Identification of the prebiotic translation apparatus within the contemporary ribosome

A structural element that could have existed independently in the prebiotic era was identified at the active site of the contemporary ribosome. It is suggested to have functioned as a proto-ribosome catalyzing peptide bond formation and non-coded elongation in the same manner that contemporary ribosomes exert positional catalysis, namely by accommodating the reactants in stereochemistry favourable for inline nucleophilic attack. This simple apparatus is a dimer of self-folding RNA units that could have assembled spontaneously into a symmetrical pocket-like structure, sufficiently efficient to be preserved throughout evolution as the active site of modern ribosomes, thus presenting a conceivable starting point for translation.Here we discuss the proto-ribosome emergence hypothesis and show that the tendency for dimerization, a prerequisite for obtaining the catalytic centre, is linked to the fold of its two components, indicating functional selection at the molecular level in the prebiotic era and supporting the existence of dimeric proto-ribosome

The Dimeric Proto-Ribosome: Structural Details and Possible Implications on the Origin of Life

A symmetric pocket-like entity, composed of two L-shaped RNA units, encircles the peptide synthesis site within the contemporary ribosome. This entity was suggested to be the vestige of a dimeric proto-ribosome, which could have formed spontaneously in the prebiotic world, catalyzing non-coded peptide bond formation and elongation. This structural element, beyond offering the initial step in the evolution of translation, is hypothesized here to be linked to the origin of life. By catalyzing the production of random peptide chains, the proto-ribosome could have enabled the formation of primary enzymes, launching a process of co-evolution of the translation apparatus and the proteins, thus presenting an alternative to the RNA world hypothesis

Hypothesis: Spontaneous Advent of the Prebiotic Translation System via the Accumulation of L-Shaped RNA Elements

The feasibility of self-assembly of a translation system from prebiotic random RNA chains is a question that is central to the ability to conceive life emerging by natural processes. The spontaneous materialization of a translation system would have required the autonomous formation of proto-transfer RNA (tRNA) and proto-ribosome molecules that are indispensable for translating an RNA chain into a polypeptide. Currently, the vestiges of a non-coded proto-ribosome, which could have only catalyzed the formation of a peptide bond between random amino acids, is consensually localized in the region encircling the peptidyl transferase center of the ribosomal large subunit. The work presented here suggests, based on high resolution structures of ribosomes complexed with messenger RNA (mRNA) and tRNAs, that three types of L-shaped RNA building blocks derived from the modern ribosome, alongside with an L-shaped proto-tRNA, each composed of about 70-mer, could have randomly occurred in the prebiotic world and combined to form a simple translation system. The model of the initial coded proto-ribosome, which includes the active sites of both ribosomal subunits, together with a bridging element, incorporates less than 6% of the current prokaryotic rRNA, yet it integrates all of the ribosomal components that are vital for synthesizing the earliest coded polypeptides

Three Biopolymers and Origin of Life Scenarios

To track down the possible roots of life, various models for the initial living system composed of different combinations of the three extant biopolymers, RNA, DNA, and proteins, are presented. The suitability of each molecular set is assessed according to its ability to emerge autonomously, sustain, and evolve continuously towards life as we know it. The analysis incorporates current biological knowledge gained from high-resolution structural data and large sequence datasets, together with experimental results concerned with RNA replication and with the activity demonstrated by standalone constructs of the ribosomal Peptidyl Transferase Center region. The scrutiny excludes the DNA–protein combination and assigns negligible likelihood to the existence of an RNA–DNA world, as well as to an RNA world that contained a replicase made of RNA. It points to the precedence of an RNA–protein system, whose model of emergence suggests specific processes whereby a coded proto-ribosome ribozyme, specifically aminoacylated proto-tRNAs and a proto-polymerase enzyme, could have autonomously emerged, cross-catalyzing the formation of each other. This molecular set constitutes a feasible starting point for a continuous evolutionary path, proceeding via natural processes from the inanimate matter towards life as we know it

Prebiotic Assembly of Cloverleaf tRNA, Its Aminoacylation and the Origin of Coding, Inferred from Acceptor Stem Coding-Triplets

tRNA is a key component in life’s most fundamental process, the translation of the instructions contained in mRNA into proteins. Its role had to be executed as soon as the earliest translation emerged, but the questions of the prebiotic tRNA materialization, aminoacylation, and the origin of the coding triplets it carries are still open. Here, these questions are addressed by utilizing a distinct pattern of coding triplets highly conserved in the acceptor stems from the modern bacterial tRNAs of five early-emerging amino acids. Self-assembly of several copies of a short RNA oligonucleotide that carries a related pattern of coding triplets, via a simple and statistically feasible process, is suggested to result in a proto-tRNA model highly compatible with the cloverleaf secondary structure of the modern tRNA. Furthermore, these stem coding triplets evoke the possibility that they were involved in self-aminoacylation of proto-tRNAs prior to the emergence of the earliest synthetases, a process proposed to underlie the formation of the genetic code. Being capable of autonomous materialization and of self-aminoacylation, this verifiable model of the proto-tRNA advent adds principal components to an initial set of molecules and processes that may have led, exclusively through natural means, to the emergence of life

Could a Proto-Ribosome Emerge Spontaneously in the Prebiotic World?

An indispensable prerequisite for establishing a scenario of life emerging by natural processes is the requirement that the first simple proto-molecules could have had a realistic probability of self-assembly from random molecular polymers in the prebiotic world. The vestige of the proto-ribosome, which is believed to be still embedded in the contemporary ribosome, is used to assess the feasibility of such spontaneous emergence. Three concentric structural elements of different magnitudes, having a dimeric nature derived from the symmetrical region of the ribosomal large subunit, were suggested to constitute the vestige of the proto-ribosome. It is assumed to have materialized spontaneously in the prebiotic world, catalyzing non-coded peptide bond formation and simple elongation. Probabilistic and energetic considerations are applied in order to evaluate the suitability of the three contenders for being the initial proto-ribosome. The analysis points to the simplest proto-ribosome, comprised of a dimer of tRNA-like molecules presently embedded in the core of the symmetrical region, as the only one having a realistic statistical likelihood of spontaneous emergence from random RNA chains. Hence it offers a feasible starting point for a continuous evolutionary path from the prebiotic matter, through natural processes, into the intricate modern translation system