On the mechanism of the primary charge separation in bacterial photosynthesis

In the light of recent experimental work on femtosecond electron transfer kinetics in the reaction center (RC) we explore the mechanism for the primary process. We focus on the special role of the bacteriochlorophyll monomer (B) located between the primary donor (¹P*), a bacteriochlorophyll dimer (P), and a bacteriopheophytin (H), considering a kinetic scheme which combines two parallel pathways of electron transfer: a unistep superexchange channel mediated via electronic interactions with P⁺B^-H, and a two-step sequential channel involving a P⁺B^-H chemical intermediate. In this kinetic scheme we used microscopic nonadiabatic electron transfer rates, which were extended to incorporate the effects of medium-controlled dynamics. The results of the kinetic modelling are presented as a function of the free-energy gap ΔG₁ between the equilibrium nuclear configurations of the donor ¹P* BH and the (physically and/or chemically) mediating state P⁺B^-H. The parallel sequential-superexchange mechanism reduces to the limit of nearly pure sequential pathway for large negative ΔG₁ at all temperatures and to the limit of almost pure superexchange pathway for large positive ΔG₁ at all temperatures and for moderate ΔG₁ at low temperatures. The existing femtosecond kinetic data at room temperature are consistent with either the superposition of sequential and superexchange at all temperatures or to a superposition of superexchange and sequential at room temperature and superexchange at low temperatures. The available femtosecond data at 10 K raise the possibility that the mechanism involves the superposition of superexchange and sequential at 300 K and the dominance of superexchange at low temperatures. Auxiliary experimental information regarding magnetic data, i.e., the singlet-triplet splitting of the radical pair P⁺BH^-, the kinetics of the charge separation in mutagenetically altered RCs, with tyrosine M208 being replaced by phenylalanine, and the unidirectionality of charge separation across the A branch of the RC are analysed in terms of the proposed mechanism. The prevalence of the parallel sequential and superexchange electron transfer routes for the primary charge separation would introduce an element of redundancy, which insures the occurrence of an efficient process which is stable with respect to the variation energetic parameters in different photosynthetic RCs.