Origin of proton affinity to membrane/water interfaces

Proton diffusion along biological membranes is vitally important for cellular energetics. It relies on a substantial Gibbs activation energy barrier that opposes proton release from the membrane. Here we have determined this barrier from Arrhenius plots of (i) protons’ surface diffusion constant and (ii) the rate coefficient for proton surface-to-bulk release. Therefore we photo-released protons from a membrane patch at different temperatures and monitored their arrival at a distant patch. The results disproved that quasi-equilibrium exists between protons in the near-membrane layers and in the aqueous bulk. Instead, non-equilibrium kinetics is consistent with this experiment. The Gibbs activation energy barrier only contains a minor enthalpic contribution that roughly corresponds to the breakage of a single hydrogen bond. Conceivably its dominating entropic component originates from the hydrogen bond orientation of surface water molecules that strongly favors proton movement towards the membrane, as indicated by ab initio molecular dynamics simulations performed herein. The simulations mirrored the large in vitro Gibbs activation energy barrier, and they revealed a back-and-forth shuffling of the excess proton between the proximity of the phosphate groups and the interfacial water layers, which suggests high proton mobility. Taken together, this work reconciles the delayed proton surface-to-bulk release with protons weak bonding to surface water molecules.