Genome-wide Mapping of Transcriptional Start Sites Defines an Extensive Leaderless Transcriptome in Mycobacterium tuberculosis

Cell Reports

Volumn 5, Issue 4, 2013, Pages 1121-1131

  Cortes, Teresa ^a   Schubert, Olga T ^b,c   Rose, Graham ^a,i   Arnvig, Kristine B ^a,d   Comas, Iñaki ^e,f   Aebersold, Ruedi ^b,g   Young, Douglas B ^a,h  

^a NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^b ETH ZURICH   (Switzerland)

^c PhD Program in Molecular Life Sciences Zurich   (Switzerland)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

^e Centre for Public Health Research CSISP   (Spain)

^f CIBER EPIDEMIOLOGÍA Y SALUD PÚBLICA CIBERESP   (Spain)

^g UNIVERSITY OF ZURICH   (Switzerland)

^h IMPERIAL COLLEGE LONDON   (United Kingdom)

ⁱ INSTITUTE FOR ANIMAL HEALTH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

RNA; TRANSCRIPTOME;

5' UNTRANSLATED REGION; ARTICLE; GENE EXPRESSION; GENE MAPPING; GENE SEQUENCE; GENETIC ASSOCIATION; GENETIC CODE; GENETIC TRANSCRIPTION; GROWTH DISORDER; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; REGULATORY SEQUENCE; RNA PROCESSING; RNA SEQUENCE; START CODON; TRANSCRIPTION INITIATION SITE;

BACTERIA (MICROORGANISMS); MYCOBACTERIUM TUBERCULOSIS;

5' UNTRANSLATED REGIONS; CHROMOSOME MAPPING; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; MYCOBACTERIUM TUBERCULOSIS; PROMOTER REGIONS, GENETIC; SEQUENCE ANALYSIS, RNA; TRANSCRIPTION INITIATION SITE; TRANSCRIPTION, GENETIC; TRANSCRIPTOME;

EID: 84888432432     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2013.10.031     Document Type: Article

References (65)

