Skip to main content
Log in

Exploring hyperfine interactions in spin-correlated radical pairs from photosynthetic proteins: High-frequency ENDOR and quantum beat oscillations

  • Published:
Applied Magnetic Resonance Aims and scope Submit manuscript

Abstract

Electron paramagnetic resonance (EPR) and related spectroscopic tools remain among the most important probes of structure and function of natural photosynthetic systems. Indeed, the challenging questions in the study of photosynthesis have to a great extent dictated the directions taken in the development of EPR and associated spectroscopies. In this overview we demonstrate, with recent examples from our laboratories, the potential of high-frequency and time-resolved EPR spectroscopy to reveal unique information about electron transfer processes and the structure of photosynthetic systems. A common feature of these experiments is that they probe hyperfine interactions of the spincorrelated radical pair. Thus, the analysis of the results requires consideration of three interacting spins: two correlated electron spins with one nuclear spin. The results illustrate the importance of resolving nuclear hyperfine structure for obtaining details of structure-function relationships in photosynthetic electron transfer.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Feher G.: Phys. Rev.103, 834 (1956)

    Article  ADS  Google Scholar 

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

    Google Scholar 

  3. Goldfarb D., Arieli D.: Annu. Rev. Biophys. Biomol. Struct.33, 441–468 (2004)

    Article  Google Scholar 

  4. Dorio M.M., Freed J.H. (eds.): Multiple Electron Resonance Spectroscopy. New York: Plenum 1979.

    Google Scholar 

  5. Feher G., Fuller C.S., Gere E.A.: Phys. Rev.107, 1462 (1957)

    Article  ADS  Google Scholar 

  6. Eisinger J., Feher G.: Phys. Rev.109, 1172 (1958)

    Article  ADS  Google Scholar 

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

    Article  Google Scholar 

  8. Feher G., Hoff A.J., Isaacson R.A., McElroy J.D.: Biophys. Soc. Abstr.13, 61a (1973); Feher G., Hoff A.J., Isaacson R.A., Ackerson L.C.: Ann. N.Y. Acad. Sci.244, 239 (1975)

    Google Scholar 

  9. Norris J.R., Druyan M.E., Katz J.J.: J. Am. Chem. Soc.95, 1680–1682 (1973); Norris J.R., Scheer H., Druyan M.E., Katz J.J.: Proc. Natl. Acad. Sci. USA71, 4897–4900 (1974); Norris J.R., Scheer H., Katz J.J.: Ann. NY Acad. Sci. USA244, 260–280 (1975)

    Article  Google Scholar 

  10. Grinberg O.Y., Berliner L.J. (eds.): Very High Frequency (VHS) ESR/EPR. Biological Magnetic Resonance, vol. 22, p. 569. New York: Kluwer Academic, Plenum 2004.

    Google Scholar 

  11. Poluektov O.G., Utschig L.M., Dubinskij A.A., Thurnauer M.C.: J. Am. Chem. Soc.126, 1644–1645 (2004)

    Article  Google Scholar 

  12. Poluektov O.G., Utschig L.M., Dubinskij A.A., Thurnauer M.C.: J. Am. Chem. Soc.127, 4049–4059 (2005)

    Article  Google Scholar 

  13. Bennebroek M.T., Arnold A., Poluektov O.G., Baranov P.G., Schmidt J.: Phys. Rev. B54, 11276–11289 (1996)

    Article  ADS  Google Scholar 

  14. Coremans J.W.A., Poluektov O.G., Groenen E.J.J., Canters G.W., Nar. H., Messerschmidt A.: J. Am. Chem. Soc.118, 12141–12153 (1996)

