Photosynthetic Electron Transfer Controlled by Protein Relaxation: Analysis by Langevin Stochastic Approach

Abstract

Relaxation processes in proteins range in time from picoseconds to seconds. Correspondingly, biological electron transfer (ET) could be controlled by slow protein relaxation. We used the Langevin stochastic approach to describe this type of ET dynamics. Two different types of kinetic behavior were revealed, namely: oscillating ET (that could occur at picoseconds) and monotonically relaxing ET. On a longer time scale, the ET dynamics can include two different kinetic components. The faster one reflects the initial, nonadiabatic ET, whereas the slower one is governed by the medium relaxation. We derived a simple relation between the relative extents of these components, the change in the free energy (DeltaG), and the energy of the slow reorganization Lambda. The rate of ET was found to be determined by slow relaxation at -DeltaG < or = Lambda. The application of the developed approach to experimental data on ET in the bacterial photosynthetic reaction centers allowed a quantitative description of the oscillating features in the primary charge separation and yielded values of Lambda for the slower low-exothermic ET reactions. In all cases but one, the obtained estimates of Lambda varied in the range of 70-100 meV. Because the vast majority of the biological ET reactions are only slightly exothermic (DeltaG > or = -100 meV), the relaxationally controlled ET is likely to prevail in proteins.

Spectral exhibition of electron-vibrational relaxation in P* state of Rhodobacter sphaeroides reaction centers

“…The classical stochastic Langevin equation together with Marcus theory and the approach of two vibrational modes was used to calculate the rate of primary electron transfer, controlled by protein relaxation (Cherepanov et al 2001). A lot of experimental and theoretical studies have clearly shown that, in real RCs, many vibrational modes contribute to primary events, and that these events occur on a timescale comparable with the characteristic time of vibrational thermalization (for related reviews see Shuvalov 2000;Yakovlev 2013;Parson and Warshel 2009).…”

Three-dimensional representations of photo-induced electron transfer rates in pyrene-(CH2)n-N,N′-dimethylaniline systems obtained by three electron transfer theories

“…Theoretical elucidations of the oscillatory behavior have been also worked [23,[28][29][30]. These theories in the CT complexes may relate to BJ theory in ET, but not to M theory and KM theory.…”

Ubiquinone reduction in the photosynthetic reaction centre of Rhodobacter sphaeroides: interplay between electron transfer, proton binding and flips of the quinone ring

“…Initially, it has been proposed that the gating event is a transition of the ubiquinone between its 'inactive' distal and 'active' proximal positions [6]. Based on the similarities between the above described fast and slow components of ET and PT respectively, we have speculated that the ET reaction is controlled not by one, but by two relaxation/gating modes [8]. In those RCs, where Q B was initially in the proximal position, the electron spillover from Q A ᭹− to Q B could be driven by proton redistribution that selectively stabilized the Q B ᭹− state (τ ∼ 100 µs and E a ∼ 10-20 kJ/mol).…”

“…In those RCs, where Q B was initially in the proximal position, the electron spillover from Q A ᭹− to Q B could be driven by proton redistribution that selectively stabilized the Q B ᭹− state (τ ∼ 100 µs and E a ∼ 10-20 kJ/mol). If Q B was initially in the distal position, it had to be brought into the proximal position (τ ∼ 500 µs and E a ∼ 60 kJ/mol) before the ET and PT could take place [8]. In several recent papers, the role of Ser-L223 in the Q B ᭹− stabilization has been discussed [12,49,50].…”

“…[2][3][4][5][6][7][8]). The core of a bacterial RC is formed by two membrane subunits L and M that are 'capped' by the H subunit.…”