We present a molecular-level model for the origin and evolution of the translation system, using a 3D comparative method. In this model, the ribosome evolved by accretion, recursively adding expansion segments, iteratively growing, subsuming, and freezing the rRNA. Functions of expansion segments in the ancestral ribosome are assigned by correspondence with their functions in the extant ribosome. The model explains the evolution of the large ribosomal subunit, the small ribosomal subunit, tRNA, and mRNA. Prokaryotic ribosomes evolved in six phases, sequentially acquiring capabilities for RNA folding, catalysis, subunit association, correlated evolution, decoding, energy-driven translocation, and surface proteinization. Two additional phases exclusive to eukaryotes led to tentacle-like rRNA expansions. In this model, ribosomal proteinization was a driving force for the broad adoption of proteins in other biological processes. The exit tunnel was clearly a central theme of all phases of ribosomal evolution and was continuously extended and rigidified. In the primitive noncoding ribosome, proto-mRNA and the small ribosomal subunit acted as cofactors, positioning the activated ends of tRNAs within the peptidyl transferase center. This association linked the evolution of the large and small ribosomal subunits, protomRNA, and tRNA.RNA evolution | translation | origin of life | A-minor interactions T he ribosome retains interpretable molecular records of a world of primordial molecules (1) from around 4 billion years ago (2-9). The records are maintained in rRNA secondary and 3D structures, which are fully conserved throughout the tree of life, and in rRNA sequences, which are more variable (SI Appendix, Fig. S1). Here we use information within ribosomes from each major branch of the tree of life to reconstruct much of the emergence of the universal translational machinery.
Large Ribosomal Subunit EvolutionPreviously, we reported a 3D comparative method that revealed a molecular level chronology of the evolution of the large ribosomal subunit (LSU) rRNA (10). Insertion fingerprints are evident when comparing 3D structures of LSU rRNAs of various sizes from various species. These insertion fingerprints mark sites where rRNA expands, recording growth steps on a molecular level.Within the common core of the LSU rRNA, insertion fingerprints were used to identify ancient growth sites. We showed that insertion fingerprints provide a roadmap from the first steps in the formation of the peptidyl transferase center (PTC) (10) located in the ancient heart of the LSU (2-6), culminating in the common core.Small Ribosomal Subunit, LSU, tRNA, and mRNA Evolution Here, using the 3D comparative method, we establish a comprehensive and coherent model for the evolution of the entire ribosome. This model covers the LSU rRNA, small ribosomal subunit (SSU) rRNA, tRNA, and mRNA. The evolution of each of these components is reconciled at the molecular level to a common chronology. This evolutionary model, which we call the "accretion model," ...