Mapping the RNA-Seq trash bin Unusual transcripts in prokaryotic transcriptome sequencing data

RNA Biology

Volumn 10, Issue 7, 2013, Pages 1204-1210

  Doose, Gero ^a   Alexis, Maria ^a,b   Kirsch, Rebecca ^a   Findeis, Sven ^e   Langenberger, David ^a   Machne, Rainer ^a,e   Morl, Mario ^a   Hoffmann, Steve ^a   Stadler, Peter F ^a,c,d,e,f,g  

^a UNIVERSITY OF LEIPZIG   (Germany)

^b STANFORD UNIVERSITY   (United States)

^c MAX PLANCK INSTITUTE FOR MATHEMATICS IN THE SCIENCES   (Germany)

^d FRAUNHOFER INSTITUTE FOR CELL THERAPY AND IMMUNOLOGY   (Germany)

^e UNIVERSITY OF VIENNA   (Austria)

^f UNIVERSITY OF COPENHAGEN   (Denmark)

^g SANTA FE INSTITUTE   (United States)

Author keywords

Circular srnas; RNA seq; Self splicing introns; Split trnas

Indexed keywords

TRANSCRIPTOME;

ARTICLE; CHROMOSOME; CONSENSUS SEQUENCE; ESCHERICHIA COLI; GENOME; INTRON; NONHUMAN; OPERON; REVERSE TRANSCRIPTION; RNA PROCESSING; RNA SEQUENCE; SALMONELLA ENTERICA;

ARCHAEA; BACTERIA (MICROORGANISMS); PROKARYOTA;

CIRCULAR SRNAS; RNA-SEQ; SELF-SPLICING INTRONS; SPLIT TRNAS;

ARCHAEA; BACTERIA; COMPUTATIONAL BIOLOGY; GENOMICS; MOLECULAR SEQUENCE ANNOTATION; PROKARYOTIC CELLS; RNA; SEQUENCE ANALYSIS, RNA; TRANSCRIPTOME;

EID: 84880894704     PISSN: 15476286     EISSN: 15558584     Source Type: Journal    
DOI: 10.4161/rna.24972     Document Type: Article

References (58)

