Ancient machinery embedded in the contemporary ribosome

Belousoff, Matthew J.; Davidovich, Chen; Zimmerman, Ella; Caspi, Yaron; Wekselman, Itai; Rozenszajn, Lin; Shapira, Tal; Sade-Falk, Ofir; Taha, Leena; Bashan, Anat; Weiss, M.S.; Yonath, Ada

doi:10.1042/bst0380422

Cited by 60 publications

(55 citation statements)

References 52 publications

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“…There is a consensus that some parts of the ribosome are even older than LUCA, predating the protein world. Parts of Domain V of the 23S rRNA are believed to be among the most ancient parts of the ribosome (Woese 2001;Wolf and Koonin 2007;Smith et al 2008;Bokov and Steinberg 2009;Belousoff et al 2010;Fox 2010) while Domain III is thought to be a more recent addition (Hury et al 2006). The data presented here support the hypothesis that Domain III was added as an intact entity to the ancestral ribosome-assuming that the 3D domain is a unit of ribosomal evolution.…”

Section: Evolutionary Implications Of the Domain Structure Of The Domsupporting

confidence: 77%

“…The ribosome in its present form was well-established at the emergence of the last universal common ancestor of life (LUCA) (Woese 2001;Wolf and Koonin 2007;Smith et al 2008;Bokov and Steinberg 2009;Belousoff et al 2010;Fox 2010). There is a consensus that some parts of the ribosome are even older than LUCA, predating the protein world.…”

Section: Evolutionary Implications Of the Domain Structure Of The Dommentioning

confidence: 99%

“…The ribosome is our most direct macromolecular connection to the distant evolutionary past and to early life (Woese 2001;Wolf and Koonin 2007;Smith et al 2008;Bokov and Steinberg 2009;Belousoff et al 2010;Fox 2010). The ribosome is believed to have emerged from the ''RNA world '' (Rich 1962;Woese 1967;Crick 1968;Orgel 1968;Gilbert 1986) following an evolutionary pathway that preserved ribosomal RNAs as central players in peptide bond formation and decoding (Noller et al 1992;Ban et al 2000;Nissen et al 2000;Harms et al 2001;Ogle et al 2001;Yusupov et al 2001;Schuwirth et al 2005;Selmer et al 2006).…”

Section: Introductionmentioning

confidence: 99%

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Domain III of the T. thermophilus 23S rRNA folds independently to a near-native state

Athavale¹,

Gossett²,

Hsiao³

et al. 2012

RNA

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The three-dimensional structure of the ribosomal large subunit (LSU) reveals a single morphological element, although the 23S rRNA is contained in six secondary structure domains. Based upon maps of inter-and intra-domain interactions and proposed evolutionary pathways of development, we hypothesize that Domain III is a truly independent structural domain of the LSU. Domain III is primarily stabilized by intra-domain interactions, negligibly perturbed by inter-domain interactions, and is not penetrated by ribosomal proteins or other rRNA. We have probed the structure of Domain III rRNA alone and when contained within the intact 23S rRNA using SHAPE (selective 29-hydroxyl acylation analyzed by primer extension), in the absence and presence of magnesium. The combined results support the hypothesis that Domain III alone folds to a near-native state with secondary structure, intra-domain tertiary interactions, and inter-domain interactions that are independent of whether or not it is embedded in the intact 23S rRNA or within the LSU. The data presented support previous suggestions that Domain III was added relatively late in ribosomal evolution.

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Section: Evolutionary Implications Of the Domain Structure Of The Domsupporting

confidence: 77%

Section: Evolutionary Implications Of the Domain Structure Of The Dommentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Domain III of the T. thermophilus 23S rRNA folds independently to a near-native state

Athavale¹,

Gossett²,

Hsiao³

et al. 2012

RNA

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“…The cumulative effect of the first four initial expansions (Fig. 5) gives a structure that is strikingly similar to an ancestral PTC proposed independently by Yonath and coworkers (30,31). Those investigators suggested rRNA components of the PTC as an ancient catalytic heart of the common core.…”

mentioning

confidence: 75%

Evolution of the ribosome at atomic resolution

Petrov

Bernier

Hsiao

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

192

261

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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...

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“…It is composed exclusively of RNA and has twofold symmetry formed by rRNA domain V (Bashan et al 2003). The extremely high degree of sequence and structural conservation of this region has engendered the proposition that this region constitutes the ''proto-ribosome'' (for review, see Polacek and Mankin 2005;Davidovich et al 2009;Belousoff et al 2010;Fox 2010). Moreover, in vitro experiments selecting for the ribozymes capable of transpeptidation selected sequences that resembled the PTC (Zhang and Cech 1997).…”

Section: Discussionmentioning

confidence: 99%

Mutations of highly conserved bases in the peptidyltransferase center induce compensatory rearrangements in yeast ribosomes

Rakauskaitė¹,

Dinman²

2011

RNA

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Molecular dynamics simulation identified three highly conserved rRNA bases in the large subunit of the ribosome that form a three-dimensional (3D) ''gate'' that induces pausing of the aa-tRNA acceptor stem during accommodation into the A-site. A nearby fourth base contacting the ''tryptophan finger'' of yeast protein L3, which is involved in the coordinating elongation factor recruitment to the ribosome with peptidyltransfer, is also implicated in this process. To better understand the functional importance of these bases, single base substitutions as well as deletions at all four positions were constructed and expressed as the sole forms of ribosomes in yeast Saccharomyces cerevisiae. None of the mutants had strong effects on cell growth, translational fidelity, or on the interactions between ribosomes and tRNAs. However, the mutants did promote strong effects on cell growth in the presence of translational inhibitors, and differences in viability between yeast and Escherichia coli mutants at homologous positions suggest new targets for antibacterial therapeutics. Mutant ribosomes also promoted changes in 25S rRNA structure, all localized to the core of peptidyltransferase center (i.e., the proto-ribosome area). We suggest that a certain degree of structural plasticity is built into the ribosome, enabling it to ensure accurate translation of the genetic code while providing it with the flexibility to adapt and evolve.

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Ancient machinery embedded in the contemporary ribosome

Cited by 60 publications

References 52 publications

Domain III of the T. thermophilus 23S rRNA folds independently to a near-native state

Domain III of the T. thermophilus 23S rRNA folds independently to a near-native state

Evolution of the ribosome at atomic resolution

Mutations of highly conserved bases in the peptidyltransferase center induce compensatory rearrangements in yeast ribosomes

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