    Article  Google Scholar 

  15. Thurnauer M.C., Norris J.R.: Chem. Phys. Lett.76, 557–561 (1980)

    Article  ADS  Google Scholar 

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

    Article  Google Scholar 

  17. Buckley C.D., Hunter D.A., Hore P.J., McLauchlan K.A.: Chem. Phys. Lett.135, 307–312 (1987)

    Article  ADS  Google Scholar 

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

    Article  Google Scholar 

  19. Bittl R., Kothe G.: Chem. Phys. Lett.177, 547–553 (1991)

    Article  ADS  Google Scholar 

  20. Kothe G., Weber S., Bittl R., Ohmes E., Thurnauer M.C., Norris J.R.: Chem. Phys. Lett.186, 474–480 (1991)

    Article  ADS  Google Scholar 

  21. Kothe G., Bechtold M., Link G., Ohmes E., Weidner J.-U.: Chem. Phys. Lett.283, 51–60 (1998)

    Article  ADS  Google Scholar 

  22. Tang J., Thurnauer M.C., Norris J.R.: Chem. Phys. Lett.219, 283–290 (1994)

    Article  ADS  Google Scholar 

  23. Salikhov K.M., Kandrashkin Yu.E., Salikhov A.K.: Appl. Magn. Reson.3, 199 (1992)

    Article  Google Scholar 

  24. Dzuba S.A., Gast P., Hoff A.J.: Chem. Phys. Lett.236, 595–602 (1995)

    Article  ADS  Google Scholar 

  25. Tang J., Norris J.R.: Chem. Phys. Lett.233, 192–200 (1995)

    Article  ADS  Google Scholar 

  26. Borovykh I.V., Kulik L.V., Dzuba S.A., Hoff A.J.: Chem. Phys. Lett.338, 173–179 (2001)

    Article  ADS  Google Scholar 

  27. Norris J.R., Morris A.L., Thurnauer M.C., Tang J.: J. Chem. Phys.92, 4239–4249 (1990)

    Article  ADS  Google Scholar 

  28. Morris A.L., Snyder S.W., Zhang Y., Tang J., Thurnauer M.C., Dutton P.L., Robertson D.E., Gunner M.R.: J. Phys. Chem.99, 3854–3866 (1995)

    Article  Google Scholar 

  29. Kandrashkin Y.E., Salikhov A.K., van der Est A., Stehlik D.: Appl. Magn. Reson.15, 417 (1998)

    Article  Google Scholar 

  30. Utschig L.M., Greenfield S.R., Tang J., Laible P.D., Thurnauer M.C.: Biochemistry36, 8548–8558 (1997)

    Article  Google Scholar 

  31. Crespi H.L.: Methods Enzymol.88, 3–5 (1982)

    Article  Google Scholar 

  32. Lakshmi K.V., Reifler M.J., Brudvig G.W., Poluektov O.G., Wagner A.M., Thurnauer M.C.: J. Phys. Chem. B104, 10445–10448 (2000)

    Article  Google Scholar 

  33. Mims W.B.: Proc. R. Soc. Lond.283, 452 (1965)

    Article  ADS  Google Scholar 

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

    Article  Google Scholar 

  35. Steffen M.A., Lao K., Boxer S.G.: Science264, 810–816 (1994)

    Article  ADS  Google Scholar 

  36. Wuttke D.S., Bjerrum M.J., Winkler J.R., Gray H.B.: Science256, 1007–1009 (1992)

    Article  ADS  Google Scholar 

  37. Langen R., Chang I.-J., Germanas J.P., Richards J.H., Winkler J.R., Gray H.B.: Science268, 1733–1735 (1995)

    Article  ADS  Google Scholar 

  38. Babini E., Bertini I., Borsari M., Capozzi F., Luchinat C., Zhang X., Moura G.L.C., Kurnikov I.V., Beratan D.N., Ponce A., Di Bilio A.J., Winkler J.R., Gray H.B.: J. Am. Chem. Soc.122, 4532–4533 (2000)

    Article  Google Scholar 

  39. Link G., Berthold T., Bechtold M., Weidner J.-U., Ohmes E., Tang J., Poluektov O., Utschig L., Schlesselman S.L., Thurnauer M.C., Kothe G.: J. Am. Chem. Soc.123, 4211–4222 (2001)

    Article  Google Scholar 

  40. Poluektov O.G., Utschig L.M., Tang J., Dubinski A.A., Schlesselman S., Thurnauer M.C.: Appl. Magn. Reson.21, 311–323 (2001)

