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Femtosecond relaxation processes in Rhodobacter sphaeroides reaction centers

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Abstract

Energy relaxation was studied with difference femtosecond spectroscopy in reaction centers of the YM210L mutant of the purple photosynthetic bacterium Rhodobacter sphaeroides at low temperature (90 K). A dynamical long-wavelength shift of stimulated emission of the excited state of the bacteriochlorophyll dimer P was found, which starts simultaneously with P* formation and is accompanied by a change in the spectral shape of this emission. The characteristic value of this shift was about 30 nm, and the characteristic time about 200 fs. Difference kinetics ΔA measured at fixed wavelengths demonstrate the femtosecond shift of the P* stimulated emission appearing as a dependence of these kinetics on wavelength. We found that the reported long-wavelength shift can be explained in terms of electron-vibrational relaxation of the P* excited state with time constants of vibrational and electronic relaxation of 100 and 50 fs, respectively. Alternative mechanisms of the dynamical shift of the P* stimulated emission spectrum are also discussed in terms of energy redistribution between vibrational modes or coherent excitation of the modes.

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Abbreviations

ΔA :

absorption change (illumination minus darkness)

BA and BB :

monomeric bacteriochlorophylls in A and B chains, respectively

HA and HB :

bacteriopheophytins in A and B chains, respectively

P:

bacteriochlorophyll dimer

PA and PB :

bacteriochlorophyll molecules that make up P

QA and QB :

primary and secondary quinones, respectively

RC:

reaction center

Rba. :

Rhodobacter

References

  1. Yakovlev, A. G., and Shuvalov, V. A. (2016) Physical stage of charge separation during photosynthesis, Adv. Phys. Sci., 126, 597–625.

    Google Scholar 

  2. Lockhart, D. J., and Boxer, S. G. (1987) Magnitude and direction of the change in dipole moment associated with excitation of the primary electron donor in Rhodopseudomonas sphaeroides reaction centers, Biochemistry, 26, 664–668.

    Article  CAS  Google Scholar 

  3. Philipson, K. D., and Sauer, K. (1973) Comparative study of the circular dichroism spectra of reaction centers from several photosynthetic bacteria, Biochemistry, 12, 535–539.

    Article  CAS  PubMed  Google Scholar 

  4. Van Brederode, M. E., and Van Grondelle, R. (1999) New and unexpected routes for ultrafast electron transfer in photosynthetic reaction centers, FEBS Lett., 455, 1–7.

    Article  PubMed  Google Scholar 

  5. Cherepy, N. J., Shreve, A. P., Moore, L. J., Franzen, S., Boxer, S. G., and Mathies, R. A. (1994) Near-infrared resonance Raman spectroscopy of the special pair and the accessory bacteriochlorophylls in photosynthetic reaction centers, J. Phys. Chem., 98, 6023–6029.

    Article  CAS  Google Scholar 

  6. Cherepy, N. J., Shreve, A. P., Moore, L. J., Boxer, S. G., and Mathies, R. A. (1997) Temperature dependence of the Qy resonance Raman spectra of bacteriochlorophylls, the primary electron donor, and bacteriopheophytins in the bacterial photosynthetic reaction center, Biochemistry, 36, 8559–8566.

    Article  CAS  PubMed  Google Scholar 

  7. Cherepy, N. J., Shreve, A. P., Moore, L. J., Boxer, S. G., and Mathies, R. A. (1997) Electronic and nuclear dynamics of the accessory bacteriochlorophylls in bacterial photosynthetic reaction centers from resonance Raman intensities, J. Phys. Chem., 101, 3250–3260.

    Article  CAS  Google Scholar 

  8. Klevanik, A. V., Ganago, A. O., Shkuropatov, A. Ya., and Shuvalov, V. A. (1988) Electron-phonon and vibronic structure of absorption spectra of the primary electron donor in reaction centers of Rhodopseudomonas viridis, Rhodobacter sphaeroides and Chloroflexus aurantiacus at 1.7-70K, FEBS Lett., 237, 61–64.

    Article  CAS  Google Scholar 

  9. Streltsov, A. M., Vulto, S. I. E., Shkuropatov, A. Ya., Hoff, A. J., Aartsma, T. J., and Shuvalov, V. A. (1998) BA and BB absorbance perturbations induced by coherent nuclear motions in reaction centers from Rhodobacter sphaeroides upon 30-femtosecond excitation of the primary donor, J. Phys. Chem., 102, 7293–7298.

    Article  CAS  Google Scholar 

  10. Vos, M. H., Jones, M. R., Hunter, C. N., Breton, J., Lambry, J.-C., and Martin, J.-L. (1994) Coherent dynamics during the primary electron-transfer reaction in membrane-bound reaction centers of Rhodobacter sphaeroides, Biochemistry, 33, 6750–6757.

    Article  CAS  PubMed  Google Scholar 

  11. Yakovlev, A. G., Shkuropatov, A. Ya., and Shuvalov, V. A. (2002) Nuclear wavepacket motion between P* and P+BA − potential surfaces with a subsequent electron transfer to HA in bacterial reaction centers at 90 K. Electron transfer pathway, Biochemistry, 41, 14019–14027.

