Chemiosmotic energy for primitive cellular life: Proton gradients are generated across lipid membranes by redox reactions coupled to meteoritic quinones

Abstract

Transmembrane proton gradients coupled to, and maintained by, electron transport are ubiquitous sources of chemiosmotic energy in all life today, but how this system first emerged is uncertain. Here we report a model liposome system in which internal ferricyanide serves as an oxidant and external ascorbate or dithionite provide a source of electrons to electron carriers embedded in liposome membranes. Quinones linked the donor to the acceptor in a coupled redox reaction that released protons into the vesicle internal volume as electrons were transported across the membranes, thereby producing substantial pH gradients. Using this system, we found that one or more quinones in extracts from carbonaceous meteorites could serve as coupling agents and that substantial pH gradients developed in the acidic interior of liposomes. If amphiphilic compounds present on the prebiotic Earth assembled into membranous compartments that separate reduced solutes in the external medium from an encapsulated acceptor, quinones can mediate electron and proton transport across the membranes, thereby providing a source of chemiosmotic energy for primitive metabolic reactions.