On the validity of the standard model for primary charge separation in the bacterial reaction center

Abstract

In the standard model the primary electron donor state (P∗) is localized on the special pair, meaning that the coupling between the lowest excited state (P_) of the special pair and charge transfer states involving radical anions of accessory cofactors is weak. This model is scrutinized using hole burning data for bacterial and green plan reaction centers (RC), antenna protein complexes and ππ∗ states of probe molecules imbedded in glasses and polymers. Attention is focused on the linear electron-phonon coupling strength (optical reorganization energy) and the dynamics afforded by the zero-phonon hole of the P∗ ← P transition. The hole burning data, together with the structural differences between the special pair of bacterial and green plant RC as well as quantum chemical calculations pertaining to the contribution of internal charge transfer states (of P) to P_, indicate that the standard model is invalid. A model is proposed that has P_ strongly coupled to a quasi-degenerate P+BL− state, where BL is the necessary bacteriochlorophyll on the L branch of the RC. In the adiabatic limit this model appears to be capable of explaining the non-single exponential decay of P870∗ (Rhodobacter sphaeroides) while resolving a serious discrepancy between the hole burning and time domain results on the decay of P∗. In the strong coupling limit, the long-standing question of whether or not P+BL− serves as a real or virtual state in the primary charge separation process becomes irrelevant. The model, especially in the adiabatic limit, may well provide the basis for understanding the extraordinarily fast energy transfer dynamics from higher energy Qy-states to P∗ in the bacterial RC. Potential problems with the strong coupling model are considered and possible approaches to its testing discussed.