1. Agarwal N., Tyagi A.K. Role of 5'-TGN-3' motif in the interaction of mycobacterial RNA polymerase with a promoter of 'extended -10' class. FEMS Microbiol. Lett. 2003, 225:75-83.
2. Albrethsen J., Agner J., Piersma S.R., Højrup P., Pham T.V., Weldingh K., Jimenez C.R., Andersen P., Rosenkrands I. Proteomic profiling of Mycobacterium tuberculosis identifies nutrient-starvation-responsive toxin-antitoxin systems. Mol. Cell. Proteomics 2013, 12:1180-1191.
3. Anders S., Huber W. Differential expression analysis for sequence count data. Genome Biol. 2010, 11:R106.
4. Arnvig K., Young D. Non-coding RNA and its potential role in Mycobacterium tuberculosis pathogenesis. RNA Biol. 2012, 9:427-436.
5. Arnvig K.B., Comas I., Thomson N.R., Houghton J., Boshoff H.I., Croucher N.J., Rose G., Perkins T.T., Parkhill J., Dougan G., Young D.B. Sequence-based analysis uncovers an abundance of non-coding RNA in the total transcriptome of Mycobacterium tuberculosis. PLoS Pathog. 2011, 7:e1002342.
6. Bailey T.L., Elkan C. Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc. Int. Conf. Intell. Syst. Mol. Biol. 1994, 2:28-36.
7. Barry C.E., Boshoff H.I., Dartois V., Dick T., Ehrt S., Flynn J., Schnappinger D., Wilkinson R.J., Young D. The spectrum of latent tuberculosis: rethinking the biology and intervention strategies. Nat. Rev. Microbiol. 2009, 7:845-855.
8. Betts J.C., Lukey P.T., Robb L.C., McAdam R.A., Duncan K. Evaluation of a nutrient starvation model of Mycobacterium tuberculosis persistence by gene and protein expression profiling. Mol. Microbiol. 2002, 43:717-731.
9. Brenneis M., Hering O., Lange C., Soppa J. Experimental characterization of Cis-acting elements important for translation and transcription in halophilic archaea. PLoS Genet. 2007, 3:e229.
10. Brock J.E., Pourshahian S., Giliberti J., Limbach P.A., Janssen G.R. Ribosomes bind leaderless mRNA in Escherichia coli through recognition of their 5'-terminal AUG. RNA 2008, 14:2159-2169.
11. Chang A., Smollett K.L., Gopaul K.K., Chan B.H.Y., Davis E.O. Mycobacterium tuberculosis H37Rv sigC is expressed from two promoters but is not auto-regulatory. Tuberculosis (Edinb.) 2012, 92:48-55.
12. Dahl J.L., Kraus C.N., Boshoff H.I.M., Doan B., Foley K., Avarbock D., Kaplan G., Mizrahi V., Rubin H., Barry C.E. The role of RelMtb-mediated adaptation to stationary phase in long-term persistence of Mycobacterium tuberculosis in mice. Proc. Natl. Acad. Sci. USA 2003, 100:10026-10031.
13. Datta P., Shi L., Bibi N., Balázsi G., Gennaro M.L. Regulation of central metabolism genes of Mycobacterium tuberculosis by parallel feed-forward loops controlled by sigma factor E (σ(E)). J.Bacteriol. 2011, 193:1154-1160.
14. Deb C., Lee C.M., Dubey V.S., Daniel J., Abomoelak B., Sirakova T.D., Pawar S., Rogers L., Kolattukudy P.E. A novel invitro multiple-stress dormancy model for Mycobacterium tuberculosis generates a lipid-loaded, drug-tolerant, dormant pathogen. PLoS One 2009, 4:e6077.
15. DeJesus M.A., Sacchettini J.C., Ioerger T.R. Reannotation of translational start sites in the genome of Mycobacterium tuberculosis. Tuberculosis (Edinb.) 2013, 93:18-25.
16. Deng W., Wang H., Xie J. Regulatory and pathogenesis roles of Mycobacterium Lrp/AsnC family transcriptional factors. J.Cell. Biochem. 2011, 112:2655-2662.
17. Donà V., Rodrigue S., Dainese E., Palù G., Gaudreau L., Manganelli R., Provvedi R. Evidence of complex transcriptional, translational, and posttranslational regulation of the extracytoplasmic function sigma factor sigmaE in Mycobacterium tuberculosis. J.Bacteriol. 2008, 190:5963-5971.
18. Dugar G., Herbig A., Förstner K.U., Heidrich N., Reinhardt R., Nieselt K., Sharma C.M. High-resolution transcriptome maps reveal strain-specific regulatory features of multiple Campylobacter jejuni isolates. PLoS Genet. 2013, 9:e1003495.
19. Forse L.N., Houghton J., Davis E.O. Enhanced expression of recX in Mycobacterium tuberculosis owing to a promoter internal to recA. Tuberculosis (Edinb.) 2011, 91:127-135.
20. Gengenbacher M., Rao S.P.S., Pethe K., Dick T. Nutrient-starved, non-replicating Mycobacterium tuberculosis requires respiration, ATP synthase and isocitrate lyase for maintenance of ATP homeostasis and viability. Microbiology 2010, 156:81-87.
21. Ghosh S., Sureka K., Ghosh B., Bose I., Basu J., Kundu M. Phenotypic heterogeneity in mycobacterial stringent response. BMC Syst. Biol. 2011, 5:18.
