Solid-state lateral proton conduction via solid-supported biological membranes reveals the role of membrane structure and bound water in 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 introduce a new molecular protonics experimental approach to investigate lateral PT across membranes by measuring long-range 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 focusing 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 amount of water and their structure, and on membrane composition, where we explore the role of the head group, the level of tail saturation, and the role of the membrane phase and fluidity. The measured PT as a function of temperature shows an inverse temperature dependency, which we explain by the desorption/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.