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REVIEW: Proton Transfer Dynamics at Membrane/Water Interface and Mechanism of Biological Energy Conversion

A. Y. Mulkidjanian1,2*, D. A. Cherepanov3, J. Heberle4, and W. Junge1

1Division of Biophysics, Department of Biology/Chemistry, University of Osnabrueck, D-49069 Osnabrueck, Germany; fax: +49-541-9692871; E-mail: mulkidjanian@biologie.uni-osnabrueck.de

2Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University, 119899 Moscow, Russia

3Institute of Electrochemistry, Russian Academy of Sciences, Leninsky pr. 31, 117071 Moscow, Russia

4Research Center Juelich, IBI-2: Structural Biology, D-52425 Juelich, Germany

* To whom correspondence should be addressed.

Received September 30, 2004
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” protons 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.
KEY WORDS: ATP synthesis, membrane potential, chemiosmotic coupling, alkaliphilic bacteria, chloroplasts, mitochondria, bacterial membranes