1. Marck C, Grosjean H. Identification of BHB splicing motifs in intron-containing tRNAs from 18 archaea: evolutionary implications. RNA 2003; 9:1516-31; PMID:14624007; http://dx.doi.org/10.1261/rna.5132503.
2. Sugahara J, Yachie N, Arakawa K, Tomita M. In silico screening of archaeal tRNA-encoding genes having multiple introns with bulge-helix-bulge splicing motifs. RNA 2007; 13:671-81; PMID:17369313; http://dx.doi.org/10.1261/ rna.309507.
3. Yoshinari S, Itoh T, Hallam SJ, DeLong EF, Yokobori S, Yamagishi A, et al. Archaeal pre-mRNA splicing: A connection to hetero-oligomeric splicing endonuclease. Biochem Biophys Res Commun 2006; 346:1024-32; PMID:16781672; http://dx.doi.org/10.1016/j.bbrc.2006.06.011.
4. Tocchini-Valentini GD, Fruscoloni P, Tocchini-Valentini GP. Evolution of introns in the archaeal world. Proc Natl Acad Sci USA 2011; 108:4782-7; PMID:21383132; http://dx.doi.org/10.1073/pnas.1100862108.
5. Salgia SR, Singh SK, Gurha P, Gupta R. Two reactions of Haloferax volcanii RNA splicing enzymes: joining of exons and circularization of introns. RNA 2003; 9:319-30; PMID:12592006; http://dx.doi.org/10.1261/rna.2118203.
6. Randau L, Söll D. Transfer RNA genes in pieces. EMBO Rep 2008; 9:623-8; PMID:18552771http://dx.doi.org/10.1038/embor.2008.101.
7. Fujishima K, Sugahara J, Kikuta K, Hirano R, Sato A, Tomita M, et al. Tri-split tRNA is a transfer RNA made from 3 transcripts that provides insight into the evolution of fragmented tRNAs in archaea. Proc Natl Acad Sci USA 2009; 106:2683-7; PMID:19190180; http://dx.doi.org/10.1073/pnas.0808246106.
8. Randau L. RNA processing in the minimal organism Nanoarchaeum equitans. Genome Biol 2012; 13:R63; PMID:22809431; http://dx.doi.org/10.1186/gb-2012-13-7- r63.
9. Dalgaard JZ, Garrett RA. Protein-coding introns from the 23S rRNA-encoding gene form stable circles in the hyperthermophilic archaeon Pyrobaculum organotrophum. Gene 1992; 121:103-10; PMID:1427083; http://dx.doi.org/10.1016/0378-1119(92)90167-N.
10. Tang TH, Rozhdestvensky TS, d'Orval BC, Bortolin ML, Huber H, Charpentier B, et al. RNomics in Archaea reveals a further link between splicing of archaeal introns and rRNA processing. Nucleic Acids Res 2002; 30:921-30; PMID:11842103; http://dx.doi.org/10.1093/nar/30.4.921.
11. Starostina NG, Marshburn S, Johnson LS, Eddy SR, Terns RM, Terns MP. Circular box C/D RNAs in Pyrococcus furiosus. Proc Natl Acad Sci USA 2004; 101:14097-101; PMID:15375211; http://dx.doi.org/10.1073/pnas.0403520101.
12. Danan M, Schwartz S, Edelheit S, Sorek R. Transcriptome-wide discovery of circular RNAs in Archaea. Nucleic Acids Res 2012; 40:3131-42; PMID:22140119; http://dx.doi.org/10.1093/nar/gkr1009.
13. Cech TR. Self-splicing of group I introns. Annu Rev Biochem 1990; 59:543-68; PMID:2197983; http://dx.doi.org/10.1146/annurev.bi.59.070190.002551.
14. Nielsen H, Johansen SD. Group I introns: Moving in new directions. RNA Biol 2009; 6:375-83; PMID:19667762; http://dx.doi.org/10.4161/rna.6.4.9334.
15. Edgell DR, Chalamcharla VR, Belfort M. Learning to live together: mutualism between self-splicing introns and their hosts. BMC Biol 2011; 9:22; PMID:21481283; http://dx.doi.org/10.1186/1741-7007-9-22.
16. Cocquet J, Chong A, Zhang G, Veitia RA. Reverse transcriptase template switching and false alternative transcripts. Genomics 2006; 88:127-31; PMID:16457984; http://dx.doi.org/10.1016/j.ygeno.2005.12.013.
17. Roy SW, Irimia M. When good transcripts go bad: Artifactual RT-PCR 'splicing' and genome analysis. Bioessays 2008; 30:601-5; PMID:18478540; http://dx.doi.org/10.1002/bies.20749.
18. Houseley J, Tollervey D. Apparent non-canonical transsplicing is generated by reverse transcriptase in vitro. PLoS One 2010; 5:e12271; PMID:20805885; http://dx.doi.org/10.1371/journal.pone.0012271.
19. Salzman J, Gawad C, Wang PL, Lacayo N, Brown PO. Circular RNAs are the predominant transcript isoform from hundreds of human genes in diverse cell types. PLoS One 2012; 7:e30733; PMID:22319583; http://dx.doi.org/10.1371/ journal.pone.0030733.
20. Jeck WR, Sorrentino JA, Wang K, Slevin MK, Burd CE, Liu J, et al. Circular RNAs are abundant, conserved, and associated with ALU repeats. RNA 2013; 19:141-57; PMID:23249747; http://dx.doi.org/10.1261/rna.035667.112.
