History of the ribosome and the origin of translation

Abstract

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, proto-mRNA, and tRNA.

Keywords: A-minor interactions; RNA evolution; origin of life; translation.

Fig. 1.

Accretion of SSU rRNA as illustrated by helices 7–10/es3 from species of increasing complexity. A four-way junction at the surface of the common core, formed by helices 7–10, has expanded by accretion. Accretion adds to the previous rRNA core, leaving insertion fingerprints. (A and B) Secondary (A) and 3D (B) structures are preserved upon the addition of new rRNA. (C) Superimposition of the 3D structures highlights how new rRNA accretes with preservation of ancestral rRNA. (D) A characteristic insertion fingerprint is shown in red and blue boxes. In all panels, the rRNA that approximates the common core is blue. An expansion observed in both archaea and eukaryotes is green. An expansion that is observed only in eukaryotes is gold. An additional expansion in higher eukaryotes (mammals) is red.

Fig. 2.

The accretion model mapped onto SSU and LSU secondary structures of E. coli rRNAs. (A and B) Ancestral expansion segments of the SSU (A) and the LSU (B) are numbered by order of acquisition. Insertion fingerprints are located at the seams between the AES or aes. AES/aes colors are arbitrary, chosen to distinguish expansion segments so that no AES or aes is the color of its neighbors. Some ancestral expansion segments appear discontinuous in the secondary structure and so are labeled multiple times. (C) Ancestral bridges B2b, B2c, and B3 mapped onto rRNA secondary structures. (D and E) SSU (D) and LSU (E) common cores are built by the addition of ancestral expansion segments in six phases. Each phase contains ancestral expansion segments that are associated in time and function.

Fig. 3.

The first six phases of the accretion model of ribosomal evolution. In Phase 1, ancestral RNAs form stem–loops and minihelices. In Phase 2, the LSU catalyzes the condensation of nonspecific oligomers. The SSU may have a single-stranded RNA-binding function. In Phase 3, the subunits associate, mediated by the expansion of tRNA from a minihelix to the modern L shape. LSU and SSU evolution is independent and uncorrelated during Phase 1–3. In Phase 4, evolution of the subunits is correlated. The ribosome is a noncoding diffusive ribozyme in which proto-mRNA and the SSU act as positioning cofactors. In Phase 5, the ribosome expands to an energy-driven, translocating, decoding machine. Phase 6 marks the completion of the common core with a proteinized surface (the proteins are omitted for clarity). The colors of the phases are the same as in Fig. 2. mRNA is shown in light green. The A-site tRNA is magenta, the P-site tRNA is cyan, and the E-site tRNA is dark green.

Fig. 4.

Comparison of an ancestral insertion in tRNA with a known insertion in rRNA. (A) The insertion fingerprint in tRNA points to the site of accretion of the D-stem and anti-codon stem–loop (green) onto the ancestral minihelix (red). (B) An insertion fingerprint at the locus of a known expansion (ES 12) in S. cerevisiae. The rRNA for E. coli (which lacks the expansion) is shown in blue and for S. cerevisiae is shown in red, except for the expansion rRNA, which is shown in green.