History of the ribosome and the origin of translation

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 112; no. 50; pp. 15396 - 15401
• Main Authors: Petrov, Anton S., Gulen, Burak, Norris, Ashlyn M., Kovacs, Nicholas A., Bernier, Chad R., Lanier, Kathryn A., Fox, George E., Harvey, Stephen C., Wartell, Roger M., Hud, Nicholas V., Williams, Loren Dean
• Format: Journal Article
• Language: English
• Published: United States National Academy of Sciences 15.12.2015; National Acad Sciences
• Subjects: Biocatalysis; Biological Sciences; Escherichia coli - metabolism; Eukaryotes; Evolution; Evolution, Molecular; Models, Molecular; Nucleic Acid Conformation; Prokaryotes; Protein Biosynthesis; Ribonucleic acid; Ribosome Subunits - metabolism; Ribosomes - metabolism; RNA; RNA, Messenger - metabolism; RNA, Ribosomal - chemistry; RNA, Ribosomal - metabolism; RNA, Transfer - chemistry; RNA, Transfer - metabolism; RNA evolution; translation; origin of life; A-minor interactions
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.1509761112

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.