21. Hansen TB, Jensen TI, Clausen BH, Bramsen JB, Finsen B, Damgaard CK, et al. Natural RNA circles function as efficient microRNA sponges. Nature 2013; 495:384-8; PMID:23446346; http://dx.doi.org/10.1038/nature11993.
22. Memczak S, Jens M, Elefsinioti A, Torti F, Krueger J, Rybak A, et al. Circular RNAs are a large class of animal RNAs with regulatory potency. Nature 2013; 495:333-8; PMID:23446348; http://dx.doi.org/10.1038/nature11928.
23. Gingeras TR. Implications of chimaeric nonco-linear transcripts. Nature 2009; 461:206-11; PMID:19741701; http://dx.doi.org/10.1038/nature08452.
24. Frenkel-Morgenstern MFM, Lacroix V, Ezkurdia I, Levin Y, Gabashvili A, Prilusky J, et al. Chimeras taking shape: potential functions of proteins encoded by chimeric RNA transcripts. Genome Res 2012; 22:1231-42; PMID:22588898; http://dx.doi.org/10.1101/gr.130062.111.
25. Yokobori S, Itoh T, Yoshinari S, Nomura N, Sako Y, Yamagishi A, et al. Gain and loss of an intron in a protein-coding gene in Archaea: The case of an archaeal RNA pseudouridine synthase gene. BMC Evol Biol 2009; 9:198; PMID:19671140; http://dx.doi.org/10.1186/1471-2148-9-198.
26. Randau L, Münch R, Hohn MJ, Jahn D, Söll D. Nanoarchaeum equitans creates functional tRNAs from separate genes for their 5'-And 3'-halves. Nature 2005; 433:537-41; PMID:15690044; http://dx.doi.org/10.1038/ nature03233.
27. Biniszkiewicz D, Cesnaviciene E, Shub DA. Selfsplicing group I intron in cyanobacterial initiator methionine tRNA: evidence for lateral transfer of introns in bacteria. EMBO J 1994; 13:4629-35; PMID:7523114.
28. Ko M, Choi H, Park C. Group I self-splicing intron in the recA gene of Bacillus anthracis. J Bacteriol 2002; 184:3917-22; PMID:12081963; http://dx.doi.org/10.1128/JB.184.14.3917-3922.2002.
29. Tourasse NJ, Kolstø AB. Survey of group I and group II introns in 29 sequenced genomes of the Bacillus cereus group: insights into their spread and evolution. Nucleic Acids Res 2008; 36:4529-48; PMID:18587153; http://dx.doi.org/10.1093/nar/gkn372.
30. Tourasse NJ, Stabell FB, Reiter L, Kolstø AB. Unusual group II introns in bacteria of the Bacillus cereus group. J Bacteriol 2005; 187:5437-51; PMID:16030238; http://dx.doi.org/10.1128/JB.187.15.5437-5451.2005.
31. Zwieb C, Gorodkin J, Knudsen B, Burks J, Wower J. tmRDB (tmRNA database). Nucleic Acids Res 2003; 31:446-7; PMID:12520048; http://dx.doi.org/10.1093/nar/ gkg019.
32. David M, Borasio GD, Kaufmann G. Bacteriophage T4-induced anticodon-loop nuclease detected in a host strain restrictive to RNA ligase mutants. Proc Natl Acad Sci USA 1982; 79:7097-101; PMID:6296815; http://dx.doi.org/10.1073/pnas.79. 23.7097.
33. Amitsur M, Levitz R, Kaufmann G. Bacteriophage T4 anticodon nuclease, polynucleotide kinase and RNA ligase reprocess the host lysine tRNA. EMBO J 1987; 6:2499-503; PMID:2444436.
34. Saikia M, Krokowski D, Guan BJ, Ivanov P, Parisien M, Hu GF, et al. Genome-wide identification and quantitative analysis of cleaved tRNA fragments induced by cellular stress. J Biol Chem 2012; 287:42708-25; PMID:23086926; http://dx.doi.org/10.1074/jbc.M112.371799.
35. Thompson DM, Lu C, Green PJ, Parker R. tRNA cleavage is a conserved response to oxidative stress in eukaryotes. RNA 2008; 14:2095-103; PMID:18719243; http://dx.doi.org/10.1261/rna.1232808.
36. Thompson DM, Parker R. Stressing out over tRNA cleavage. Cell 2009; 138:215-9; PMID:19632169; http://dx.doi.org/10.1016/j.cell.2009.07.001.
37. Jöchl C, Rederstorff M, Hertel J, Stadler PF, Hofacker IL, Schrettl M, et al. Small ncRNA transcriptome analysis from Aspergillus fumigatus suggests a novel mechanism for regulation of protein synthesis. Nucleic Acids Res 2008; 36:2677-89; PMID:18346967; http://dx.doi.org/10.1093/nar/gkn123.
38. Li Y, Luo J, Zhou H, Liao JY, Ma LM, Chen YQ, et al. Stress-induced tRNA-derived RNAs: A novel class of small RNAs in the primitive eukaryote Giardia lamblia. Nucleic Acids Res 2008; 36:6048-55; PMID:18820301; http://dx.doi.org/10.1093/nar/gkn596.
