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Light-driven production of ATP catalysed by F0F1-ATP synthase in an artificial photosynthetic membrane

Abstract

Energy-transducing membranes of living organisms couple spontaneous to non-spontaneous processes through the intermediacy of protonmotive force (p.m.f.) — an imbalance in electrochemical potential of protons across the membrane. In most organisms, p.m.f. is generated by redox reactions that are either photochemically driven, such as those in photosynthetic reaction centres, or intrinsically spontaneous, such as those of oxidative phosphorylation in mitochondria. Transmembrane proteins (such as the cytochromes and complexes I, III and IV in the electron-transport chain in the inner mitochondrial membrane) couple the redox reactions to proton translocation, thereby conserving a fraction of the redox chemical potential as p.m.f. Many transducer proteins couple p.m.f. to the performance of biochemical work, such as biochemical synthesis and mechanical and transport processes. Recently, an artificial photosynthetic membrane was reported in which a photocyclic process was used to transport protons across a liposomal membrane, resulting in acidification of the liposome's internal volume1. If significant p.m.f. is generated in this system, then incorporating an appropriate transducer into the liposomal bilayer should make it possible to drive a non-spontaneous chemical process. Here we report the incorporation of FOF1-ATP synthase into liposomes containing the components of the proton-pumping photocycle. Irradiation of this artificial membrane with visible light results in the uncoupler- and inhibitor-sensitive synthesis of adenosine triphosphate (ATP) against an ATP chemical potential of 12 kcal mol−1, with a quantum yield of more than 7%. This system mimics the process by which photosynthetic bacteria convert light energy into ATP chemical potential.

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Figure 1: Diagram of a liposome-based artificial photosynthetic membrane.
Figure 2: The [ATP]-dependent steady-state luminescence of oxyluciferin3 measured as a function of liposo.
Figure 3: The rate of ATP synthesis as a function of actinic light intensity.
Figure 4: The synthesis of ATP as a function of irradiation time at different ratios of [ATP]/[ADP].

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Acknowledgements

We thank F. Haraux for the gift of purified CF0F1, and both F. Haraux and W. Frasch for discussions. This work was supported by the US DOE.

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Correspondence to Thomas A. Moore.

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Steinberg-Yfrach, G., Rigaud, JL., Durantini, E. et al. Light-driven production of ATP catalysed by F0F1-ATP synthase in an artificial photosynthetic membrane. Nature 392, 479–482 (1998). https://doi.org/10.1038/33116

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