Comprehensive Analysis of Archaeal tRNA Genes Reveals Rapid Increase of tRNA Introns in the Order Thermoproteales

Sugahara, Junichi; Kikuta, Kaoru; Fujishima, Kosuke; Yachie, Nozomu; Tomita, Masaru; Kanai, Akio

doi:10.1093/molbev/msn216

Cited by 65 publications

(108 citation statements)

References 35 publications

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“…3B). These results further support the recently proposed intron translocation scenario in the order Thermoproteales (18). However, we could not find intron sequences that are similar to the leader sequences of tRNA Gly (CCC/TCC/GCC) and tRNA Glu (CGC/TGC).…”

Section: Evolutionary Relationship Between Split Trna and Intron-contsupporting

confidence: 89%

“…A comprehensive prediction of archaeal tRNA genes remains a challenging task in the field of bioinformatics, because various types of disrupted tRNA genes are found in archaea. To provide a complete picture of tRNA diversity and evolution in the archaeal domain, we recently developed a novel tRNA database, SPLITSdb (18), by retrieving a set of reliable archaeal tRNA sequences using 3 tRNA prediction software packages: tRNAscan-SE (19), ARAGORN (20), and SPLITS (9). Application of this tRNA prediction procedure to the recently sequenced genome of the hyperthermoacidophilic archaeon C. maquilingensis predicted 4 of the 6 missing tRNAs: tRNA Gly (CCC), tRNA Ala (CGC/TGC), and tRNA Glu (TTC) as the typical 2-fragmented type of split tRNAs.…”

Section: Resultsmentioning

confidence: 99%

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Tri-split tRNA is a transfer RNA made from 3 transcripts that provides insight into the evolution of fragmented tRNAs in archaea

Fujishima

Sugahara

Kikuta

et al. 2009

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

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Transfer RNA (tRNA) is essential for decoding the genome sequence into proteins. In Archaea, previous studies have revealed unique multiple intron-containing tRNAs and tRNAs that are encoded on 2 separate genes, so-called split tRNAs. Here, we discovered 10 fragmented tRNA genes in the complete genome of the hyperthermoacidophilic Archaeon Caldivirga maquilingensis that are individually transcribed and further trans-spliced to generate all of the missing tRNAs encoding glycine, alanine, and glutamate. Notably, the 3 mature tRNA Gly 's with synonymous codons are created from 1 constitutive 3 half transcript and 4 alternatively switching transcripts, representing tRNA made from a total of 3 transcripts named a ''tri-split tRNA.'' Expression and nucleotide sequences of 10 split tRNA genes and their joined tRNA products were experimentally verified. The intervening sequences of split tRNA have high identity to tRNA intron sequences located at the same positions in intron-containing tRNAs in related Thermoproteales species. This suggests that an evolutionary relationship between intron-containing and split tRNAs exists. Our findings demonstrate the first example of split tRNA genes in a free-living organism and a unique tri-split tRNA gene that provides further insight into the evolution of fragmented tRNAs.tRNA intron ͉ RNA processing ͉ molecular evolution ͉ trans-splicing ͉ Caldivirga maquilingensis T he origin and evolution of tRNA is one of the most important subjects being discussed in the field of molecular evolution, with varying hypotheses being proposed (1-6). Three types of tRNA genes have previously been identified in archaeal genomes: nonintronic tRNA, which is encoded on a single gene with no intron sequence; intron-containing tRNA, which is encoded on a single gene with a maximum of 3 introns punctuating the mature tRNA sequence at various locations (7-9); and trans-spliced tRNA-so-called split tRNA-which has 5Ј and 3Ј halves encoded on 2 separate genes found only in the hyperthermophilic archaeal parasite, Nanoarchaeum equitans (10). Interestingly, split tRNA and intron-containing tRNA share a common bulge-helix-bulge (BHB) consensus motif around the intron/leader-exon boundaries that can be cleaved by the same tRNA splicing endonucleases (11,12). BHB motifs are further classified by their structure into the canonical form (hBHBhЈ) and relaxed forms (HBhЈ and BHL). The discovery of these tRNA genes raised the question of whether ancestral tRNA was encoded on a single gene or on separate genes. Our previous study has shown clear phylogenetic relationships among these 3 types of archaeal tRNAs (13). Because N. equitans is a parasite with indications of a massive genome reduction (14), whether its tRNAs represent the ancient form of tRNA or a later product of genome reduction is still unclear. Therefore, we have been conducting comprehensive prediction and analysis of tRNA sequences in various species on the basis of our original software, SPLITS (8,9,13,15,16). We have especially focused on the hyperther...