39. Lee YS, Shibata Y, Malhotra A, Dutta A. A novel class of small RNAs: TRNA-derived RNA fragments (tRFs). Genes Dev 2009; 23:2639-49; PMID:19933153; http://dx.doi.org/10.1101/gad.1837609.
40. Gebetsberger J, Zywicki M, Künzi A, Polacek N. tRNA-derived fragments target the ribosome and function as regulatory non-coding RNA in Haloferax volcanii. Archaea 2012; 2012:260909; PMID:23326205; http://dx.doi.org/10.1155/2012/260909.
41. Keppetipola N, Nandakumar J, Shuman S. Reprogramming the tRNA-splicing activity of a bacterial RNA repair enzyme. Nucleic Acids Res 2007; 35:3624-30; PMID:17488852; http://dx.doi.org/10.1093/nar/gkm110.
42. Tanaka N, Shuman S. RtcB is the RNA ligase component of an Escherichia coli RNA repair operon. J Biol Chem 2011; 286:7727-31; PMID:21224389; http://dx.doi.org/10.1074/jbc.C111.219022.
43. Konarska M, Filipowicz W, Gross HJ. RNA ligation via 2'-phosphomonoester, 3', 5'-phosphodiester linkage: requirement of 2', 3'-cyclic phosphate termini and involvement of a 5'-hydroxyl polynucleotide kinase. Proc Natl Acad Sci USA 1982; 79:1474-8; PMID:6280184; http://dx.doi.org/10.1073/pnas.79.5.1474.
44. Englert M, Sheppard K, Aslanian A, Yates JR 3rd, Söll D. Archaeal 3'-phosphate RNA splicing ligase characterization identifies the missing component in tRNA maturation. Proc Natl Acad Sci USA 2011; 108:1290-5; PMID:21209330; http://dx.doi.org/10.1073/pnas.1018307108.
45. Popow J, Schleiffer A, Martinez J. Diversity and roles of (t)RNA ligases. Cell Mol Life Sci 2012; 69:2657-70; PMID:22426497; http://dx.doi.org/10.1007/ s00018-012-0944-2.
46. Tanaka N, Meineke B, Shuman S. RtcB, a novel RNA ligase, can catalyze tRNA splicing and HAC1 mRNA splicing in vivo. J Biol Chem 2011; 286:30253-7; PMID:21757685; http://dx.doi.org/10.1074/jbc.C111.274597.
47. Heinemann IU, Söll D, Randau L. Transfer RNA processing in archaea: unusual pathways and enzymes. FEBS Lett 2010; 584:303-9; PMID:19878676; http://dx.doi.org/10.1016/j.febslet.2009.10.067.
48. Vesper O, Amitai S, Belitsky M, Byrgazov K, Kaberdina AC, Engelberg-Kulka H, et al. Selective translation of leaderless mRNAs by specialized ribosomes generated by MazF in Escherichia coli. Cell 2011; 147:147-57; PMID:21944167; http://dx.doi.org/10.1016/j.cell.2011.07.047.
49. Moll I, Engelberg-Kulka H. Selective translation during stress in Escherichia coli. Trends Biochem Sci 2012; 37:493-8; PMID:22939840; http://dx.doi.org/10.1016/j.tibs.2012.07.007.
50. Sharma CM, Hoffmann S, Darfeuille F, Reignier J, Findeiss S, Sittka A, et al. The primary transcriptome of the major human pathogen Helicobacter pylori. Nature 2010; 464:250-5; PMID:20164839; http://dx.doi.org/10.1038/nature08756.
51. Schmidtke C, Findeiss S, Sharma CM, Kuhfuss J, Hoffmann S, Vogel J, et al. Genome-wide transcriptome analysis of the plant pathogen Xanthomonas identifies sRNAs with putative virulence functions. Nucleic Acids Res 2012; 40:2020-31; PMID:22080557; http://dx.doi.org/10.1093/nar/gkr904.
52. Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnetjournal 2011; 17.
53. Zhou Y, Lu C, Wu QJ, Wang Y, Sun ZT, Deng JC, et al. GISSD: Group I intron sequence and structure database. Nucleic Acids Res 2008; 36(Database issue):D31-7; PMID:17942415; http://dx.doi.org/10.1093/nar/gkm766.
54. Candales MA, Duong A, Hood KS, Li T, Neufeld RA, Sun R, et al. Database for bacterial group II introns. Nucleic Acids Res 2012; 40(Database issue):D187-90; PMID:22080509; http://dx.doi.org/10.1093/nar/gkr1043.
55. Hoffmann S, Otto C, Kurtz S, Sharma CM, Khaitovich P, Vogel J, et al. Fast mapping of short sequences with mismatches, insertions and deletions using index structures. PLoS Comput Biol 2009; 5:e1000502; PMID:19750212; http://dx.doi.org/10.1371/journal.pcbi.1000502.
56. Hoffmann S, et al. A multi-split mapping algorithm for splicing, trans-splicing, and fusion detection in singleend reads 2012.
57. Quinlan AR, Hall IM. BEDTools: A flexible suite of utilities for comparing genomic features. Bioinformatics 2010; 26:841-2; PMID:20110278; http://dx.doi.org/10.1093/bioinformatics/btq033.
58. Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 1994; 22:4673-80; PMID:7984417; http://dx.doi.org/10.1093/nar/22.22.4673.