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Biochemistry (Moscow)

, Volume 75, Issue 4, pp 412–422 | Cite as

Femtosecond stage of electron transfer in reaction centers of the triple mutant SL178K/GM203D/LM214H of Rhodobacter sphaeroides

  • A. G. YakovlevEmail author
  • T. A. Shkuropatova
  • V. A. Shkuropatova
  • V. A. Shuvalov
Accelerated Publication

Abstract

Coherent processes in an initial phase of charge transfer in reaction centers (RCs) of the triple mutant S(L178)K/G(M203)D/L(M214)H of Rhodobacter sphaeroides were investigated by difference (light — dark) absorption spectroscopy with 18 fsec time resolution. Electron transfer in the B cofactor branch is activated in this mutant, while the A-branch electron transfer is slowed in comparison with native RCs of Rba. sphaeroides. A bulk of absorption difference spectra was analyzed in the 940–1060 nm range (stimulated emission of excited bacteriochlorophyll dimer P* and absorption of bacteriochlorophyll anions B A and β, where β is a bacteriochlorophyll substituting the native bacteriopheophytin HA) and in the 735–775 nm range (bleaching of the absorption band of the bacteriopheophytin HB in the B-branch) in the −0.1 to 4 psec range of delays with respect to the moment of photoexcitation of P at 870 nm. Spectra were measured at 293 and 90 K. The kinetics of P* stimulated emission at 940 nm shows its decay with a time constant of ∼14 psec at 90 K and ∼18 psec at 293 K, which is accompanied by oscillations with a frequency of ∼150 cm−1. A weak absorption band is found at 1018 nm that is formed ∼100 fsec after excitation of P and reflects the electron transfer from P* to β and/or BA with accumulation of the P+β and/or P+B A states. The kinetics of ΔA at 1018 nm contains the oscillations at ∼150 cm−1 and distinct low-frequency oscillations at 20–100 cm−1; also, the amplitude of the oscillations at 150 cm−1 is much smaller at 293 than at 90 K. The oscillations in the kinetics of the 1018 nm band do not contain a 32 cm−1 mode that is characteristic for native Rba. sphaeroides RCs having water molecule HOH55 in their structure. The ΔA kinetics at 751 nm reflects the electron transfer to HB with formation of the P+H B state. The oscillatory part of this kinetics has the form of a single peak with a maximum at ∼50 fsec completely decaying at ∼200 fsec, which might reflect a reversible electron transfer to the B-branch. The results are analyzed in terms of coherent nuclear wave packet motion induced in the P* excited state by femtosecond light pulses, of an influence of the incorporated mutations on the mutual position of the energy levels of charge separated states, and of the role of water HOH55 in the dynamics of the initial electron transfer.

Key words

photosynthesis charge separation reaction center wave packet electron transfer 

Abbreviations

ΔA

absorption changes (light minus dark)

