Dynamics of the Primary Events in Bacterial Photosynthesis

This paper considers the primary light-induced electron-transfer (ET) processes in the reaction center of photosynthetic bacteria which involved ET from the electronically excited state of the bacteriochlorphyll a dimer (BChl)2 to bacteriopheophytin (BPh) ((1.1)) and ET from BPh” to ubiquinone (Q) ((1.2)). Ultrafast reactions 1.1 and 1.2, which are practically temperature independent over the range 4-300 K, cannot be accounted for in terms of low-temperature nuclear tunnelling through a nuclear barrier, as such a mechanism would imply an unrealistically high characteristic molecular frequency for the electron-donor and the electron-acceptor centers. Two mechanisms for ultrashort, temperature-independent processes 1.1 and 1.2 were examined. The rate of the ET reaction (1.2) is considerably longer than characteristic medium-induced vibrational relaxation rates, so that process 1.2 has to occur from a thermally equilibrated nuclear configuration of BPh-Q. Reaction 1.2 is assigned to an activationless nonadiabatic ET process, the short lifetimes for this reaction stemming from a large value of the electronic coupling V si 4 cm-1 which, according to rough estimates, implies that the average BPh'Q spacing is ~10 Å. We propose that the ultrafast reaction (1.1) occurs from a nonequilibrium nuclear configuration of the (BChl)2*BPh initially excited state which is located above the crossing point of the nuclear potential surfaces for (BChl)2*BPh and for (BChl)2+BPh”. Such a novel ET mechanism involves competition between ET and vibrational relaxation. A theory has been developed to handle this problem and applied to reaction 1.1. A microscopic molecular scheme for the primary events of charge separation in bacterial photosynthesis is proposed, which rests on the optimization of (a) the intramolecular distortions of the equilibrium nuclear configurations (these nuclear distortions determine the vibrational overlap contributions to the ET rates) and (b) the intermolecular spatial organization of the donor and the acceptor (the donor-acceptor separation (and orientation) determines the electronic coupling which dominates the preexponential contribution to the ET rate). The molecular scheme is successful in accounting for the qualitative and the quantitative features of the primary ET rates and in providing a picture for the directionality, selectivity, and efficiency of the charge separation events.