A KINETIC-ANALYSIS OF THE PRIMARY CHARGE SEPARATION IN BACTERIAL PHOTOSYNTHESIS - ENERGY GAPS AND STATIC HETEROGENEITY

We consider the energetics, the mechanism and the implications of stat ic heterogeneity for the primary electron transfer (ET) from the elect ronically excited singlet state of the bacteriochlorophyll dimer (P-1 ) in the bacterial photosynthetic reaction center (RC) and some of its mutants. The energetics of the primary ET was inferred from an analys is of the experimental free energy relation (at T = 300 K) between the short-time decay rates of P-1 and the oxidation potentials of the di mer (P) for a series of single site ''good'' mutants, for which geomet rical changes are minimized and perturbations of the prosthetic groups of the accessory bacteriochlorophyll (B) and of the bacteriopheophyti n (H) by the mutants are minor. This analysis resulted in the reasonab le value of lambda(1) = 800 +/- 250 cm(-1) for the (mutant invariant) medium reorganization energy and Delta G(1)(0)(N) = -480 +/- 180 cm(-1 ) for the energy gap for the native (N) RC. The low value of Delta G(1 )(0)(N) implies that the dominant room temperature ET mechanism for th e native RC involves sequential ET. Next, we have explored the effects of heterogeneity on the primary ET by model calculations for the para llel sequential-superexchange mechanism, which is subjected to Gaussia n energy distributions of the energies of the P+B-H and P+BH- ion pair states (with a width parameter of (T = 400 cm(-1)). The modelling of the heterogeneous kinetics by varying the (mean) energy gap Delta G(1) between P+B-H and P-1 was performed to elucidate the temporal decay of P-1 and the ET quantum yield in ''good'' mutants, to explore the g ross feature of primary ET in a triple hydrogen bonded mutant and to c haracterize some of the temperature dependence of the primary ET. The most pronounced manifestations of heterogeneity within the native RC a nd its single site mutants (Delta G(1) = -900 to 300 cm(-1)) are the n onexponential temporal decay probabilities for Ip, which exhibit long -time tails, with heterogeneity effects being marked (in the classical limit) when sigma(Delta G(1)+ lambda(1)) > lambda(1)k(B)T. When Delta G(1) >> sigma (i.e., Delta G(1) greater than or equal to 1000 cm(-1)) , the relaxation rate of (1)p is slow, being dominated by the dimer i nternal 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 tempera ture, primary ET in the native RC and its single site mutants is domin ated by the sequential route and only the triple mutant exhibits a mar ked contribution of the superexchange route. At low temperature (T = 2 0 K), ET in the native RC is still dominated by the sequential route ( with a small (i.e., similar to 10%) superexchange contribution being m anifested in its long-time decay), for single site mutants there is an interplay between sequential and superexchange routes, while superexc hange dominates ET in the triple mutant. The heterogeneous parallel se quential-superexchange mechanism is of intrinsic significance to insur e the stability of primary photosynthetic ET for different native and mutagenetically modified RCs over a broad temperature domain.