Thermal oscillations enable reshuffling of genetic material in a primitive cell cycle

Abstract

Self-assembling single-chain amphiphiles available in the prebiotic environment likely played a fundamental role in the advent of primitive cell cycles. However, the instability of prebiotic fatty acid-based membranes to temperature and pH seems to suggest that primitive cells could only host prebiotically-relevant processes in a narrow range of non-fluctuating environmental conditions. Here we propose a novel primitive cell cycle driven by environmental fluctuations, which enable the generation of daughter protocells with reshuffled content. A reversible membrane-to-oil phase transition accounts for the dissolution of fatty acid-based vesicles at high temperatures, and the concomitant release of genetic content. At low temperatures, fatty acid bilayers reassemble and encapsulate reshuffled genetic material in a new cohort of protocells. Notably, we find that our disassembly/reassembly cycle drives the emergence of functional RNA-containing primitive cells from parent non-functional compartments. Thus, by exploiting the intrinsic instability of prebiotic fatty acid vesicles, our results point at an environmentally-driven tunable primitive cell cycle, which supports the release and reshuffle of protocellular genetic and membrane components, potentially leading to a new generation of protocells with superior traits. In the absence of protocellular transport machinery, the environmentally-driven disassembly/assembly cycle proposed herein would have supported genetic content reshuffling transmitted to primitive cell progeny, hinting at a potential mechanism important to initiate Darwinian evolution of early lifeforms.