Evolution of the ribosome at atomic resolution

Abstract

The origins and evolution of the ribosome, 3-4 billion years ago, remain imprinted in the biochemistry of extant life and in the structure of the ribosome. Processes of ribosomal RNA (rRNA) expansion can be "observed" by comparing 3D rRNA structures of bacteria (small), yeast (medium), and metazoans (large). rRNA size correlates well with species complexity. Differences in ribosomes across species reveal that rRNA expansion segments have been added to rRNAs without perturbing the preexisting core. Here we show that rRNA growth occurs by a limited number of processes that include inserting a branch helix onto a preexisting trunk helix and elongation of a helix. rRNA expansions can leave distinctive atomic resolution fingerprints, which we call "insertion fingerprints." Observation of insertion fingerprints in the ribosomal common core allows identification of probable ancestral expansion segments. Conceptually reversing these expansions allows extrapolation backward in time to generate models of primordial ribosomes. The approach presented here provides insight to the structure of pre-last universal common ancestor rRNAs and the subsequent expansions that shaped the peptidyl transferase center and the conserved core. We infer distinct phases of ribosomal evolution through which ribosomal particles evolve, acquiring coding and translocation, and extending and elaborating the exit tunnel.RNA evolution | C value | origin of life | translation | phylogeny T he translation system, one of life's universal processes, synthesizes all coded protein in living systems. Our understanding of translation has advanced over the last decade and a half with the explosion in sequencing data and by the determination of 3D structures (1-4). X-ray crystallography and cryoelectron microscopy (cryo-EM) have provided atomic resolution structures of ribosomes from all three domains of life. Eukaryotic ribosomal structures are now available from protists (5), fungi (6), plants (7), insects, and humans (8). Here we describe an atomic level model of the evolution of ribosomal RNA (rRNA) from the large ribosomal subunit (LSU). Our evolutionary model is grounded in patterns of rRNA growth in relatively recent ribosomal expansions, for which there is an extensive, atomicresolution record.The common core LSU rRNA (9, 10), which is approximated here by the rRNA of Escherichia coli, is conserved over the entire phylogenetic tree, in sequence, and especially in secondary structure (11) and 3D structure (12). By contrast, the surface regions and the sizes of ribosomes are variable (13,14). Most of the size variability is found in eukaryotic LSUs (Fig. 1). The integrated rRNA size in the LSU follows the trend Bacteria ≤ Archaea < Eukarya. The added rRNA in eukaryotes interacts with eukaryotic-specific proteins (5, 8, 9) (SI Appendix, Fig. S1 and Dataset S1).Bacterial and archaeal LSU rRNAs are composed entirely of the common core, with only subtle deviations from it. By contrast, eukaryotic LSU rRNAs are expanded beyond the common core. Sacccharomyce...

Universal and domain-specific sequences in 23S–28S ribosomal RNA identified by computational phylogenetics

“…Structural studies of the ribosome have shown that the active site of peptide bond formation is composed solely of ribosomal RNA (rRNA) . This underscores the central role of rRNA in translation and the probability that the initial ribosome in early evolution was composed only of rRNA (Moore and Steitz 2010;Noller 2012;Petrov et al 2014b). The evolution of rRNA sequences as deduced through sequence comparisons has provided a wealth of information about phylogenetic relationships, including a revised tree of life containing three primary domains: Bacteria, Archaea, and Eukarya (Woese et al 1990).…”

“…The eukaryotic dsCNEs correspond in all but one case to regions of rRNA hypothesized to have arisen in the second half of the evolution of the large ribosomal subunit (stages 4 and beyond in Petrov et al 2014b). Both dsCNEs and expansion segments (which are thought to have arisen even later in ribosome evolution; Petrov et al 2014b) are largely eukaryotic phenomena, but dsCNEs have structural (but not sequence) homologs in all three domains of life and the expansion segments do not. When superimposed on the X-ray crystal structure of the yeast 60S ribosomal subunit, the eukaryotic dsCNEs are arranged as a semi-circle cluster (Fig.…”

A search for relict ribonucleotide and amino acid sequences that played a key role in the development of the ribosome and modern protein diversity

“…The highly conservative fragment containing the 3'-chains of stems H74 and H89 not included into the study, as well as the segment of the PTR directly involved in the transpeptidation stage, are particularly interesting (especially since the latter site is considered to be the most ancient element of the 23S rRNA [18]). Remarkably, less conservative sites of the 23S rRNA are perhaps the derivatives of one or two initial rather small rRNA molecules (roughly corresponding to the A-and P-sites), which formed the early structure of the PTC [7,8,19].…”

Small genomes and the difficulty to define minimal translation and metabolic machineries

“…Although it must have been highly simple in primitive cells, the translation apparatus has evolved toward its great present complexity ensuring accurate mRNA decoding and optimizing the efficiency of the mRNA-dependent protein synthesis (Petrov et al, 2014). Nevertheless, host-dependent bacteria (whether parasitic or mutualistic) derived from free-living ancestors have lost some of the components of this complex machinery and are good models for identifying the essential components for proper translation.…”