Does the Ribosome Challenge our Understanding of the RNA World?

In a recent article published in these pages, Bowman and colleagues propose that the ribosome represents a challenge to the RNA world model, a long-standing framework to explain the origin of DNA and genetically encoded proteins from a hypothetical RNA-based system. Specifically, they outline a scenario for the emergence and subsequent coevolution of the peptidyl transferase centre (PTC) of the ribosome with non-templated peptide products of this RNA through chemical evolution. They also propose that the PTC would have predated the emergence of enzymatic RNA replication, and that this in turn indicates that the RNA world never existed. We and others have previously incorporated non-templated peptide production as an early stage in the evolution of protein synthesis, which we would count as a chemical process, in agreement with Bowman and colleagues' model. However, their model raises an important question: to what extent could early protein synthesis and its products have evolved in the absence of Darwinian processes? We argue that evolution of the early ribosome requires Darwinian evolution, and that, while chemical evolution could give rise to peptidyl transferase activity, it is insufficient for subsequent improvement of a proto-PTC, or for ongoing coevolution of the proto-PTC with its early non-templated peptide products. We conclude that it is difficult to preclude the involvement of replicative processes, themselves subject to Darwinian evolution, from the evolution of the PTC. Finally, Bowman et al. call into question current models for the RNA to protein transition. We show that the difficulty that Bowman et al. have with this scenario is down to a misreading of our previous work.