Sustained Formation, Movement and Destruction of Complex Coacervates in a Waste-Less System Driven by Electricity

Transient compartmentalization and directional motion are key elements of living matter, and milestones in the development of complex chemical systems such as protocells. Coacervate droplets have been proposed as compartments in this context, as they share properties with biomolecular condensates, which act as transient compartments in biology. Previous efforts to develop out-of-equilibrium coacervates use exergonic reactions as an energy source, but this leads to the accumulation of the side-products of the driving reaction, preventing operation over long periods of time. Here, we present a novel strategy to drive the transient formation and movement of coacervate compartments, using an electric potential between two electrodes as an energy source. In this system, the electrochemical oxidation of a cysteine-containing peptide increases its multivalency, leading to complexation with a polyanion and coacervate formation at the anode. The electrochemically-formed coacervates then move by electrophoresis over a distance more than three orders of magnitude larger than their diameter. In the proximity of the cathode, an electrocatalytic cycle dissolves the coacervates by reduction, recovering the free peptide and polyanion, which can diffuse back to the anode and react again. The system reaches a steady state, in which coacervates are simultaneously forming, moving, and disappearing in different regions of the cell. Since no side- products are generated, the formation-movement-destruction regime can be sustained for more than 16 hours, (two orders of magnitude longer than the lifetime of individual droplets), reaching a steady state. This combination of transient formation, directional movement and coacervate compartments is unique, and can be used for electricity-driven active transport.