Compositional and functional diversity of minimal primitive coacervates in a nucleic acid-peptide world

The RNA-peptide world hypothesis postulates the early co-evolution of RNA and peptides, leading to the emergence of non-enzymatic RNA replication and peptide synthesis. Although nucleotides and amino acids were shown to form and polymerise under prebiotic conditions, the origin of their synergy, ubiquitously preserved in the central dogma of modern biology, remains unclear. We propose that the cooperation between DNA, RNA and peptides might have stemmed from their co-localisation in early compartments. Here we show that heterogeneous mixtures of prebiotic oligonucleotides and peptides spontaneously assemble into primitive coacervates. Experimental and computational studies reveal that peptide/nucleic acid coacervates are more robust and form over a broader range of conditions than peptide/peptide analogues. Notably, RNA-based coacervates exhibit exceptional stability and, in the presence of DNA, minimal viscosity, facilitating the diffusion of reactive oligonucleotides and supporting prebiotic RNA chemistry. Our findings suggest that coacervation may have occurred in the early on the evolutionary timeline, fostering the emergence of a nucleic acid-peptide world. This study provides new insights into the prebiotic role of coacervates, reconsidering their significance in the origins of life and the emergence of primitive replication and translation systems.