Computational modeling of an RNA-peptide world

Abstract

Emergence and evolution of functional RNA and protein structures are the central problems for understanding the origin of life. Although it is well known that catalytically active RNA elements, ribozymes, can catalyze many reactions 1–3, including peptide bond formation, the specifics of the transition from the hypothetical, primordial RNA world 4–6 to protein-based life centered at the translation system remain enigmatic 7–9. We developed AMES, Atomistic Molecular Evolution Simulator, and employed it to perform computer simulations of the evolution of short RNA molecules and RNA-peptide complexes. Comparison of the evolutionary trajectories and the structures of RNA molecules and RNA-peptide complexes emerging in these simulations shows that short random peptides accelerate RNA evolution, stabilize RNA folds, and boost the structural diversity of evolving RNA molecules, potentially enabling a broader range of activities. We hypothesize that the RNA world was, actually, an ‘RNA-peptide world’, in which, from the earliest stages of evolution, evolving RNA molecules interacted with short random peptides synthesized in a non-templated manner. These interactions could drive the evolution of diverse RNA structures and activities, and eventually, of the translation machinery.