davies M.J., Murphy D.M., eds.), pp. 174–242. Specialist Periodical Reports. Cambridge: Royal Society of Chemistry 2000.

    Google Scholar 

  91. van der Est A.: Biochim. Biophys. Acta1507, 212–225 (2001)

    Article  Google Scholar 

  92. Thurnauer M.C., Poluektov O.G., Kothe G. in: Very High Frequency (VHF) ESR/EPR. Biological Magnetic Resonance, vol. 22 (Grinberg O., Berliner L.J., eds.), pp. 166–206. New York: Kluwer Academic/Plenum 2004.

    Google Scholar 

  93. Denysenkov V.P., Prisner T.F., Stubbe J., Bennati M.: Appl. Magn. Reson.29, 375–384 (2005)

    Article  Google Scholar 

  94. Denysenkov V.P., Prisner T.F., Stubbe J., Bennati M.: Proc. Natl. Acad. Sci. USA103, 13386–13390 (2006)

    Article  ADS  Google Scholar 

  95. Kamlowski A., Zech S.G., Fromme P., Bittl R., Lubitz W., Witt H.T., Stehlik D.: J. Phys. Chem. B102, 8266–8277 91998)

    Article  Google Scholar 

  96. Stehlik D., Bock C.H., Petersen J.: J. Phys. Chem.93, 1612–1619 (1989)

    Article  Google Scholar 

  97. Hore P.J., Hunter D.A., McKie C.D., Hoff A.J.: Chem. Phys. Lett.137, 495–500 (1987)

    Article  ADS  Google Scholar 

  98. Closs G.L., Forbes M.D.E., Norris J.R.: J. Phys. Chem.91, 3592–3599 (1987)

    Article  Google Scholar 

  99. Kandrashkin Y., van der Est A.: Spectrochim. Acta A57, 1697–1709 (2001)

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Google Scholar 

  102. Schnegg A., Fuhs M., Rohrer M., Lubitz W., Prisner T.F., Möbius K.: J. Phys. Chem. B106, 9454–9462 (2002)

    Article  Google Scholar 

  103. Stoll S., Schweiger A.: J. Magn. Reson. 178, 42–55 (2006)

    Article  ADS  Google Scholar 

Download references

Author information

Author notes

  1. M. R. Fuchs

    Present address: Bessy GmbH, Berlin, Germany

  2. E. P. Kirilina

    Present address: PTB, Berlin, Germany

Authors and Affiliations

  1. Department of Physics, Free University Berlin, Berlin, Germany

    A. Schnegg, M. R. Fuchs, E. P. Kirilina, M. Plato, A. Savitsky & K. Möbius

  2. Institute of Chemical Physics, Russian Academy of Sciences, Moscow, Russian Federation

    A. A. Dubinskii

  3. Institute of Chemical Kinetics and Combustion, Russian Academy of Sciences, Novosibirsk, Russian Federation

    Yu. A. Grishin

  4. Max Planck Institute for Bioinorganic Chemistry, Mülheim an der Ruhr, Germany

    W. Lubitz

Authors
  1. A. Schnegg
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. A. Dubinskii
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. M. R. Fuchs
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yu. A. Grishin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. E. P. Kirilina
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. W. Lubitz
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. M. Plato
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. A. Savitsky
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. K. Möbius
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Schnegg, A., Dubinskii, A.A., Fuchs, M.R. et al. High-field EPR, ENDOR and ELDOR on bacterial photosynthetic reaction centers. Appl. Magn. Reson. 31, 59–98 (2007). https://doi.org/10.1007/BF03166248

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF03166248

Keywords

Search

Navigation