Biopolym. Cell. 2010; 26(4):286-294.
Molecular Biophysics
Deceleration of the electron transfer reaction in the photosynthetic reaction centre as a manifestation of its structure fluctuations
1Kharkyanen V. N., 1Barabash Yu. M., 1Berezetskaya N. M., 1Olenchuk M. V., 2Knox P. P., 3Christophorov L. N.
  1. Institute of Physics, NAS of Ukraine
    46, Prospect Nauki, Kyiv, Ukraine, 03028
  2. M. V. Lomonosov Moscow State University
    Leninskie Gory, Moscow, Russian Federation, 119991
  3. Bogolyubov Institute for Theoretical Physics, NAS of Ukraine
    14 b Metrologichna Str., Kyiv, Ukraine, 03680

Abstract

Aim. To extract information on the nature of protein structural relaxation from the kinetics of electron transfer reaction in the photosynthetic reaction centre (RC). Methods. The kinetic curves obtained by absorption spectroscopy are processed by a maximum entropy method to get the spectrum of relaxation times. Results. A series of distinctive peaks of this spectrum in the interval from 0.1 s to hundreds of seconds is revealed. With the time of exposure of the sample to actinic light increasing, the positions of the peak maxima grow linearly. Conclusions. Theoretical analysis of these results reveals the formation of several structural states of the RC protein. Remarkably, in each of these states the slow reaction kinetics follow the same fractional power law that reflects the glass-like properties of the protein.
Keywords: protein structure relaxation, nonexponential kinetics, time-dependent reaction barrier, primary reactions of photosynthesis

References

[1] Karplus M. Aspects of protein reaction dynamics: Deviations from simple behavior. J. Phys. Chem. 2000 104, N 1 P. 11–27.
[2] Agmon N., Doster W., Post F. The transition from inhomogeneous to homogeneous kinetics in CO binding to myoglobin. Biophys. J 1994 66, N 5:1612–1622.
[3] Jackson T. A., Lim M., Anfinrud P. A. Complex nonexponential relaxation in myoglobin after photodissociation of MbCO: measurement and analysis from 2 ps to 56 s Chem. Phys 1994 180, N 2–3:131–140.
[4] Goushcha A. O., Dobrovolskii A. A., Kapoustina M. T., Privalko A. V., Kharkyanen V. N. New physical phenomenon of dynamical self-organization in molecular electron transfer systems Phys. Lett. A 1994 191, N 5–6:393–397.
[5] Abgaryan G. A., Christophorov L. N., Goushcha A. O., Holzwarth A. R., Kharkyanen V. N., Knox P. P., Lukashev E. A. Effects of mutual influence of photoinduced electron transitions and slow structural rearrangements in bacterial photosynthetic reaction centers J. Biol. Phys 1998 24, N 1:1–17.
[6] Zwanzig R. Rate processes with dynamic disorder Acc. Chem. Res 1990 23, N 5:148–152.
[7] Plonka A. Dispersive kinetics. Ann. Rep. Progr. Chem. C 2001 97, N 1:91–147.
[8] Agmon N. Conformational cycle of a single working enzyme J. Phys.Chem. B 2000 104, N 32:7830–7834.
[9] Christophorov L. N., Kharkyanen V. N. Discrete versus continuous schemes of conformational regulation. Chem. Phys. Res. J. 2007; 1, N 1:1–14.
[10] Frauenfelder H., Wolynes P. G., Austin R. H. Biological physics Rev. Mod. Phys 1999 71, N 2:S419–S430.
[11] Palmer R. G., Stein D. L., Abrahams E., Anderson P. W. Models of hierarchically constrained dynamics for glassy relaxation Phys. Rev. Lett 1984 53, N 10:958–961.
[12] Berlin Yu. A., Burin A. L., Siebbeles L. D. A., Ratner M. A. Conformationally gated rate processes in biological macromolecules J. Phys. Chem. A 2001 105, N 23:5666–5678.
[13] Frauenfelder H., Wolynes P. G. Biomolecules: Where the physics of simplicity and complexity meet Phys. Today 1994 47, N 2:58–64.
[14] Sokolov I. M., Klafter J., Blumen A. Fractional kinetics Phys. Today 2002 55, N 11:48–54.
[15] Berlin Yu. A., Fisher S. F., Chekunaev N. I., Goldanskii V. I. Non-exponential non-Arrhenius relaxation in the course of CO rebinding to heme proteins Chem. Phys 1995 200, N 3:369–385.
[16] Hoff A. J., Deisenhofer J. Photophysics of photosynthesis. Structure and spectroscopy of reaction centers of purple bacteria Phys. Rep 1997 287, N 1–2:1–247.
[17] Stowell M. H. B., McPhillips T. M., Rees D. S., Soltis S., Abresh E., Feher G. Light-induced structural changes and the mechanism of electron/proton transfer in the photosynthetic reaction center Science 1997 276, N 5313:812–816.
[18] Okamura M. Y., Feher G. Proton transfer in reaction centers from photosynthetic bacteria Ann. Rev. Biochem 1992 61, N 1:861–896.
[19] Barabash Yu. M., Berezetskaya N. M., Christophorov L. N., Goushcha A. O., Kharkyanen V. N. Effects of structural memory in protein reactions J. Chem. Phys 2002 116, N 10:4339–4352.
[20] Goushcha A. O., Manzo A. J., Scott G. W., Christophorov L. N., Knox P. P., Barabash Yu. M., Kapoustina M. T., Berezetska N. M., Kharkyanen V. N. Self-regulation phenomena applied to bacterial reaction centers. Nonequilibrium adiabatic potential: dark and light conformations revisited Biophys. J 2003 84, N 2:1146–1160.
[21] Christophorov L. N., Kharkyanen V. N. Synergetic mechanisms of structural regulation of the electron transfer and other reactions of biological macromolecules Chem. Phys 2005 319, N 1–3:330–341.
[22] Lukashev E. P., Knox P. P., Rubin A. B., Olenchuk M. V., Barabash Yu. M., Berezetskaya N. M., Kharkyanen V. N. The analysis of the kinetics of dark recombination of photodivided charges in the Rhodobacter sphaeroides photosynthetic reaction centers using the method of relaxation time constant distribution. Biofizika. 2009;54(3):425-33.
[23] Austin R. H., Beeson K., Eisenstein L., Frauenfelder H., Gunsalus I. C., Marshall V. P. Activation energy spectrum of a biomolecule: Photodissociation of carbonmonoxy myoglobin at low temperatures. Phys. Rev. Lett 1974 32, N 8 P. 403–405.
[24] Kleinfeld D., Okamura M. Y., Feher G. Electron transfer kinetics in photosynthetic reaction centers cooled to cryogenic temperatures in the charge-separated states: Evidence for light-induced structural changes Biochemistry 1984 23, N 24:5780–5786.
[25] Bateman H., Erdelyi A. Tables of integral transforms NewYork: McGraw-Hill Inc., 1954 Vol. 1 343 p.
[26] Berlin Yu. A., Siebbeles L. D. A. Energy relaxation during thermally activated diffusion along one-dimensional chains with site disorder Chem. Phys. Lett 1998 291, N 1–2 P. 85–93.