    Article  Google Scholar 

  41. Dubinski A.A., Perekhotsev G.D., Poluektov O.G., Rajh T., Thurnauer M.C.: J. Phys. Chem. B106, 938–944 (2002)

    Article  Google Scholar 

  42. Bone S., Pething R.: J. Mol. Biol.181, 323–326 (1985)

    Article  Google Scholar 

  43. Dashdorj N., Xu W., Martinsson P., Chitnis P.R., Savikhin S.: Biophys. J.86, 3121–3130 (2004)

    Article  ADS  Google Scholar 

  44. Kleinfield D., Okamura M.Y., Feher G.: Biochemistry,23, 5780–5786 (1984)

    Article  Google Scholar 

  45. Deisenhofer J., Norris J.R. (eds.): Photosynthetic Reaction Centers. New York: Academic Press 1993.

    Google Scholar 

  46. Wraight C.A.: Front. Biosci.9, 309–337 (2004)

    Article  Google Scholar 

  47. Graige M.S., Feher G., Okamura M.Y.: Proc. Natl. Acad. Sci. USA95, 11679–11684 (1998)

    Article  ADS  Google Scholar 

  48. Xu Q., Gunner M.R.: Biochemistry40, 3232–3241 (2001)

    Article  Google Scholar 

  49. Treutlein H., Schulten K., Brunger A.T., Karplus M., Deisenhofer J., Michel H.: Proc. Natl. Acad. Sci. USA89, 75–79 (1992)

    Article  ADS  Google Scholar 

  50. Trissl H.W., Bernhardt K., Lapin M.: Biochemistry40, 5290–5298 (2001)

    Article  Google Scholar 

  51. Fursman C.E., Teutloff C., Bittl R.: J. Phys. Chem. B106, 9679–9686 (2002)

    Article  Google Scholar 

  52. Jordan P., Fromme P., Witt H.T., Klukas O., Saenger W., Krauss N.: Nature411, 909–917 (2001)

    Article  ADS  Google Scholar 

  53. Käss H., Bittersmann-Weidlich E., Andréasson L.-E., Bönigk B., Lubitz W.: Chem. Phys.194, 419–432 (1995)

    Article  Google Scholar 

  54. Mac M., Bowlby N.R., Babcock G.T., McCracken J.: J. Am. Chem. Soc.120, 13215–13223 (1998)

    Article  Google Scholar 

  55. Jeschke G.: J. Chem. Phys.106, 10072–10086 (1997)

    Article  ADS  Google Scholar 

  56. Jeschke G., Schweiger A.: J. Chem. Phys.105, 2199–2211 (1996)

    Article  ADS  Google Scholar 

  57. Krabben L., Schlodder E., Jordan R., Carbonera D., Giacometti G., Lee H., Webber A.N., Lubitz W.: Biochemistry39, 13012–13025 (2000)

    Article  Google Scholar 

  58. Stone A.G.: Mol. Phys.7, 311–316 (1963)

    Article  ADS  Google Scholar 

  59. Zech S.G., Hofbauer W., Kamlowski A., Fromme P., Stehlik D., Lubitz W., Bittl R.: J. Phys. Chem. B104, 9728–9739 (2000)

    Article  Google Scholar 

  60. Mac M., Tang X.S., Diner B.A., McCracken J., Babcock G.T.: Biochemistry35, 13288–13293 (1996)

    Article  Google Scholar 

  61. Poluektov O.G., Utschig L.M., Schlesselman S.L., Lakshmi K.V., Brudvig G.W., Kothe G., Thurnauer M.C.: J. Phys. Chem. B106, 8911–8916 (2002)

    Article  Google Scholar 

  62. Petrenko A., Redding K., Kispert L.D.: Chem. Phys. Lett.406, 327–331 (2005)

    Article  ADS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to O. G. Poluektov.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Poluektov, O.G., Utschig, L.M., Thurnauer, M.C. et al. Exploring hyperfine interactions in spin-correlated radical pairs from photosynthetic proteins: High-frequency ENDOR and quantum beat oscillations. Appl. Magn. Reson. 31, 123–143 (2007). https://doi.org/10.1007/BF03166251

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF03166251

Keywords

Navigation