Applied Magnetic Resonance

, Volume 49, Issue 9, pp 1011–1025 | Cite as

The Decrease of the ESEEM Frequency of \({\text{P}}_{700}^{ + } {\text{A}}_{1}^{ - }\) Ion-Radical Pair in Photosystem I Embedded in Trehalose Glassy Matrix at Room Temperature can be Explained by Acceleration of Spin–Lattice Relaxation

  • A. A. SukhanovEmail author
  • M. D. Mamedov
  • K. Möbius
  • A. Yu. Semenov
  • K. M. Salikhov
Original Paper


The main observation in this work is a decrease in the modulation frequency of the primary electron spin-echo decay (ESEEM) of the \({\text{P}}_{ 7 0 0}^{ + }\) cofactor in the reaction center of Photosystem I (PS I) from cyanobacteria Synechocystis sp. PCC 6803 embedded in dry trehalose matrix as the temperature rises from 150 K to room temperature. From the previous studies of the EPR spectrum shape of this system, it is known that, in dry trehalose matrix at room temperature, the distance between \({\text{P}}_{ 7 0 0}^{ + }\) and \({\text{A}}_{ 1}^{ - }\) spins does not increase compared to the distance measured in glycerol–water solution at cryogenic temperature. From the present ESEEM study, we conclude that the decrease of modulation frequency with rising temperature in trehalose matrix can be fully attributed to the influence of accelerated spin–lattice relaxation of \({\text{A}}_{ 1}^{ - }\). Our calculations show that this requires a decrease in the spin–lattice relaxation time from 3 to 1 μs. To the best of our knowledge, this is the first time that a shift in the ESEEM frequency due to the dipole–dipole interaction between the spins is observed that is caused by spin–lattice relaxation. Based on the above-mentioned results, we formulate a model of the protective effect of trehalose matrix on the electron transfer in the reaction center of PS I that is based on different hydrogen-bond networks between trehalose, local water, and protein.



A. Yu. Semenov acknowledges the Russian Foundation for Basic Research (RFBR Grants 17-00-00201). K. Möbius acknowledges sustaining support by the Free University of Berlin. We want to thank Giovanni Venturoli (University of Bologna) for stimulating and fruitful discussions.


