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

Daniel Milshteyn,George Cooper,David Deamer

doi:10.1038/s41598-019-48328-5

Daniel Milshteyn, George Cooper + Show 1 more

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https://doi.org/10.1038/s41598-019-48328-5

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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.

Highlights

All forms of life require an energy source linked to metabolic reactions to sustain cellular processes such as metabolism, growth and reproduction
When phenazine methosulfate (PMS) is reduced by ascorbate into PMSH, the PMSH diffuses to the inner surface of the lipid bilayer where it donates electrons to ferricyanide contained by the liposomes, releasing protons and lowering the internal pH
Given a redox gradient across membranes, quinones associated with electron transport systems are coupled to proton transport such that a chemiosmotic proton gradient develops in microbial, mitochondrial and chloroplast membranes

Summary

Introduction

All forms of life require an energy source linked to metabolic reactions to sustain cellular processes such as metabolism, growth and reproduction. Bioenergetic electron transfer involving various quinones is ubiquitous in all three domains of life, including ubiquinone in mitochondria, plastoquinone in chloroplasts, and menaquinone in bacteria[2] In these electron transport systems, the quinones act as an electron carrier when they diffuse across membranes after being reduced by an external electron donor and oxidized by an encapsulated electron acceptor. In this cycle (Fig. 1) quinones act as lipid soluble hydrogen shuttles because they partition into the non-polar hydrocarbons of the lipids and diffuse within the bilayers between external and internal volumes as they pick up and drop off electrons and protons. Descriptions, and background information on all meteorites, see the Meteoritical Society Bulletin database[12]

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