A heated rock crack captures and polymerizes primordial DNA and RNA.

Life is based on informational polymers such as DNA or RNA. For their polymerization, high concentrations of complex monomer building blocks are required. Therefore, the dilution by diffusion poses a major problem before early life could establish a non-equilibrium of compartmentalization. Here, we explored a natural non-equilibrium habitat to polymerize RNA and DNA. A heat flux across thin rock cracks is shown to accumulate and maintain nucleotides. This boosts the polymerization to RNA and DNA inside the crack. Moreover, the polymers remain localized, aiding both the creation of longer polymers and fostering downstream evolutionary steps. In a closed system, we found single nucleotides concentrate 104-fold at the bottom of the crack compared to the top after 24 hours. We detected enhanced polymerization for 2 different activation chemistries: aminoimidazole-activated DNA nucleotides and 2',3'-cyclic RNA nucleotides. The copolymerization of 2',3'-cGMP and 2',3'-cCMP in the thermal pore showed an increased heterogeneity in sequence composition compared to isothermal drying. Finite element models unravelled the combined polymerization and accumulation kinetics and indicated that the escape of the nucleotides from such a crack is negligible over a time span of years. The thermal non-equilibrium habitat establishes a cell-like compartment that actively accumulates nucleotides for polymerization and traps the resulting oligomers. We argue that the setting creates a pre-cellular non-equilibrium steady state for the first steps of molecular evolution.

Non-equilibrium conditions inside rock pores drive fission, maintenance and selection of coacervate protocells.

Key requirements for the first cells on Earth include the ability to compartmentalize and evolve. Compartmentalization spatially localizes biomolecules from a dilute pool and an evolving cell, which, as it grows and divides, permits mixing and propagation of information to daughter cells. Complex coacervate microdroplets are excellent candidates as primordial cells with the ability to partition and concentrate molecules into their core and support primitive and complex biochemical reactions. However, the evolution of coacervate protocells by fusion, growth and fission has not yet been demonstrated. In this work, a primordial environment initiated the evolution of coacervate-based protocells. Gas bubbles inside heated rock pores perturb the coacervate protocell distribution and drive the growth, fusion, division and selection of coacervate microdroplets. Our findings provide a compelling scenario for the evolution of membrane-free coacervate microdroplets on the early Earth, induced by common gas bubbles within heated rock pores.