  1. 1.
    M. Guergova-Kuras, B. Boudreaux, A. Joliot, P. Joliot, K. Redding, Proc. Natl. Acad. Sci. USA. 98, 4437 (2001)ADSCrossRefGoogle Scholar
  2. 2.
    S. Santabarbara, P. Heathcote, M.C.W. Evans, Biochim. Biophys. Acta Bioenerg. 1708, 283 (2005)CrossRefGoogle Scholar
  3. 3.
    N. Srinivasan, J.H. Golbeck, Biochim. Biophys. Acta Bioenerg. 1787, 1057 (2009)CrossRefGoogle Scholar
  4. 4.
    J. Sun, S. Hao, M. Radle, W. Xu, I. Shelaev, V. Nadtochenko, V. Shuvalov, A. Semenov, H. Gordon, A. Van Der Est, J.H. Golbeck, Biochim. Biophys. Acta Bioenerg. 1837, 1362 (2014)CrossRefGoogle Scholar
  5. 5.
    H. Makita, G. Hastings, FEBS Lett. 589, 1412 (2015)CrossRefGoogle Scholar
  6. 6.
    G. Palazzo, A. Mallardi, A. Hochkoeppler, L. Cordone, G. Venturoli, Biophys. J. 82, 558 (2002)CrossRefGoogle Scholar
  7. 7.
    F. Francia, M. Dezi, A. Mallardi, G. Palazzo, L. Cordone, G. Venturoli, J. Am. Chem. Soc. 130, 10240 (2008)CrossRefGoogle Scholar
  8. 8.
    M. Malferrari, F. Francia, G. Venturoli, J. Phys. Chem. B 119, 13600 (2015)CrossRefGoogle Scholar
  9. 9.
    M. Malferrari, A. Savitsky, M.D. Mamedov, G.E. Milanovsky, W. Lubitz, K. Möbius, A.Y. Semenov, G. Venturoli, Biochim. Biophys. Acta Bioenerg. 1857, 1440 (2016)CrossRefGoogle Scholar
  10. 10.
    I. Shelaev, M. Gorka, A. Savitsky, V. Kurashov, M. Mamedov, F. Gostev, K. Möbius, V. Nadtochenko, J. Golbeck, A. Semenov, Z. Phys. Chem 231, 325 (2017)CrossRefGoogle Scholar
  11. 11.
    F. Francia, G. Palazzo, A. Mallardi, L. Cordone, G. Venturoli, Biophys. J. 85, 2760 (2003)CrossRefGoogle Scholar
  12. 12.
    A. Savitsky, O. Gopta, M. Mamedov, J.H. Golbeck, A. Tikhonov, K. Möbius, A. Semenov, Appl. Magn. Reson. 37, 85 (2010)CrossRefGoogle Scholar
  13. 13.
    L.M. Crowe, D.S. Reid, J.H. Crowe, Biophys. J. 71, 2087 (1996)ADSCrossRefGoogle Scholar
  14. 14.
    J.H. Crowe, J.F. Carpenter, L.M. Crowe, Annu. Rev. Physiol. 60, 73 (1998)CrossRefGoogle Scholar
  15. 15.
    J.S. Clegg, Comp. Biochem. Physiol. B 128, 613 (2001)CrossRefGoogle Scholar
  16. 16.
    L.M. Crowe, Comp. Biochem. Physiol. A Mol. Integr. Physiol. 131, 505–513 (2002)CrossRefGoogle Scholar
  17. 17.
    M. Sakurai, T. Furuki, K. Akao, D. Tanaka, Y. Nakahara, T. Kikawada, M. Watanabe, T. Okuda, Proc. Natl. Acad. Sci. USA 105, 5093 (2008)ADSCrossRefGoogle Scholar
  18. 18.
    A.K. Garg, J.-K. Kim, T.G. Owens, A.P. Ranwala, Y.D. Choi, L.V. Kochian, R.J. Wu, Proc. Natl. Acad. Sci. USA 99, 15898 (2002)ADSCrossRefGoogle Scholar
  19. 19.
    S.S. Jun, Y.Y. Jin, J.C. Hye, N.R. Kim, C.P. Min, Y.N. Hong, J. Plant Biol. 48, 456 (2005)CrossRefGoogle Scholar
  20. 20.
    O. Fernandez, L. Béthencourt, A. Quero, R.S. Sangwan, C. Clément, Christophe. Trends Plant Sci. 15, 409 (2010)CrossRefGoogle Scholar
  21. 21.
    S. Ohtake, Y.J. Wang, J. Pharm. Sci. 100, 2020 (2011)CrossRefGoogle Scholar
  22. 22.
    K. Möbius, W. Lubitz, A. Savitsky, Prog. Nucl. Magn. Reson. Spectrosc. 75, 1 (2013)CrossRefGoogle Scholar
  23. 23.
    A.D. Milov, K.M. Salikhov, M.D. Schirov, Fiz. Tverd. Tela (in Russian) 23, 975–982 (1981)Google Scholar
  24. 24.
    S.A. Dzuba, P. Gast, A.J. Hoff, Chem. Phys. Lett. 236, 595 (1995)ADSCrossRefGoogle Scholar
  25. 25.
    A.J. Hoff, P. Gast, S.A. Dzuba, C.R. Timmel, C.E. Fursman, P.J. Hore, Spectrochem. Acta Part A Mol. Biomol. Spectrosc. 54, 2283 (1998)ADSCrossRefGoogle Scholar
  26. 26.
