Compositional selection of phospholipid compartments in icy environments drives the enrichment of encapsulated genetic information

Abstract

The lipid world hypothesis proposes that both intracellular components and the chemical composition of the membrane compartment can act as heritable information, contributing to protocellular fitness. However, there are few experimental demonstrations of membrane compositional selection, and none of them have expanded to the associated transfer of encapsulated contents, representing a possible early form of inheritance. Here, we quantitatively demonstrated that the growth of phospholipid vesicles depends on their lipid composition under freezing and thawing (F/T) cycling: Vesicles with more unsaturated bonds in the acyl chain showed higher growth, membrane mixing, and content mixing efficiencies. When vesicles composed of phospholipids with either one or two unsaturated bonds were mixed and subjected to F/T cycles, a selective enrichment of the lipid with two unsaturated bonds was observed in the grown vesicles. Moreover, selection acting on lipid composition was propagated to the encapsulated genetic material, which was also enriched, while it did not play a particular role and thus was selectively neutral. We conclude that membrane lipid composition can be a direct target of selection for grown vesicles under an icy environment, leading to indirect but concurrent enrichment of compartmentalized genetic molecules—independent of their encoded information.