Electron transport chains as a window into the earliest stages of evolution

Abstract

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, "top-down" research on early evolutionary history is able to provide a historical account about ancient organisms, but is unable to investigate stages that occurred during and just after the origin of life. Here, we consider ancient electron transport chains (ETCs) as a potential bridge between early evolutionary history and a protocellular stage that preceded it. Current phylogenetic evidence suggests that ancestors of several extant ETC components were present at least as late as the last universal common ancestor of life. In addition, recent experiments have shown that some aspects of modern ETCs can be replicated by minerals, protocells, or organic cofactors in the absence of biological proteins. Here, we discuss the diversity of ETCs and other forms of chemiosmotic energy conservation, describe current work on the early evolution of membrane bioenergetics, and advocate for several lines of research to enhance this understanding by pairing top-down and bottom-up approaches.

Keywords: ATP synthase; early evolution; last universal common ancestor; membrane bioenergetics; origin of life.

Fig. 1.

A general progression of the origin and early evolution of life and the scientific approaches that address each stage. The Protobiological Geochemistry stage, sometimes referred to as protometabolism or chemical evolution, depicts abiotic chemistry in a geochemical context that produced complex organic compounds and prebiotic macromolecules. The Early Genetic Inheritance/Simple Protocells stage depicts an early lifeform with a simple genetic system such as proposed by the RNA World hypothesis encapsulated within membranes that form and divide spontaneously. The Early Cellular Life stage depicts organisms with the level of complexity similar to that of the LUCA. While this final stage may be studied through so-called top–down methods, earlier stages may only be accessed through nonhistorical bottom–up approaches.

Fig. 2.

Signatures of early evolution across different types of chemiosmotic energy conservation. Electron flow is shown as blue arrows. Likely ancestry from the LUCA is reflected by either direct phylogenetic evidence or the number of different LUCA proteome studies (out of eight total) that predict a component of the complex to be descended from the LUCA (SI Appendix) (38, 64). Protein cofactors that are potential relics of prebiotic mineral catalysis (65) or ribozyme catalysts (66) are highlighted in green and purple, respectively. Homology across different ETC components is indicated by a dashed line. Electron carrier proteins that are components of ETC complexes such as cytochrome B are not shown.

Fig. 3.

Previously published hypotheses of ancient chemiosmotic energy conservation systems based on phylogenetic evidence. (A) An ancestral ATP synthase motor complex is powered by a geochemical proton gradient produced in an alkaline vent environment (103, 109). (B) An ancestor of Rieske/cytB proteins (Complex III) produces a proton gradient through a quinone-based redox loop (100) in which quinones and the ancestor of Rieske/cytB complex link the oxidation of S⁰ and the reduction of nitric oxide (110). (C) An ancestor to the MBH, MBX, FPO, and Nuo (Complex I) complexes produces a proton gradient through proton pumping activity and substrate turnover (89). Phylogenetic evidence suggests that ancestors of all three of these ETC components were present at the time of the LUCA.