BChl

bacteriochlorophyll

BA and BB

monomeric BChl in A- and B-branch, respectively

BPheo

bacteriopheophytin

HA and HB

BPheo in A- and B-branch, respectively

P

primary electron donor, dimer BChl

PA and PB

BChl molecules forming P

QA and QB

primary and secondary quinone, respectively

RC

reaction center

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References

  1. 1.
    Deisenhofer, J., Epp, O., Miki, K., Huber, R., and Michel, H. (1984) J. Mol. Biol., 180, 385–398.CrossRefPubMedGoogle Scholar
  2. 2.
    Allen, J. P., Feher, G., Yeates, T. O., Komiya, H., and Rees, D. C. (1987) Proc. Natl. Acad. Sci. USA, 84, 5730–5734.CrossRefPubMedGoogle Scholar
  3. 3.
    Shuvalov, V. A. (2000) Transformation of Solar Energy in Primary Act of Charge Separation in Reaction Centers of Photosynthesis [in Russian], Nauka, Moscow.Google Scholar
  4. 4.
    Kennis, J. T. M., Shkuropatov, A. Ya, van Stokkum, I. H. M., Gast, P., Hoff, A. J., Shuvalov, V. A., and Aartsma, T. J. (1997) Biochemistry, 36, 16231–16238.CrossRefPubMedGoogle Scholar
  5. 5.
    Carter, B., Boxer, S. G., Holten, D., and Kirmaier, C. (2009) Biochemistry, 48, 2571–2573.CrossRefPubMedGoogle Scholar
  6. 6.
    Heller, B. A., Holten, D., and Kirmaier, C. (1995) Science, 269, 940–945.CrossRefPubMedGoogle Scholar
  7. 7.
    Marcus, R. A. (1988) in The Photosynthetic Bacterial Reaction Center: Structure and Dynamics (Breton, J., and Vermeglio, A., eds.) Plenum Press, New York-London, pp. 389–398.Google Scholar
  8. 8.
    Larsson, S., and Ivashin, N. V. (1999) J. Appl. Spectrosc., 66, 539–543.CrossRefGoogle Scholar
  9. 9.
    Stowell, M. H. B., McPhillips, T. M., Rees, D. C., Soltis, S. M., Abresch, E., and Feher, G. (1997) Science, 276, 812–816.CrossRefPubMedGoogle Scholar
  10. 10.
    Vos, M. H., Rappaport, F., Lambry, J.-C., Breton, J., and Martin, J.-L. (1993) Nature, 363, 320–325.CrossRefGoogle Scholar
  11. 11.
    Stanley, R. J., and Boxer, S. G. (1995) J. Phys. Chem., 99, 859–863.CrossRefGoogle Scholar
  12. 12.
    Yakovlev, A. G., Shkuropatov, A. Ya., and Shuvalov, V. A. (2000) FEBS Lett., 466, 209–212.CrossRefPubMedGoogle Scholar
  13. 13.
    Yakovlev, A. G., Shkuropatov, A. Ya., and Shuvalov, V. A. (2002) Biochemistry, 41, 2667–2674.CrossRefPubMedGoogle Scholar
  14. 14.
    Yakovlev, A. G., Shkuropatov, A. Ya., and Shuvalov, V. A. (2002) Biochemistry, 41, 14019–14027.CrossRefPubMedGoogle Scholar
  15. 15.
    Streltsov, A. M., Vulto, S. I. E., Shkuropatov, A. Ya., Hoff, A. J., Aartsma, T. J., and Shuvalov, V. A. (1998) J. Phys. Chem. B, 102, 7293–7298.CrossRefGoogle Scholar
  16. 16.
    Vos, M. H., Rischel, C., Jones, M. R., and Martin, J.-L. (2000) Biochemistry, 39, 8353–8361.CrossRefPubMedGoogle Scholar
  17. 17.
    Yakovlev, A. G., Vasilieva, L. G., Shkuropatov, A. Ya., Bolgarina, T. I., Shkuropatova, V. A., and Shuvalov, V. A. (2003) J. Phys. Chem. A, 107, 8330–8338.CrossRefGoogle Scholar
  18. 18.
    Potter, J. A., Fyfe, P. K., Frolov, D., Wakeham, M. C., van Grondelle, R., Robert, B., and Jones, M. R. (2005) J. Biol. Chem., 280, 27155–27164.CrossRefPubMedGoogle Scholar
  19. 19.
    Yakovlev, A. G., Jones, M. R., Potter, J. A., Vasilieva, L. G., Shkuropatov, A. Y., and Shuvalov, V. A. (2005) Chem. Phys., 319, 297–307.CrossRefGoogle Scholar
  20. 20.
    Fyfe, P. K., Ridge, J. P., McAuley, K. E., Cogdell, R. J., Isaacs, N. W., and Jones, M. R. (2000) Biochemistry, 39, 5953–5960.CrossRefPubMedGoogle Scholar