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Section: Evolutionary Relationship Between Split Trna and Intron-contsupporting

confidence: 89%

Section: Resultsmentioning

confidence: 99%

Tri-split tRNA is a transfer RNA made from 3 transcripts that provides insight into the evolution of fragmented tRNAs in archaea

Fujishima

Sugahara

Kikuta

et al. 2009

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

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“…The presence of rRNA gene introns is a distinguishing characteristic of Pyrobaculum spp. and, more broadly, the entire order Thermoproteales (52,53,(53)(54)(55)(56). Two of the three 16S rRNA gene introns (PyWP30.S919 and PyWP30.S1391) (57) encode a homing endonuclease that contains at least one LAGL-IDADG DNA binding motif.…”

Section: Growth Characteristicsmentioning

confidence: 99%

Pyrobaculum yellowstonensis Strain WP30 Respires on Elemental Sulfur and/or Arsenate in Circumneutral Sulfidic Geothermal Sediments of Yellowstone National Park

Jay

Beam

Dohnálková

et al. 2015

Appl Environ Microbiol

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d Thermoproteales (phylum Crenarchaeota) populations are abundant in high-temperature (>70°C) environments of Yellowstone National Park (YNP) and are important in mediating the biogeochemical cycles of sulfur, arsenic, and carbon. The objectives of this study were to determine the specific physiological attributes of the isolate Pyrobaculum yellowstonensis strain WP30, which was obtained from an elemental sulfur sediment (Joseph's Coat Hot Spring [JCHS], 80°C, pH 6.1, 135 M As) and relate this organism to geochemical processes occurring in situ. Strain WP30 is a chemoorganoheterotroph and requires elemental sulfur and/or arsenate as an electron acceptor. Growth in the presence of elemental sulfur and arsenate resulted in the formation of thioarsenates and polysulfides. The complete genome of this organism was sequenced (1.99 Mb, 58% G؉C content), revealing numerous metabolic pathways for the degradation of carbohydrates, amino acids, and lipids. Multiple dimethyl sulfoxide-molybdopterin (DMSO-MPT) oxidoreductase genes, which are implicated in the reduction of sulfur and arsenic, were identified. Pathways for the de novo synthesis of nearly all required cofactors and metabolites were identified. The comparative genomics of P. yellowstonensis and the assembled metagenome sequence from JCHS showed that this organism is highly related (ϳ95% average nucleotide sequence identity) to in situ populations. The physiological attributes and metabolic capabilities of P. yellowstonensis provide an important foundation for developing an understanding of the distribution and function of these populations in YNP.

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“…loop and extending into the C-C-C motif, as illustrated in Supplemental Figure S2. With the abundance of noncanonical introns in the Pyrobaculum genus (Sugahara et al 2008), it is remarkable that the tRNA region targeted by sR210 is free of introns in all species other than P. calidifontis, where 30% contain an intron in this region. Introns in the tRNA region used to position sRNA-guided modification would likely be under negative selection unless intron removal occurs before modification.…”

Section: Predicted Variation In Rrna Targetsmentioning

confidence: 99%

Discovery of Pyrobaculum small RNA families with atypical pseudouridine guide RNA features

Bernick¹,

Dennis²,

Höchsmann³

et al. 2012

RNA

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In the Eukarya and Archaea, small RNA-guided pseudouridine modification is believed to be an essential step in ribosomal RNA maturation. While readily modeled and identified by computational methods in eukaryotic species, these guide RNAs have not been found in most archaeal genomes. Using high-throughput transcriptome sequencing and comparative genomics, we have identified ten novel small RNA families that appear to function as H/ACA pseudouridylation guide sRNAs, yet surprisingly lack several expected canonical features. The new RNA genes are transcribed and highly conserved across at least six species in the archaeal hyperthermophilic genus Pyrobaculum. The sRNAs exhibit a single hairpin structure interrupted by a conserved kinkturn motif, yet only two of ten families contain the complete canonical structure found in all other H/ACA sRNAs. Half of the sRNAs lack the conserved 39-terminal ACA sequence, and many contain only a single 39 guide region rather than the canonical 59 and 39 bipartite guides. The predicted sRNA structures contain guide sequences that exhibit strong complementarity to ribosomal RNA or transfer RNA. Most of the predicted targets of pseudouridine modification are structurally equivalent to those known in other species. One sRNA appears capable of guiding pseudouridine modification at positions U54 and U55 in most or all Pyrobaculum tRNAs. We experimentally tested seven predicted pseudouridine modifications in ribosomal RNA, and all but one was confirmed. The structural insights provided by this new set of Pyrobaculum sRNAs will augment existing models and may facilitate the identification and characterization of new guide sRNAs in other archaeal species.

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Comprehensive Analysis of Archaeal tRNA Genes Reveals Rapid Increase of tRNA Introns in the Order Thermoproteales

Cited by 65 publications

References 35 publications

Tri-split tRNA is a transfer RNA made from 3 transcripts that provides insight into the evolution of fragmented tRNAs in archaea

Tri-split tRNA is a transfer RNA made from 3 transcripts that provides insight into the evolution of fragmented tRNAs in archaea

Pyrobaculum yellowstonensis Strain WP30 Respires on Elemental Sulfur and/or Arsenate in Circumneutral Sulfidic Geothermal Sediments of Yellowstone National Park

Discovery of Pyrobaculum small RNA families with atypical pseudouridine guide RNA features

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