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

Abstract

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, ΔGγ, and the reorganization energy, λγ, 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.

Biomolecular Basis of Cellular Consciousness via Subcellular Nanobrains

“…In addition, the plasma membrane and derived endosomal/vesicular membranes support transmembrane electron transport as an essential feature of any eukaryotic cell [ 154 , 155 , 156 , 157 , 158 , 159 , 160 , 161 , 162 ]. Importantly, ultrafast and abundant electron transfers occur within proteins [ 163 ]. Thus, not only the sequence of amino acids but especially these electrostatic forces control post-translational protein folding [ 164 , 165 , 166 ].…”

Ultrafast Dynamics of Nonequilibrium Short-Range Electron Transfer in Semiquinone Flavodoxin

“…The transients probed at 800 nm directly describe the forward ET dynamics, and the signals at shorter wavelengths are a mixture of the excited state, intermediates, and final products. Clearly, the signals probed by 800 nm show nonexponential decays, indicating that the ET is coupled with active-site solvation, as observed in many proteins. ,,, The transients can be best fit by a single stretched exponential decay ( , β < 1), and the fitting results are summarized in Table .…”

“…Short-range electron transfer (ET) is ubiquitous in nature and is closely related to function in photosynthetic systems, , photoenzymes, − and photoreceptors. − As short-range ET occurs on an ultrafast time scale ranging from femtoseconds to picoseconds, − which is similar to or even faster than the local environment relaxation of the protein and solvent molecules, the dynamics is in nonequilibrium. − Several theoretical models have been proposed to analyze the nonequilibrium ET, such as the Sumi–Marcus two-dimensional model and recently proposed nonergodic model. − However, more experimental data are needed to solidify nonequilibrium ET theory. Here, we use a small ET flavin protein, Anabaena flavodoxin, as a model system for short-range ET studies.…”

“…Using the solvation dynamics resolved in D. vulgaris semiquinone as an approximation, we apply our recently developed nonergodic mode to analyze the forward ET dynamics in Anabaena semiquinone. The averaged times are calculated using .…”

“…The averaged times are calculated using . The dynamic factor γ and the modified thermodynamic parameters λ γ and Δ G γ are calculated using the method described previously (also see the Supporting Information for calculations). , The simulated forward ET dynamics by the model are shown in Figure A, and the results are listed in Table . Clearly, the value of γ is 0.3–0.6, indicating that the ET is coupled with protein fluctuations.…”