Long distance electron transfer through the aqueous solution between redox partner proteins

Abstract

Despite the importance of electron transfer between redox proteins in photosynthesis and respiration, the inter-protein electron transfer rate between redox partner proteins has never been measured as a function of their separation in aqueous solution. Here, we use electrochemical tunneling spectroscopy to show that the current between two protein partners decays along more than 10 nm in the solution. Molecular dynamics simulations reveal a reduced ionic density and extended electric field in the volume confined between the proteins. The distance-decay factor and the calculated local barrier for electron transfer are regulated by the electrochemical potential applied to the proteins. Redox partners could use electrochemically gated, long distance electron transfer through the solution in order to conciliate high specificity with weak binding, thus keeping high turnover rates in the crowded environment of cells.

Electrochemically Gated Long‐Distance Charge Transport in Photosystem I

“…These events may correspond to hopping through the electronic states of the P700 LUMO. Long‐distance electron transport through the solution has also been observed between redox partner proteins of the respiratory chain . As in the case of cytochromes c and bc 1 , electrostatic interactions play a key role in the binding between PSI and its natural redox partners, Pc and Fd .…”

“…As the ionic concentration is reduced, charge screening is weaker and the electrostatic field over these regions extends several nanometers from the surface into the solvent, in agreement with calculations reported previously and performed in our experimental conditions (pH 7.4, 50 m m ; see Supporting Information, Figure S10). This electrostatic distribution may create a favorable conduit for charge transport over long distances, accounting for the low β values observed in PSI (Figures and ). It has been suggested for different redox proteins that active site surface residues rearrange the local solvent properties, stabilizing water‐mediated pathways for charge transport .…”

“…First, I– z plots with low β are found mostly at U S ≈200–400 mV (Figure ), which is near the P700 redox potential of PSI that is reported and observed in our voltammetry and amperometry recordings (Figure ). These low β values also occur close to the redox midpoint of Pc, the native electron donor of PSI (170 mV), in agreement with results reported for other redox protein partners (see further discussion below). I– z events displaying long current decay ( β <4 nm −1 ) account for 5–15 % of all recordings (depending on U S ) but they are never observed in control experiments and thus bear high statistical significance (Figures S3–S8).…”

“…We have shown that ECSTM allows studying charge transport through individual PSI complexes under bipotentiostatic control, and reveals a long‐distance current that is electrochemically gated around the redox potential of P700 (i.e., long‐distance events are only observed for U S values below 400 mV, suggesting that they are regulated by U S in analogy to the gate potential of a transistor). The current spatial extension is longer at bias corresponding to electron collection or hole injection.…”

New moonlighting functions of mitochondrial cytochrome c in the cytoplasm and nucleus

“…This event is essential to life because it greatly contributes to creating an electron–proton energy transduction mechanism that enables the synthesis of ATP, the major molecule for storing and transferring energy in cells. Recently, it has been proposed that C c and the cytochrome bc 1 complex could use long‐distance electron transfer through the solution to keep high turnover rates in the crowded environment of cells . On the other hand, the functionality of the mitochondrial electron transport chain fully relies on C c , as shown by the observation that C c knockout mice die at mid‐gestation, when the fetal metabolism switches from glycolysis to oxidative phosphorylation .…”