A kinetic analysis of the primary charge separation in bacterial photosynthesis. Energy gaps and static heterogeneity

Abstract

Abstract We consider the energetics, the mechanism and the implications of static heterogeneity for the primary electron transfer (ET) from the electronically excited singlet state of the bacteriochlorophyll dimer (1O∗) in the bacterial photosynthetic reaction center (RC) and some of its mutants. The energetics of the primary ET was inferred from an analysis of the experimental free energy relation (at T = 300 K) between the short-time decay rates of 1P∗ and the oxidation potentials of the dimer (P) for a series of single site “good” mutants, for which geometrical changes are minimized and perturbations of the prosthetic groups of the accessory bacteriochlorophyll (B) and of the bacteriopheophytin (H) by the mutants are minor. This analysis resulted in the reasonable value of λ1 = 800 ± 250 cm−1 for the (mutant invariant) medium reorganization energy and ΔG10(N) = −480 ± 180 cm−1 for the energy gap for the native (N) RC. The low value of ΔG10(N) implies that the dominant room temperature ET mechanism for the native RC involves sequential ET. Next, we have explored the effects of heterogeneity on the primary ET by model calculations for the parallel sequential-superexchange mechanism, which is subjected to Gaussian energy distributions of the energies of the P+B−H and P+BH− ion pair states (with a width parameter of σ = 400 cm−1). The modelling of the heterogeneous kinetics by varying the (mean) energy gap ΔG1 between P+B−H and 1P∗ was performed to elucidate the temporal decay of 1P∗ and the ET quantum yield in “good” mutants, to explore the gross feature of primary ET in a triple hydrogen bonded mutant and to characterize some of the temperature dependence of the primary ET. The most pronounced manifestations of heterogeneity within the native RC and its single site mutants (ΔG1 = −900 to 300 cm−1) are the nonexponential temporal decay probabilities for 1P∗, which exhibit long-time tails, with heterogeneity effects being marked (in the classical limit) when σ(ΔG1 + λ1) > λ1kBT. When ΔG1 ⪢ σ (i.e., ΔG1 ⩾ 1000 cm−1), the relaxation rate of 1P∗ is slow, being dominated by the dimer internal conversion rate, with the effects of heterogeneity being less marked, as is the case for the triple hydrogen bond mutant. Regarding mechanistic issues, our kinetic modelling implies that at room temperature, primary ET in the native RC and its single site mutants is dominated by the sequential route and only the triple mutant exhibits a marked contribution of the superexchange route. At low temperature (T = 20 K), ET in the native RC is still dominated by the sequential route (with a small (i.e., ∼ 10%) superexchange contribution being manifested in its long-time decay), for single site mutants there is an interplay between sequential and superexchange routes, while superexchange dominates ET in the triple mutant. The heterogeneous parallel sequential-superexchange mechanism is of intrinsic significance to insure the stability of primary photosynthetic ET for different native and mutagenetically modified RCs over a broad temperature domain.