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      Circularization restores signal recognition particle RNA functionality in Thermoproteus

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          Abstract

          Signal recognition particles (SRPs) are universal ribonucleoprotein complexes found in all three domains of life that direct the cellular traffic and secretion of proteins. These complexes consist of SRP proteins and a single, highly structured SRP RNA. Canonical SRP RNA genes have not been identified for some Thermoproteus species even though they contain SRP19 and SRP54 proteins. Here, we show that genome rearrangement events in Thermoproteus tenax created a permuted SRP RNA gene. The 5'- and 3'-termini of this SRP RNA are located close to a functionally important loop present in all known SRP RNAs. RNA-Seq analyses revealed that these termini are ligated together to generate circular SRP RNA molecules that can bind to SRP19 and SRP54. The circularization site is processed by the tRNA splicing endonuclease. This moonlighting activity of the tRNA splicing machinery permits the permutation of the SRP RNA and creates highly stable and functional circular RNA molecules.

          DOI: http://dx.doi.org/10.7554/eLife.11623.001

          eLife digest

          Cells make many proteins that are eventually released outside the cell or inserted into the cell’s membrane. As these proteins are still being made, they are captured by a “signal recognition particle” (or SRP); this molecular machine then guides the newly forming protein to the cell’s membrane. SRPs are found in all living organisms on Earth and contain several different proteins and a short RNA molecule. However, a few species belonging to the archaeal domain of life did not seem to contain an identifiable gene for the RNA component of the SRP.

          Now Plagens et al. have sought to solve the mystery of the “missing” component of this essential protein-targeting machine. This involved searching through the RNAs that are produced by an archaeon called Thermoproteus tenax, a single-celled microbe which grows in the absence of oxygen and at temperatures of up to 95°C.

          Plagens et al. discovered that the “missing” SRP RNA gene had not yet been identified because rearrangements in this archaeon’s genome had swapped the left and right portions of the SRP RNA gene. Further experiments revealed that the correct sequence order is restored in mature SRP RNA molecules by the two ends of the molecule being linked to form a circle. These RNA circles are made by the cellular machinery that normally removes the unneeded sections from other RNA molecules (called transfer RNAs).

          Circular RNA is much more stable at high temperatures and does not degrade easily, and Plagens et al. suggest that this particular arrangement is therefore especially advantageous for this species. Future work will now aim to work out which selective pressures favor the evolution of such fragmented RNAs.

          DOI: http://dx.doi.org/10.7554/eLife.11623.002

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          Most cited references27

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          GtRNAdb: a database of transfer RNA genes detected in genomic sequence

          Transfer RNAs (tRNAs) represent the single largest, best-understood class of non-protein coding RNA genes found in all living organisms. By far, the major source of new tRNAs is computational identification of genes within newly sequenced genomes. To organize the rapidly growing collection and enable systematic analyses, we created the Genomic tRNA Database (GtRNAdb), currently including over 74 000 tRNA genes predicted from 740 species. The web resource provides overview statistics of tRNA genes within each analyzed genome, including information by isotype and genetic locus, easily downloadable primary sequences, graphical secondary structures and multiple sequence alignments. Direct links for each gene to UCSC eukaryotic and microbial genome browsers provide graphical display of tRNA genes in the context of all other local genetic information. The database can be searched by primary sequence similarity, tRNA characteristics or phylogenetic group. The database is publicly available at http://gtrnadb.ucsc.edu.
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            HSPC117 is the essential subunit of a human tRNA splicing ligase complex.

            Splicing of mammalian precursor transfer RNA (tRNA) molecules involves two enzymatic steps. First, intron removal by the tRNA splicing endonuclease generates separate 5' and 3' exons. In animals, the second step predominantly entails direct exon ligation by an elusive RNA ligase. Using activity-guided purification of tRNA ligase from HeLa cell extracts, we identified HSPC117, a member of the UPF0027 (RtcB) family, as the essential subunit of a tRNA ligase complex. RNA interference-mediated depletion of HSPC117 inhibited maturation of intron-containing pre-tRNA both in vitro and in living cells. The high sequence conservation of HSPC117/RtcB proteins is suggestive of RNA ligase roles of this protein family in various organisms.
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              Nanoarchaeum equitans creates functional tRNAs from separate genes for their 5'- and 3'-halves.

              Analysis of the genome sequence of the small hyperthermophilic archaeal parasite Nanoarchaeum equitans has not revealed genes encoding the glutamate, histidine, tryptophan and initiator methionine transfer RNA species. Here we develop a computational approach to genome analysis that searches for widely separated genes encoding tRNA halves that, on the basis of structural prediction, could form intact tRNA molecules. A search of the N. equitans genome reveals nine genes that encode tRNA halves; together they account for the missing tRNA genes. The tRNA sequences are split after the anticodon-adjacent position 37, the normal location of tRNA introns. The terminal sequences can be accommodated in an intervening sequence that includes a 12-14-nucleotide GC-rich RNA duplex between the end of the 5' tRNA half and the beginning of the 3' tRNA half. Reverse transcriptase polymerase chain reaction and aminoacylation experiments of N. equitans tRNA demonstrated maturation to full-size tRNA and acceptor activity of the tRNA(His) and tRNA(Glu) species predicted in silico. As the joining mechanism possibly involves tRNA trans-splicing, the presence of an intron might have been required for early tRNA synthesis.
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                Author and article information

                Contributors
                Role: Reviewing editor
                Journal
                eLife
                Elife
                eLife
                eLife
                eLife
                eLife Sciences Publications, Ltd
                2050-084X
                24 October 2015
                2015
                : 4
                : e11623
                Affiliations
                [1 ]Max Planck Institute for Terrestrial Microbiology , Marburg, Germany
                [2 ]deptLOEWE Center for Synthetic Microbiology , Synmikro , Marburg, Germany
                [3]National Institute of Child Health and Human Development , United States
                [4]National Institute of Child Health and Human Development , United States
                Author notes
                Article
                11623
                10.7554/eLife.11623
                4731332
                26499493
                0b376f54-257f-4338-9de1-96e18fb60d3a
                © 2015, Plagens et al

                This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

                History
                : 15 September 2015
                : 23 October 2015
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100004189, Max-Planck-Gesellschaft;
                Award Recipient :
                The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
                Categories
                Biochemistry
                Genomics and Evolutionary Biology
                Short Report
                Custom metadata
                2.5
                Archaea can contain permuted versions of the universal signal recognition particle RNA, which require a moonlighting activity of the tRNA splicing machinery to generate functional circular RNAs.

                Life sciences
                thermoproteus tenax,rna processing,splicing,archaea,signal recognition particle,other
                Life sciences
                thermoproteus tenax, rna processing, splicing, archaea, signal recognition particle, other

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