How did LUCA make a living? Chemiosmosis in the origin of life

Abstract

Despite thermodynamic, bioenergetic and phylogenetic failings, the 81-year-old concept of primordial soup remains central to mainstream thinking on the origin of life. But soup is homogeneous in pH and redox potential, and so has no capacity for energy coupling by chemiosmosis. Thermodynamic constraints make chemiosmosis strictly necessary for carbon and energy metabolism in all free-living chemotrophs, and presumably the first free-living cells too. Proton gradients form naturally at alkaline hydrothermal vents and are viewed as central to the origin of life. Here we consider how the earliest cells might have harnessed a geochemically created proton-motive force and then learned to make their own, a transition that was necessary for their escape from the vents. Synthesis of ATP by chemiosmosis today involves generation of an ion gradient by means of vectorial electron transfer from a donor to an acceptor. We argue that the first donor was hydrogen and the first acceptor CO2.