Ribosomal History Reveals Origins of Modern Protein Synthesis

Abstract

The origin and evolution of the ribosome is central to our understanding of the cellular world. Most hypotheses posit that the ribosome originated in the peptidyl transferase center of the large ribosomal subunit. However, these proposals do not link protein synthesis to RNA recognition and do not use a phylogenetic comparative framework to study ribosomal evolution. Here we infer evolution of the structural components of the ribosome. Phylogenetic methods widely used in morphometrics are applied directly to RNA structures of thousands of molecules and to a census of protein structures in hundreds of genomes. We find that components of the small subunit involved in ribosomal processivity evolved earlier than the catalytic peptidyl transferase center responsible for protein synthesis. Remarkably, subunit RNA and proteins coevolved, starting with interactions between the oldest proteins (S12 and S17) and the oldest substructure (the ribosomal ratchet) in the small subunit and ending with the rise of a modern multi-subunit ribosome. Ancestral ribonucleoprotein components show similarities to in vitro evolved RNA replicase ribozymes and protein structures in extant replication machinery. Our study therefore provides important clues about the chicken-or-egg dilemma associated with the central dogma of molecular biology by showing that ribosomal history is driven by the gradual structural accretion of protein and RNA structures. Most importantly, results suggest that functionally important and conserved regions of the ribosome were recruited and could be relics of an ancient ribonucleoprotein world.

Evolution of the protein stoichiometry in the L12 stalk of bacterial and organellar ribosomes

“…The time of adding r-proteins is controversial 36,40 . It seems reasonable to assume that the emergence of the L12 stalk proteins is coupled to the evolution of the translation factors and leads to higher speed and fidelity of translation 40 , which is consistent with the important role of L12 in the recruitment of translation factors to the modern ribosome 9 . Very early in evolution, probably only one copy of L12 was present on the ancestral ribosome (Fig.…”

Aminoacylating Urzymes Challenge the RNA World Hypothesis

“…5). Thus, rather than an RNA world, life more likely began in a Peptide⅐RNA World (36,38,39), in which evolutionary development of catalysis and coding were intimately coupled via stereochemical thermodynamics.…”

When Competing Viruses Unify: Evolution, Conservation, and Plasticity of Genetic Identities

“…For example, ribosomes are essentially very complex ribozymes which are composed of a complicated set of covalently linked stem-loop RNAs which interact in complex ways to provide it with its core function, catalytic synthesis of peptide bonds (Bokov and Steinberg 2009). Given that their individual stem loops appear to have distinct evolutionary histories, the ribosome seems to represent consortia of stem loops that were built up historically over time during evolution (Harish and Caetano-Anollés 2012). Thus, when ribosomes became a resident of DNA in the first cells, the stem-loop RNA consortia were made stable.…”