    K.M. Salikhov, I.T. Khairuzhdinov, R.B. Zaripov, Appl. Magn. Reson. 45, 573 (2014)CrossRefGoogle Scholar
  27. 27.
    G. Zhidomirov, K. Salikhov, Zhur. Experim. Teoret. Fiz. 56, 1933 (1969)Google Scholar
  28. 28.
    K.M. Salikhov, S.A. Dzuba, A.M. Raitsimring, J. Magn. Reson. 42, 255 (1981)ADSGoogle Scholar
  29. 29.
    K.M. Salikhov, Appl. Magn. Reson. 47, 1207 (2016)CrossRefGoogle Scholar
  30. 30.
    L.V. Kulik, S.A. Dzuba, I.A. Grigoryev, Y.D. Tsvetkov, Chem. Phys. Lett. 343, 315 (2001)ADSCrossRefGoogle Scholar
  31. 31.
    L.V. Kulik, E.S. Salnikov, S.A. Dzuba, Appl. Magn. Reson. 28, 1 (2005)CrossRefGoogle Scholar
  32. 32.
    K.M. Salikhov, Y.E. Kandrashkin, A.K. Salikhov, Appl. Magn. Reson. 3, 199 (1992)CrossRefGoogle Scholar
  33. 33.
    G. Shen, J. Zhao, S.K. Reimer, M.L. Antonkine, Q. Cai, S.M. Weiland, J.H. Golbeck, D.A. Bryant, J. Biol. Chem. 277, 20343 (2002)CrossRefGoogle Scholar
  34. 34.
    M. Malferrari, A. Nalepa, G. Venturoli, F. Francia, W. Lubitz, K. Möbius, A. Savitsky, Phys. Chem. Chem. Phys. 16, 9831 (2014)CrossRefGoogle Scholar
  35. 35.
    A. Angerhofer, R. Bittl, Photochem. Photobiol. 63, 11 (1996)CrossRefGoogle Scholar
  36. 36.
    D. Stehlik, K. Möbius, Annu. Rev. Phys. Chem. 48, 745 (1997)ADSCrossRefGoogle Scholar
  37. 37.
    A. Savitsky, J. Niklas, J.H. Golbeck, K. Möbius, W. Lubitz, J. Phys. Chem. B 117, 11184 (2013)CrossRefGoogle Scholar
  38. 38.
    R. Bittl, S.G. Zech, J. Phys. Chem. B 101, 1429 (1997)CrossRefGoogle Scholar
  39. 39.
    R. Bittl, S.G. Zech, P. Fromme, H.T. Witt, W. Lubitz, Biochemistry 36, 12001 (1997)CrossRefGoogle Scholar
  40. 40.
    S.G. Zech, W. Lubitz, R. Bittl, Ber. Bunsen-Ges. 100, 2041 (1996)CrossRefGoogle Scholar
  41. 41.
    B. Zybailov, A. van der Est, S.G. Zech, C. Teutloff, T.W. Johnson, G. Shen, R. Bittl, D. Stehlik, P.R. Chitnis, J.H. Golbeck, J. Biol. Chem. 275, 8531 (2000)CrossRefGoogle Scholar
  42. 42.
    S. Mula, A. Savitsky, K. Möbius, W. Lubitz, J.H. Golbeck, M.D. Mamedov, A.Y. Semenov, A. van der Est, Photochem. Photobiol. Sci. 11, 946 (2012)CrossRefGoogle Scholar
  43. 43.
    G.E. Milanovsky, V.V. Ptushenko, J.H. Golbeck, A.Y. Semenov, D.A. Cherepanov, Biochim. Biophys. Acta Bioenerg. 1837, 1472 (2014)CrossRefGoogle Scholar
  44. 44.
    T.E. Mølholt, R. Mantovan, H.P. Gunnlaugsson, D. Naidoo, S. Ólafsson, K. Bharuth-Ram, M. Fanciulli, K. Johnston, Y. Kobayashi, G. Langouche, H. Masenda, R. Sielemann, G. Weyer, H.P. Gíslason, Hyperfine Interact. 197, 89 (2010)ADSCrossRefGoogle Scholar
  45. 45.
    N. Bloembergen, S. Shapiro, P.S. Pershan, J.O. Artman, Phys. Rev. 114, 445 (1959)ADSCrossRefGoogle Scholar
  46. 46.
    T. Li, M.B. Tracka, S. Uddin, J. Casas-Finet, D.J. Jacobs, D.R. Livesay, PLoS One 9, 3 (2014)Google Scholar
  47. 47.
    B. Van den Burg, V.G. Eijsink, Curr. Opin. Biotechnol. 13, 333 (2002)CrossRefGoogle Scholar
  48. 48.
    J. Hollien, S. Marqusee, Biochemistry 38, 3831 (1999)CrossRefGoogle Scholar
  49. 49.
    C. Olsson, H. Jansson, T. Youngs, J. Swenson, J. Phys Chem. B 120, 12669 (2016)CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Zavoisky Physical-Technical InstituteFRC Kazan Scientific Center of RASKazanRussia
  2. 2.A.N. Belozersky Institute of Physical–Chemical BiologyMoscowRussia
  3. 3.Department of PhysicsFree University BerlinBerlinGermany

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