Inverted region in the reaction of the quinone reduction in the A-site of photosystem I from cyanobacteria.

Photosystem I from the menB strain of Synechocystis sp. PCC 6803 containing foreign quinones in the A sites was used for studying the primary steps of electron transfer by pump-probe femtosecond laser spectroscopy. The free energy gap (- ΔG) of electron transfer between the reduced primary acceptor A and the quinones bound in the A site varied from 0.12 eV for the low-potential 1,2-diamino-anthraquinone to 0.88 eV for the high-potential 2,3-dichloro-1,4-naphthoquinone, compared to 0.5 eV for the native phylloquinone. It was shown that the kinetics of charge separation between the special pair chlorophyll P and the primary acceptor A was not affected by quinone substitutions, whereas the rate of A → A electron transfer was sensitive to the redox-potential of quinones: the decrease of - ΔG by 400 meV compared to the native phylloquinone resulted in a ~ fivefold slowing of the reaction The presence of the asymmetric inverted region in the ΔG dependence of the reaction rate indicates that the electron transfer in photosystem I is controlled by nuclear tunneling and should be treated in terms of quantum electron-phonon interactions. A three-mode implementation of the multiphonon model, which includes modes around 240 cm (large-scale protein vibrations), 930 cm (out-of-plane bending of macrocycles and protein backbone vibrations), and 1600 cm (double bonds vibrations) was applied to rationalize the observed dependence. The modes with a frequency of at least 1600 cm make the predominant contribution to the reorganization energy, while the contribution of the "classical" low-frequency modes is only 4%.