    Article  CAS  PubMed  Google Scholar 

  12. Shuvalov, V. A., Klevanik, A. V., Ganago, A. O., Shkuropatov, A. Ya., and Gubanov, V. S. (1988) Burning of a narrow spectral hole at 1.7 K in the absorption band of the primary electron donor of Rhodopseudomonas viridis reaction centers with blocked electron transfer, FEBS Lett., 237, 57–60.

    Article  CAS  Google Scholar 

  13. Plato, M., Lendzian, F., Lubitz, W., and Mobius, K. (1992) Molecular orbital study of electronic asymmetry in primary donors of bacterial reaction centers, in The Photosynthetic Bacterial Reaction Center II: Structure, Spectroscopy, and Dynamics (Breton, J., and Vermeglio, A., eds.) Plenum, New York, pp. 109–118.

    Chapter  Google Scholar 

  14. Hamm, P., and Zinth, W. (1995) Ultrafast initial reaction in bacterial photosynthesis revealed by femtosecond infrared spectroscopy, J. Phys. Chem., 99, 13537–13544.

    Article  CAS  Google Scholar 

  15. Lyle, P. A., Kolaczkowski, S. V., and Small, G. J. (1993) Photochemical hole-burned spectra of protonated and deuterated reaction centers of Rhodobacter sphaeroides, J. Phys. Chem., 97, 6924–6933.

    Article  CAS  Google Scholar 

  16. Khatypov, R. A., Khmelnitskiy, A. Yu., Khristin, A. M., Fufina, T. Yu., Vasilieva, L. G., and Shuvalov, V. A. (2012) Primary charge separation within P870* in wild type and heterodimer mutants in femtosecond time domain, Biochim. Biophys. Acta, 1817, 1392–1398.

    Article  CAS  PubMed  Google Scholar 

  17. Warshel, A., and Parson, W. W. (1987) Spectroscopic properties of photosynthetic reaction centers. 1. Theory, J. Am. Chem. Soc., 109, 6143–6152.

    Article  CAS  Google Scholar 

  18. Parson, W. W., and Warshel, A. (2004) Dependence of photosynthetic electron-transfer kinetics on temperature and energy in a density-matrix model, J. Phys. Chem., 108, 10474–10483.

    Article  CAS  Google Scholar 

  19. Renger, T. (2004) Theory of optical spectra involving charge transfer states: dynamic localization predicts a temperature dependent optical band shift, Phys. Rev. Lett., 93, 1–4.

    Article  Google Scholar 

  20. Yakovlev, A. G., Vasilieva, L. G., Shkuropatov, A. Ya., Bolgarina, T. I., Shkuropatova, V. A., and Shuvalov, V. A. (2003) Mechanism of charge separation and stabilization of separated charges in reaction centers of Chloroflexus aurantiacus and of YM210W(L) mutants of Rhodobacter sphaeroides excited by 20 fs pulses at 90 K, J. Phys. Chem., 107, 8330–8338.

    Article  CAS  Google Scholar 

  21. Struve, W. S. (1995) Vibrational equilibration in absorption difference spectra of chlorophyll a, Biophys. J., 69, 2739–2744.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Yakovlev, A. G., and Shuvalov, V. A. (2015) Spectral exhibition of electron-vibrational relaxation in P* state of Rhodobacter sphaeroides reaction centers, Photosynth. Res., 125, 9–22.

    Article  CAS  PubMed  Google Scholar 

  23. Parshakov, A. N. (2010) Physics of Oscillations [in Russian], Perm State University, Perm, p. 302.

    Google Scholar 

  24. Milanovsky, G. E., Shuvalov, V. A., Semenov, A. Yu., and Cherepanov, D. A. (2015) Elastic vibrations in the photosynthetic bacterial reaction center coupled to the primary charge separation: implications from molecular dynamics simulations and stochastic Langevin approach, J. Phys. Chem., 119, 13656–13667.

    Article  CAS  Google Scholar 

  25. Eisenmayer, T. J., De Groot, H. J. M., Van de Wetering, E., Neugebauer, J., and Buda, F. (2012) Mechanism and reaction coordinate of directional charge separation in bacterial reaction centers, J. Phys. Chem. Lett., 3, 694–697.

    Article  CAS  PubMed  Google Scholar 

  26. Eisenmayer, T. J., Lasave, J. A., Monti, A., De Groot, H. J. M., and Buda, F. (2013) Proton displacements coupled to primary electron transfer in the Rhodobacter sphaeroides reaction center, J. Phys. Chem., 117, 11162–11168.

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University, 119991, Moscow, Russia

    A. G. Yakovlev & V. A. Shuvalov

  2. Institute of Basic Biological Problems, Russian Academy of Sciences, 142290, Pushchino, Moscow Region, Russia

    V. A. Shuvalov

Authors
  1. A. G. Yakovlev
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  2. V. A. Shuvalov
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Correspondence to A. G. Yakovlev.

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Original Russian Text © A. G. Yakovlev, V. A. Shuvalov, 2017, published in Biokhimiya, 2017, Vol. 82, No. 8, pp. 1176-1187.

Originally published in Biochemistry (Moscow) On-Line Papers in Press, as Manuscript BM17-158, July 17, 2017.

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Yakovlev, A.G., Shuvalov, V.A. Femtosecond relaxation processes in Rhodobacter sphaeroides reaction centers. Biochemistry Moscow 82, 906–915 (2017). https://doi.org/10.1134/S0006297917080053

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  • DOI: https://doi.org/10.1134/S0006297917080053

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