22. Hotter G.S., Mouat P., Collins D.M. Independent transcription of glutamine synthetase (glnA2) and glutamine synthetase adenylyltransferase (glnE) in Mycobacterium bovis and Mycobacterium tuberculosis. Tuberculosis (Edinb.) 2008, 88:382-389.
23. Irnov I., Sharma C.M., Vogel J., Winkler W.C. Identification of regulatory RNAs in Bacillus subtilis. Nucleic Acids Res. 2010, 38:6637-6651.
24. Jacques D.A., Langley D.B., Hynson R.M.G., Whitten A.E., Kwan A., Guss J.M., Trewhella J. A novel structure of an antikinase and its inhibitor. J.Mol. Biol. 2011, 405:214-226.
25. Kaberdina A.C., Szaflarski W., Nierhaus K.H., Moll I. An unexpected type of ribosomes induced by kasugamycin: a look into ancestral times of protein synthesis?. Mol. Cell 2009, 33:227-236.
26. Kröger C., Dillon S.C., Cameron A.D.S., Papenfort K., Sivasankaran S.K., Hokamp K., Chao Y., Sittka A., Hébrard M., Händler K., et al. The transcriptional landscape and small RNAs of Salmonella enterica serovar Typhimurium. Proc. Natl. Acad. Sci. USA 2012, 109:E1277-E1286.
27. Krzywinski M.I., Schein J.E., Birol I., Connors J., Gascoyne R., Horsman D., Jones S.J., Marra M.A. Circos: an information aesthetic for comparative genomics. Genome Res. 2009, 19:1639-1645.
28. Lew J.M., Kapopoulou A., Jones L.M., Cole S.T. TubercuList-10 years after. Tuberculosis (Edinb.) 2011, 91:1-7.
29. Li H., Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 2009, 25:1754-1760.
30. Ma J., Campbell A., Karlin S. Correlations between Shine-Dalgarno sequences and gene features such as predicted expression levels and operon structures. J.Bacteriol. 2002, 184:5733-5745.
31. Maier T., Güell M., Serrano L. Correlation of mRNA and protein in complex biological samples. FEBS Lett. 2009, 583:3966-3973.
32. Miotto P., Forti F., Ambrosi A., Pellin D., Veiga D.F., Balazsi G., Gennaro M.L., Di Serio C., Ghisotti D., Cirillo D.M. Genome-wide discovery of small RNAs in Mycobacterium tuberculosis. PLoS One 2012, 7:e51950.
33. Moll I., Engelberg-Kulka H. Selective translation during stress in Escherichia coli. Trends Biochem. Sci. 2012, 37:493-498.
34. Moll I., Grill S., Gualerzi C.O., Bläsi U. Leaderless mRNAs in bacteria: surprises in ribosomal recruitment and translational control. Mol. Microbiol. 2002, 43:239-246.
35. Moll I., Hirokawa G., Kiel M.C., Kaji A., Bläsi U. Translation initiation with 70S ribosomes: an alternative pathway for leaderless mRNAs. Nucleic Acids Res. 2004, 32:3354-3363.
36. Mortazavi A., Williams B.A., McCue K., Schaeffer L., Wold B. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat. Methods 2008, 5:621-628.
37. Nakagawa S., Niimura Y., Miura K.i., Gojobori T. Dynamic evolution of translation initiation mechanisms in prokaryotes. Proc. Natl. Acad. Sci. USA 2010, 107:6382-6387.
38. Newton-Foot M., Gey van Pittius N.C. The complex architecture of mycobacterial promoters. Tuberculosis (Edinb.) 2013, 93:60-74.
39. Pellin D., Miotto P., Ambrosi A., Cirillo D.M., Di Serio C. A genome-wide identification analysis of small regulatory RNAs in Mycobacterium tuberculosis by RNA-Seq and conservation analysis. PLoS One 2012, 7:e32723.
40. Perkins T.T., Kingsley R.A., Fookes M.C., Gardner P.P., James K.D., Yu L., Assefa S.A., He M., Croucher N.J., Pickard D.J., et al. A strand-specific RNA-Seq analysis of the transcriptome of the typhoid bacillus Salmonella typhi. PLoS Genet. 2009, 5:e1000569.
41. Quinlan A.R., Hall I.M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 2010, 26:841-842.
42. Ramaswamy S.V., Reich R., Dou S.J., Jasperse L., Pan X., Wanger A., Quitugua T., Graviss E.A. Single nucleotide polymorphisms in genes associated with isoniazid resistance in Mycobacterium tuberculosis. Antimicrob. Agents Chemother. 2003, 47:1241-1250.
43. Reddy M.C., Gokulan K., Jacobs W.R., Ioerger T.R., Sacchettini J.C. Crystal structure of Mycobacterium tuberculosis LrpA, a leucine-responsive global regulator associated with starvation response. Protein Sci. 2008, 17:159-170.
44. Rohde K.H., Veiga D.F.T., Caldwell S., Balázsi G., Russell D.G. Linking the transcriptional profiles and the physiological states of Mycobacterium tuberculosis during an extended intracellular infection. PLoS Pathog. 2012, 8:e1002769.
45. Rose G., Cortes T., Comas I., Coscolla M., Gagneux S., Young D.B. Mapping of genotype-phenotype diversity among clinical isolates of Mycobacterium tuberculosis by sequence-based transcriptional profiling. Genome Biol. Evol. 2013, 5:1849-1862.
