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Proton transfer dynamics at membrane/water interface and mechanism of biological energy conversion

Abstract

Proton transfer between water and the interior of membrane proteins plays a key role in bioenergetics. Here we survey the mechanism of this transfer as inferred from experiments with flash-triggered enzymes capturing or ejecting protons at the membrane surface. These experiments have revealed that proton exchange between the membrane surface and the bulk water phase proceeds at ≥1 msec because of a kinetic barrier for electrically charged species. From the data analysis, the barrier height for protons could be estimated as about 0.12 eV, i.e., high enough to account for the observed retardation in proton exchange. Due to this retardation, the proton activity at the membrane surface might deviate, under steady turnover of proton pumps, from that measured in the adjoining water phase, so that the driving force for ATP synthesis might be higher than inferred from the bulk-to-bulk measurements. This is particularly relevant for alkaliphilic bacteria. The proton diffusion along the membrane surface, on the other hand, is unconstrained and fast, occurring between the neighboring enzymes at less than 1 µsec. The anisotropy of proton dynamics at the membrane surface helps prokaryotes diminish the “futile” escape of pumped protons into the external volume. In some bacteria, the inner membrane is invaginated, so that the “ejected ” pro tons get trapped in the closed space of such intracellular membrane “sacks” which can be round or flat. The chloroplast thylakoids and the mitochondrial cristae have their origin in these intracellular structures.

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Correspondence to A. Y. Mulkidjanian.

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Translated from Biokhimiya, Vol. 70, No. 2, 2005, pp. 308–314.

Original Russian Text Copyright © 2005 by Mulkidjanian, Cherepanov, Heberle, Junge.

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Mulkidjanian, A.Y., Cherepanov, D.A., Heberle, J. et al. Proton transfer dynamics at membrane/water interface and mechanism of biological energy conversion. Biochemistry (Moscow) 70, 251–256 (2005). https://doi.org/10.1007/s10541-005-0108-1

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Key words

  • ATP synthesis
  • membrane potential
  • chemiosmotic coupling
  • alkaliphilic bacteria
  • chloroplasts
  • mitochondria
  • bacterial membranes