Coevolution of RNase P and the ribosome.

Translation is carried out by the most conserved assemblies in biology. Among these assemblies, the ribosome and RNase P are central players. These ancient ribonucleoprotein complexes achieved structural and functional maturity by the last universal common ancestor (LUCA) of life. In prior work, we reconstructed the evolutionary history of the ribosome using its three-dimensional structure, based on accretion and molecular fingerprints that date back to life's earliest stages. Here, we extend our structural phylogenetic framework-based on the accretion model-to RNase P, a ribonucleoprotein responsible for processing pre-tRNAs. By sampling RNase P RNA (RPR) sequences and structures across phylogeny and partitioning them into RNA fragments based on insertion fingerprints, we characterize the state of RPR at LUCA and reconstruct the chronology of its emergence. The chronology reveals that RNase P, like the ribosome, accreted modular RNA elements over evolution, while preserving the structure of preexisting elements, thus maintaining a structural record. We used interactions with tRNA to link and unify the evolutionary trajectories of RPR and rRNA. These results support the view that RNase P and the ribosome coevolved as part of a functionally integrated system. The ancestral catalytic sites of rRNA and RPR formed by the same process, fusion of two stem-elbow-stem elements. Analysis of these two coevolving RNAs also suggests that some of their accreted elements share common ancestry. Application of the accretion model requires correct secondary structures and was successful for RPR only when the traditional secondary structure was corrected by reorganizing a pseudoknot.