Prebiotic amino acids bind to and stabilize prebiotic fatty acid membranes

Abstract

Significance How did the first cells on Earth arise? In a minimal cell, a membrane separates proteins and RNA from the surrounding aqueous environment. Cell-like membranes spontaneously assemble from simple prebiotic surfactants called fatty acids. However, fatty acid membranes are unstable in solutions containing salts that were likely present in environments of the early Earth. We find that amino acids, the building blocks of proteins, bind to fatty acid membranes and stabilize them against salts. Moreover, enhanced stabilization persists after dilution as would occur when a dehydrated pool refills with water—a likely setting for the emergence of cells. In addition to explaining how the first membranes were stabilized, our findings answer how key components of the first cells colocalized. The membranes of the first protocells on the early Earth were likely self-assembled from fatty acids. A major challenge in understanding how protocells could have arisen and withstood changes in their environment is that fatty acid membranes are unstable in solutions containing high concentrations of salt (such as would have been prevalent in early oceans) or divalent cations (which would have been required for RNA catalysis). To test whether the inclusion of amino acids addresses this problem, we coupled direct techniques of cryoelectron microscopy and fluorescence microscopy with techniques of NMR spectroscopy, centrifuge filtration assays, and turbidity measurements. We find that a set of unmodified, prebiotic amino acids binds to prebiotic fatty acid membranes and that a subset stabilizes membranes in the presence of salt and Mg2+. Furthermore, we find that final concentrations of the amino acids need not be high to cause these effects; membrane stabilization persists after dilution as would have occurred during the rehydration of dried or partially dried pools. In addition to providing a means to stabilize protocell membranes, our results address the challenge of explaining how proteins could have become colocalized with membranes. Amino acids are the building blocks of proteins, and our results are consistent with a positive feedback loop in which amino acids bound to self-assembled fatty acid membranes, resulting in membrane stabilization and leading to more binding in turn. High local concentrations of molecular building blocks at the surface of fatty acid membranes may have aided the eventual formation of proteins.