  21. 21.
    Williams, J. C., Alden, R. G., Murchison, H. A., Peloquin, J. M., Woodbury, N. W., and Allen, J. P. (1992) Biochemistry, 31, 11029–11037.CrossRefPubMedGoogle Scholar
  22. 22.
    Shuvalov, V. A., and Yakovlev, A. G. (2003) FEBS Lett., 540, 26–34.CrossRefPubMedGoogle Scholar
  23. 23.
    Kirmaier, C., Weems, D., and Holten, D. (1999) Biochemistry, 38, 11516–11530.CrossRefPubMedGoogle Scholar
  24. 24.
    Roberts, J. A., Holten, D., and Kirmaier, C. (2001) J. Phys. Chem. B, 105, 5575–5584.CrossRefGoogle Scholar
  25. 25.
    Kirmaier, C., and Holten, D. (2009) J. Phys. Chem. B, 113, 1132–1142.CrossRefPubMedGoogle Scholar
  26. 26.
    Kee, H. L., Laible, P. D., Bautista, J. A., Hanson, D. K., Holten, D., and Kirmaier, C. (2006) Biochemistry, 45, 7314–7322.CrossRefPubMedGoogle Scholar
  27. 27.
    Chuang, J. I., Boxer, S. G., Holten, D., and Kirmaier, C. (2008) J. Phys. Chem. B, 112, 5487–5499.CrossRefPubMedGoogle Scholar
  28. 28.
    Kirmaier, C., Bautista, J. A., Laible, P. D., Hanson, D. K., and Holten, D. (2005) J. Phys. Chem. B, 109, 24160–24172.CrossRefPubMedGoogle Scholar
  29. 29.
    Yakovlev, A. G., Shkuropatova, T. A., Vasilieva, L. G., Shkuropatov, A. Y., Gast, P., and Shuvalov, V. A. (2006) Biochim. Biophys. Acta, 1757, 369–379.CrossRefPubMedGoogle Scholar
  30. 30.
    Yakovlev, A. G., Shkuropatova, T. A., Vasilieva, L. G., Shkuropatov, A. Y., and Shuvalov, V. A. (2008) J. Bioinform. Comput. Biol., 6, 643–666.CrossRefPubMedGoogle Scholar
  31. 31.
    Paddock, M. L., Rongey, S. H., Feher, G., and Okamura, M. Y. (1989) Proc. Natl. Acad. Sci. USA, 86, 6602–6606.CrossRefPubMedGoogle Scholar
  32. 32.
    De Boer, A. L., Neerken, S., de Wijn, R., Permentier, H. P., Gast, P., Vijgenboom, E., and Hoff, A. J. (2002) Photosynth. Res., 71, 221–239.CrossRefPubMedGoogle Scholar
  33. 33.
    Goldsmith, J. O., and Boxer, S. G. (1996) Biochim. Biophys. Acta, 1276, 171–175.CrossRefGoogle Scholar
  34. 34.
    Shuvalov, V. A., Shkuropatov, A. Ya., Kulakova, S. M., Ismailov, M. A., and Shkuropatova, V. A. (1986) Biochim. Biophys. Acta, 849, 337–348.CrossRefGoogle Scholar
  35. 35.
    Heller, B. A., Holten, D., and Kirmaier, C. (1995) Biochemistry, 34, 5294–5302.CrossRefPubMedGoogle Scholar
  36. 36.
    Kirmaier, C., Laporte, L., Schenck, C. C., and Holten, D. (1995) J. Phys. Chem., 99, 8910–8917.CrossRefGoogle Scholar
  37. 37.
    Heller, B. A., Holten, D., and Kirmaier, C. (1996) Biochemistry, 35, 15418–15427.CrossRefPubMedGoogle Scholar
  38. 38.
    Alden, R. G., Parson, W. W., Chu, Z., and Warshel, A. (1995) J. Am. Chem. Soc., 117, 12284–12302.CrossRefGoogle Scholar
  39. 39.
    Czarnecki, K., Kirmaier, C., Holten, D., and Bocian, D. (1999) J. Phys. Chem. A, 103, 2235–2246.CrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2010

Authors and Affiliations

  • A. G. Yakovlev
    • 1
    Email author
  • T. A. Shkuropatova
    • 2
  • V. A. Shkuropatova
    • 3
  • V. A. Shuvalov
    • 1
    • 3
  1. 1.Department of Photobiophysics, Belozersky Institute of Physico-Chemical BiologyLomonosov Moscow State UniversityMoscowRussia
  2. 2.Department of Biophysics, Huygens LaboratoryLeiden UniversityLeidenThe Netherlands
  3. 3.Institute of Basic Biological ProblemsRussian Academy of SciencesPushchino, Moscow RegionRussia

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