Solid-State Molecular Protonics Devices of Solid-Supported Biological Membranes Reveal the Mechanism of Long-Range Lateral Proton Transport.

Lateral proton transport (PT) on the surface of biological membranes is a fundamental biochemical process in the bioenergetics of living cells, but a lack of available experimental techniques has resulted in a limited understanding of its mechanism. Here, we present a molecular protonics experimental approach to investigate lateral PT across membranes by measuring long-range (70 μm) lateral proton conduction via a few layers of lipid bilayers in a solid-state-like environment, i.e., without having bulk water surrounding the membrane. This configuration enables us to focus on lateral proton conduction across the surface of the membrane while decoupling it from bulk water. Hence, by controlling the relative humidity of the environment, we can directly explore the role of water in the lateral PT process. We show that proton conduction is dependent on the number of water molecules and their structure and on membrane composition, where we explore the role of the headgroup, the tail saturation, the membrane phase, and membrane fluidity. The measured PT as a function of temperature shows an inverse temperature dependency, which we explain by the desorption and adsorption of water molecules into the solid membrane platform. We explain our findings by discussing the role of percolating hydrogen bonding within the membrane structure in a Grotthuss-like mechanism.