Origin of proton affinity to membrane/water interfaces

Maria Österbauer,Noam Agmon,Denis G. Knyazev,Peter Pohl,Ewald Weichselbaum,Paolo Carloni,Günther Knör,Sergey A. Akimov,Trung Hai Nguyen,Oleg V. Batishchev,Chao Zhang

doi:10.1038/s41598-017-04675-9

Abstract

Proton diffusion along biological membranes is vitally important for cellular energetics. Here we extended previous time-resolved fluorescence measurements to study the time and temperature dependence of surface proton transport. We determined the Gibbs activation energy barrier ΔG‡r that opposes proton surface-to-bulk release from Arrhenius plots of (i) protons’ surface diffusion constant and (ii) the rate coefficient for proton surface-to-bulk release. The large size of ΔG‡r disproves that quasi-equilibrium exists in our experiments between protons in the near-membrane layers and in the aqueous bulk. Instead, non-equilibrium kinetics describes the proton travel between the site of its photo-release and its arrival at a distant membrane patch at different temperatures. ΔG‡r contains only a minor enthalpic contribution that roughly corresponds to the breakage of a single hydrogen bond. Thus, our experiments reveal an entropic trap that ensures channeling of highly mobile protons along the membrane interface in the absence of potent acceptors.

Highlights

Proton production and consumption processes play a pivotal role for bioenergetics across all organisms[1]
Protons move extremely fast along lipid membranes[6, 7]: their lateral proton diffusivity is almost as large as in bulk water[7, 8]. This fast proton migration establishes an efficient link between these proton release and consumption sites[3, 9, 10]
The long interfacial travel distance observed for protons implies that a substantial free energy barrier, ΔG‡r, for proton release prevents the surface proton from readily equilibrating with its bulk counterparts[7, 11]

Summary

Introduction

Proton production and consumption processes play a pivotal role for bioenergetics across all organisms[1] Most of these processes involve proton diffusion at the cellular membrane/water interface[2, 3]. The long interfacial travel distance observed for protons implies that a substantial free energy barrier, ΔG‡r, for proton release prevents the surface proton from readily equilibrating with its bulk counterparts[7, 11]. It allows placing regulatory proteins (uncoupling protein 4) at some distance from both ATP synthases and proton pumps on the inner mitochondrial membrane[12]. Where T, kB, and ν0 ≈ 1013 s−1 are the absolute temperature, the Boltzmann constant, and the universal transition state theory attempt frequency for rate processes at surfaces[15]

Methods

Results

Conclusion