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, 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," ...

Commentary: History of the ribosome and the origin of translation

“…Substructure 15 (in gray) contains the proposed central core (domain A) of 16S rRNA, which bares structural similarity to the anticodon stem of tRNA Val but little resemblance to its central tRNA junction (Gulen et al, 2016). Similarities are incompatible with the Petrov et al (2015) chronology.…”

“…While our objections remain basically unanswered (see Caetano-Anollés and Caetano-Anollés, 2015b), in a recent follow up paper, Petrov et al (2015) use the same algorithm to extend their evolutionary inferences to the small ribosomal subunit. Here, we highlight the perils of systematically disposing of evidence with formal and argumentative ad hoc hypotheses to salvage pre-falsified theory.…”

“…Some junctions are labeled with the names of IFs with incorrect branch-to-trunk assignments and notable subtending helices that play functional and structural roles. (C) Example of an inward growth IF claimed to represent an insertion of branch h33-h34 onto trunk h32 of the 16S rRNA molecule ( see aes10/11 in Table S2 of Petrov et al, 2015). The atomic structural model shows instead that coaxially stacked h33-h34 helices (colored red) actually make the trunk of this typical “family B” three-way junction.…”

Coding of Class I and II Aminoacyl-tRNA Synthetases

“…As noted [40,41], the code comprises a programming language and an associated set of programs written using that language. In this sense, it closely resembles a computer operating system, as Williams has noted elsewhere [52,167,168]. The key here is that computer operating systems are built around a simple set of instructions sufficient to enable the hardware, by executing those instructions, to build successively more sophisticated levels of functionality using a very limited set of alternatives.…”

Self-Referential Encoding on Modules of Anticodon Pairs—Roots of the Biological Flow System

“…There are many other instances of reduction of the tRNA set, most appealing the generally forbidden 5'A anticodons. This rationale would be part of the RNA World proposition [57,58,59], indicating that RNAs started the construction of the biosystem and at some point developed the proteins as functional helpers for structures and catalysis, and developed the DNA as more stable genomic helpers, thereafter receding to the job of intermediates between those. These propositions seem to be now being made more flexible in favor of the coevolutionary panorama [16], that is, some kind of an RNP World preceding the present cellular DNP World, which is in entire consistency with the proposal of the Self-Referential Model (SRM), as sketched in Figure 2.…”