Differential stability and dynamics of DNA-based and RNA-based coacervates affect non-enzymatic RNA chemistry

The RNA-peptide world hypothesis postulates the early co-evolution of RNA and peptides that led to the emergence of non-enzymatic RNA replication and peptide synthesis. Although nucleotides and amino acids have been shown to form and polymerise under prebiotic conditions, the origins of their synergy remain unclear. We propose that cooperation between DNA, RNA and peptides could have stemmed from their co-localisation in early biological compartments. Here, we show that heterogeneous mixtures of prebiotic oligonucleotides and peptides can spontaneously assemble into primitive coacervates. Experimental and computational studies reveal that peptide/nucleic acid coacervates are highly robust and form under a notably broad range of conditions. RNA-based coacervates are exceptionally stable and, in the presence of DNA, very fluid, which facilitates diffusion of reactive oligonucleotides and supports prebiotic RNA chemistry. Our findings suggest that coacervation may have occurred very early on the evolutionary timeline and fostered the emergence of a nucleic acid-peptide world. This study provides insights into the prebiotic role of coacervates and reconsiders their significance for the origins of life and the emergence of primitive replication and translation systems.