Solvation and Stabilization of Single-Strand RNA at the Air/Ice Interface Support a Primordial RNA World on Ice

Outstanding questions about the RNA world hypothesis for the emergence of life on Earth concern the stability and self-replication of prebiotic aqueous RNA. Recent experimental work has suggested that solid substrates and low temperatures could help resolve these issues. Herein, we use classical molecular dynamics simulations to explore the possibility that the substrate is ice itself. Simulations at -20 °C show that an eight-nucleotide single strand of RNA, initially situated in the quasi-liquid layer at the air/ice interface, exhibits a robust propensity to reorient itself - its bases turn toward the (hydrophobic) air/ice interface, while its anionic phosphodiester oxygens align with the underlying ice lattice. Kinetic analysis of hydrogen bonding indicates resistance to hydrolysis that is greater than that of an aqueous single-strand RNA at the same temperature. This enhanced resistance, in turn, could increase the opportunities for polymerization and self-copying. These findings thus offer the possibility of a role for an ancient RNA world on ice distinct from that considered in extant elaborations of the RNA world hypothesis. This work is, to the best of our knowledge, the first molecular dynamics study of RNA on ice.