Effects of nonequilibrium fluctuations on ultrafast short-range electron transfer dynamics

A variety of electron transfer (ET) reactions in biological systems occurs at short distances and is ultrafast. Many of them show behaviors that deviate from the predictions of the classic Marcus theory. Here, we show that these ultrafast ET dynamics highly depend on the coupling between environmental fluctuations and ET reactions. We introduce a dynamic factor, γ (0 ≤ γ ≤ 1), to describe such coupling, with 0 referring to the system without coupling to a “frozen” environment, and 1 referring to the system’s complete coupling with the environment. Significantly, this system’s coupling with the environment modifies the reaction free energy, ΔG(γ), and the reorganization energy, λ(γ), both of which become smaller. This new model explains the recent ultrafast dynamics in flavodoxin and elucidates the fundamental mechanism of nonequilibrium ET dynamics, which is critical to uncovering the molecular nature of many biological functions.