Compositional heterogeneity confers selective advantage to protocellular membranes during the origins of cellular life

Abstract

Protocell membranes are considered the boundaries of cellular life that first emerged on the prebiotic Earth. They are thought to be comprised of mixtures of single chain amphiphiles, such as fatty acids and their derivatives, moieties which would have been part of the complex prebiotic chemical landscape. In addition to their composition, the physico-chemical properties of these prebiological membranes would have been significantly affected, and regulated, by the physical environment that they were present in. In this study, the physico-chemical properties of two different chain length membrane systems, were systematically characterized, under prebiotically pertinent environmental conditions. The membrane systems have been designed to be composed of fatty acid and/or their alcohol and glycerol monoester derivatives, to make a range of vesicle combinations (e.g. binary and tertiary systems). Their properties were evaluated as a function of multiple factors including their composition, stability under varying pH, Mg 2+ ion concentration and dilution regimes, and permeability. These environmental constraints would have acted as important prebiotic selection pressures to shape the evolution of prebiological membranes. Our results indicate that complex membrane systems are more stable and robust to multiple selection pressures, thereby making them more suitable for supporting protocellular life. Furthermore, different fatty acid derivatives conferred varying degrees of stability when mixed with their respective fatty acid moiety. Importantly, the aforesaid depended on the chain length of the system, and the selection pressure that was applied. Significantly, when the systems were subjected to multiple selection pressures in a consecutive manner, only the heterogeneous membrane systems survived the race. These results highlight the requirement of compositional complexity, and underscore its implications for the emergence of mixed membrane systems during the dawn of life on Earth.