A Multilamellar Lipid-Polymer Progenitor Can Promote the Assembly of Improbable Functional Polymer Complexes at...

The original conditions from which primitive life emerged on the early Earth were likely to be dilute mixtures of organic compounds in aqueous solutions. A significant challenge for origins of life research is to discover the reactions that allowed such mixtures to become increasingly complex with products such as polymers that had structural and functional properties related to biology. The chances are low that potential reactants could find one another in dilute solutions composed of thousands of different molecular species. To improve the probability of such encounters, we have investigated a novel condition that both concentrates and organizes potential reactants and encapsulates polymeric products to form protocells. The condition involves a source of freshwater that falls as rainfall precipitation on land masses such as volcanic islands. The water dissolves exogenously and endogenously available organic compounds and feeds into hydrothermal fields where the solutions undergo cycles of evaporation and rehydration, a process easily observed today. Most researchers would agree that monomers such as amino acids and nucleotides would be present in the mixture, but less attention has been paid to the self-assembly of amphiphilic compounds that are also essential components of widely studied protocells. Here, we hypothesize how a closely related medium--multilamellar lipid-polymer (LP) matrices exposed to wet-dry cycles--can act as a progenitor and drive three essential processes: concentration of monomers, polymerization by synthesis of ester and peptide bonds, and promotion of interactions between peptides and nucleotide oligomers. We propose that such matrices represent "combinatorial engines" that can generate otherwise improbable functional complexes. After characterizing the sources of organics, the geochemical settings, and energetic environments in which such an LP progenitor can assemble, we present a conceptual model system that informs both chemical and computational experimental approaches to test this hypothesis.