Electron-transfer kinetics in photosynthetic reaction centers cooled to cryogenic temperatures in the charge-separated state: evidence for light-induced structural changes

Abstract

We have compared the electron-transfer kinetics in reaction centers (RCs) cooled in the dark with those cooled under illumination (i.e., in the charge-separated state). Large differences between the two cases were observed. We interpreted these findings in terms of light-induced structural changes. The kinetics of charge recombination D+QA-----DQA in RCs containing one quinone were modeled in terms of a distribution of donor-acceptor electron-transfer distances. For RCs cooled under illumination the distribution broadened and shifted to larger distances compared to the distribution for RCs cooled in the dark. The model accounts for the nonexponential decay observed at low temperatures [McElroy, J. D., Mauzerall, D. C., & Feher, G. (1974) Biochim. Biophys. Acta 333, 261-277; Morrison, L.E., & Loach, P.A. (1978) Photochem. Photobiol. 27, 751-757]. A possible physiological role of the structural changes is an enhanced charge stabilization. For RCs with two quinones, the recombination kinetics D+QAQB-----DQAQB were found to be strongly temperature dependent. This was interpreted in terms of temperature-dependent transitions between structural states [Agmon, N., & Hopfield, J.J. (1983) J. Chem. Phys. 78, 6947-6959]. This interpretation requires that these transitions occur at cryogenic temperatures on a time scale t greater than or approximately 10(3) s. The electron transfer from QA- to QB was found to not take place in RCs cooled in the dark (tau ABdark greater than 10(-1) s). In RCs cooled under illumination, we found tau ABlight less than 10(-3) s. We suggest the possibility that the drastic decrease in tau AB observed in RCs cooled under illumination is due to the trapping of a proton near QB-.

Trapped Conformational States of Semiquinone (D+•QB-•) Formed by B-Branch Electron Transfer at Low Temperature in Rhodobacter sphaeroides Reaction Centers

“…In this study, electron transfer rates were measured for RCs frozen in different states at cryogenic temperature (5,43,63,64). s with a fraction that did not recover, attributed to samples that may have lost the electron on the acceptor side.…”

“…The existence of different protein conformations with very different characteristics was shown by the inhibition of electron transfer from Q A −• to Q B in RCs frozen in the dark (4,5); this was in contrast to viable electron transfer in RCs frozen under illumination. Subsequently several studies to investigate these conformers (i.e.…”

“…sphaeroides is an example of a gated electron transfer process. The reaction rate was shown to depend upon protein conformation based on changes of electron transfer upon freezing to cryogenic temperatures (4,5), crosslinking of the protein subunits (6) and embedding the protein in a glassy matrix (7) or PVA film (8). Furthermore, quinone (Q A ) substitution studies showed that the observed rate of electron transfer was independent of the driving force indicating a conformational gating mechanism (9).…”

“…The configurations of the protein before and after reduction were trapped by freezing RCs to cryogenic temperature as has been done previously (4,5). Since in the native RC Q B −• cannot be formed by electron transfer from Q A −• in samples frozen in the dark (5, 43), we developed a modified RC (Fig.…”

Dynamics of radiationless transitions in large molecular systems: A Franck–Condon-based method accounting for displacements and rotations of all the normal coordinates

“…Here, we will consider the problem of long range ET between the primary (Q A ) and the secondary quinone (Q B ) in bacterial photosynthetic reaction centres, because, as for pyrazine, this biochemical system has been well characterized both as concerns the three-dimensional structure, [56][57][58] as well as the thermodynamics and the kinetics of ET. [59][60][61][62][63][64] We will draw attention only to the internal dynamics of the two cofactors leading to ET, thus considering only an isolated, solvent free, supermolecule constituted by the two redox cofactors and the interposed bridge. The spatial arrangement found in the X-ray structure of Rhodobacter sphaeroides frozen under illumination, 58 shown in figure 4, has been adopted.…”