Electron Transport Chains as a Window into the Earliest Stages of Evolution

Our understanding of the origin and early evolution of life is generally studied under two different paradigms: bottom up and top down. Prebiotic chemistry and early Earth geochemistry allow researchers to explore possible origin of life scenarios. But for these “bottom up” approaches, even successful experiments only amount to a proof of principle. On the other hand, phylogenetic “top down” research on early evolutionary history is able to provide a historical account about ancient organisms, but is unable to investigate evolutionary events that occurred during and just after the origin of life. Here, we consider ancient electron transport chains (ETCs) as a potential bridge between prebiotic geochemistry and early evolutionary history. Current phylogenetic evidence suggests that the ATP synthase motor that converts pH gradients across membranes into stored chemical potential energy and the cellular organization that would have been required for membrane bioenergetics, both predate the last universal common ancestor (LUCA) of life. At the same time, recent experiments have shown that some aspects of modern electron transport chains can be replicated by minerals, protocells, and/or organic cofactors in the absence of proteins. We review the diversity of prokaryotic electron transport chains, describe current work on the early evolution of cellular organization and prebiotic membrane energetics, and advocate for several lines of research to bridge our understanding of the earliest evolution of membrane bioenergetics across prebiotic geochemistry and early evolution.