46. Rustad T.R., Harrell M.I., Liao R., Sherman D.R. The enduring hypoxic response of Mycobacterium tuberculosis. PLoS One 2008, 3:e1502.
47. Rustad T.R., Minch K.J., Brabant W., Winkler J.K., Reiss D.J., Baliga N.S., Sherman D.R. Global analysis of mRNA stability in Mycobacterium tuberculosis. Nucleic Acids Res. 2013, 41:509-517.
48. Schwanhäusser B., Busse D., Li N., Dittmar G., Schuchhardt J., Wolf J., Chen W., Selbach M. Global quantification of mammalian gene expression control. Nature 2011, 473:337-342.
49. Seo J.H., Hong J.S.J., Kim D., Cho B.K., Huang T.W., Tsai S.F., Palsson B.O., Charusanti P. Multiple-omic data analysis of Klebsiella pneumoniae MGH 78578 reveals its transcriptional architecture and regulatory features. BMC Genomics 2012, 13:679.
50. Sharma C.M., Hoffmann S., Darfeuille F., Reignier J., Findeiss S., Sittka A., Chabas S., Reiche K., Hackermüller J., Reinhardt R., et al. The primary transcriptome of the major human pathogen Helicobacter pylori. Nature 2010, 464:250-255.
51. Shine J., Dalgarno L. The 3'-terminal sequence of Escherichia coli 16S ribosomal RNA: complementarity to nonsense triplets and ribosome binding sites. Proc. Natl. Acad. Sci. USA 1974, 71:1342-1346.
52. Slupska M.M., King A.G., Fitz-Gibbon S., Besemer J., Borodovsky M., Miller J.H. Leaderless transcripts of the crenarchaeal hyperthermophile Pyrobaculum aerophilum. J.Mol. Biol. 2001, 309:347-360.
53. Soutourina O.A., Monot M., Boudry P., Saujet L., Pichon C., Sismeiro O., Semenova E., Severinov K., Le Bouguenec C., Coppée J.Y., et al. Genome-wide identification of regulatory RNAs in the human pathogen Clostridium difficile. PLoS Genet. 2013, 9:e1003493.
54. Stewart G.R., Wernisch L., Stabler R., Mangan J.A., Hinds J., Laing K.G., Young D.B., Butcher P.D. Dissection of the heat-shock response in Mycobacterium tuberculosis using mutants and microarrays. Microbiology 2002, 148:3129-3138.
55. Tolstrup N., Sensen C.W., Garrett R.A., Clausen I.G. Two different and highly organized mechanisms of translation initiation in the archaeon Sulfolobus solfataricus. Extremophiles 2000, 4:175-179.
56. Torarinsson E., Klenk H.P., Garrett R.A. Divergent transcriptional and translational signals in Archaea. Environ. Microbiol. 2005, 7:47-54.
57. Trauner A., Lougheed K.E.A., Bennett M.H., Hingley-Wilson S.M., Williams H.D. The dormancy regulator DosR controls ribosome stability in hypoxic mycobacteria. J.Biol. Chem. 2012, 287:24053-24063.
58. Uplekar S., Rougemont J., Cole S.T., Sala C. High-resolution transcriptome and genome-wide dynamics of RNA polymerase and NusA in Mycobacterium tuberculosis. Nucleic Acids Res. 2013, 41:961-977.
59. Vesper O., Amitai S., Belitsky M., Byrgazov K., Kaberdina A.C., Engelberg-Kulka H., Moll I. Selective translation of leaderless mRNAs byspecialized ribosomes generated by MazF in Escherichia coli. Cell 2011, 147:147-157.
60. Vizcaíno J.A., CÔté R.G., Csordas A., Dianes J.A., Fabregat A., Foster J.M., Griss J., Alpi E., Birim M., Contell J., et al. The PRoteomics IDEntifications (PRIDE) database and associated tools: status in 2013. Nucleic Acids Res. 2013, 41(Database issue):D1063-D1069.
61. Weisser H., Nahnsen S., Grossmann J., Nilse L., Quandt A., Brauer H., Sturm M., Kenar E., Kohlbacher O., Aebersold R., Malmström L. An automated pipeline for high-throughput label-free quantitative proteomics. J.Proteome Res. 2013, 12:1628-1644.
62. Woong Park S., Klotzsche M., Wilson D.J., Boshoff H.I., Eoh H., Manjunatha U., Blumenthal A., Rhee K., Barry C.E., Aldrich C.C., et al. Evaluating the sensitivity of Mycobacterium tuberculosis to biotin deprivation using regulated gene expression. PLoS Pathog. 2011, 7:e1002264.
63. Wurtzel O., Sesto N., Mellin J.R., Karunker I., Edelheit S., Bécavin C., Archambaud C., Cossart P., Sorek R. Comparative transcriptomics of pathogenic and non-pathogenic Listeria species. Mol. Syst. Biol. 2012, 8:583.
64. Yus E., Güell M., Vivancos A.P., Chen W.H., Lluch-Senar M., Delgado J., Gavin A.C., Bork P., Serrano L. Transcription start site associated RNAs in bacteria. Mol. Syst. Biol. 2012, 8:585.
65. Zheng X., Hu G.Q., She Z.S., Zhu H. Leaderless genes in bacteria: clue to the evolution of translation initiation mechanisms in prokaryotes. BMC Genomics 2011, 12:361.