Sequence-based analysis uncovers an abundance of non-coding RNA in the total transcriptome of Mycobacterium tuberculosis

PLoS Pathogens

Volumn 7, Issue 11, 2011, Pages

  Arnvig, Kristine B ^a   Comas, Iñaki ^a,d   Thomson, Nicholas R ^b   Houghton, Joanna ^a   Boshoff, Helena I ^c   Croucher, Nicholas J ^b   Rose, Graham ^a   Perkins, Timothy T ^b   Parkhill, Julian ^b   Dougan, Gordon ^b   Young, Douglas B ^a  

^a NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^b WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^c NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^d Centre for Public Health Research   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

RIBOSOME RNA; RNA; TRANSFER RNA; BACTERIAL RNA; TRANSCRIPTOME; UNTRANSLATED RNA;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ARTICLE; CODING; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PATHOGENESIS; RNA SEQUENCE; ANIMAL; C57BL MOUSE; DNA MICROARRAY; GENE EXPRESSION REGULATION; GENETICS; MOUSE; NUCLEOTIDE SEQUENCE; PATHOGENICITY; SEQUENCE ANALYSIS;

BACILLI (CLASS); MUS; MYCOBACTERIUM TUBERCULOSIS;

ANIMALS; BASE SEQUENCE; GENE EXPRESSION REGULATION, BACTERIAL; MICE; MICE, INBRED C57BL; MYCOBACTERIUM TUBERCULOSIS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RNA, BACTERIAL; RNA, UNTRANSLATED; SEQUENCE ANALYSIS, RNA; TRANSCRIPTOME;

EID: 81755177792     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002342     Document Type: Article

References (77)

1. WHO, (2009) Global tuberculosis control- epidemiology, strategy, financing. Geneva WHO.
2. Barry CE, 3rd, Boshoff HI, Dartois V, Dick T, Ehrt S, et al. (2009) The spectrum of latent tuberculosis: rethinking the biology and intervention strategies. Nat Rev Microbiol 7: 845-855.
3. Reddy TB, Riley R, Wymore F, Montgomery P, DeCaprio D, et al. (2009) TB database: an integrated platform for tuberculosis research. Nucleic Acids Res 37: D499-508.
4. Manganelli R, Voskuil MI, Schoolnik GK, Dubnau E, Gomez M, et al. (2002) Role of the extracytoplasmic-function sigma factor sigma(H) in Mycobacterium tuberculosis global gene expression. Mol Microbiol 45: 365-374.
5. Park HD, Guinn KM, Harrell MI, Liao R, Voskuil MI, et al. (2003) Rv3133c/dosR is a transcription factor that mediates the hypoxic response of Mycobacterium tuberculosis. Mol Microbiol 48: 833-843.
6. Rustad TR, Harrell MI, Liao R, Sherman DR, (2008) The enduring hypoxic response of Mycobacterium tuberculosis. PLoS One 3: e1502.
7. Schnappinger D, Ehrt S, Voskuil MI, Liu Y, Mangan JA, et al. (2003) Transcriptional Adaptation of Mycobacterium tuberculosis within Macrophages: Insights into the Phagosomal Environment. J Exp Med 198: 693-704.
8. Voskuil MI, Schnappinger D, Visconti KC, Harrell MI, Dolganov GM, et al. (2003) Inhibition of respiration by nitric oxide induces a Mycobacterium tuberculosis dormancy program. J Exp Med 198: 705-713.
9. Walters SB, Dubnau E, Kolesnikova I, Laval F, Daffe M, et al. (2006) The Mycobacterium tuberculosis PhoPR two-component system regulates genes essential for virulence and complex lipid biosynthesis. Mol Microbiol 60: 312-330.
10. Cole ST, Brosch R, Parkhill J, Garnier T, Churcher C, et al. (1998) Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393: 537-544.
11. Gripenland J, Netterling S, Loh E, Tiensuu T, Toledo-Arana A, et al. (2010) RNAs: regulators of bacterial virulence. Nat Rev Microbiol 8: 857-866.
12. Papenfort K, Vogel J, (2010) Regulatory RNA in bacterial pathogens. Cell Host Microbe 8: 116-127.
13. Waters LS, Storz G, (2009) Regulatory RNAs in bacteria. Cell 136: 615-628.
14. Mandal M, Breaker RR, (2004) Gene regulation by riboswitches. Nat Rev Mol Cell Biol 5: 451-463.
15. Loh E, Dussurget O, Gripenland J, Vaitkevicius K, Tiensuu T, et al. (2009) A trans-acting riboswitch controls expression of the virulence regulator PrfA in Listeria monocytogenes. Cell 139: 770-779.
16. Gottesman S, Storz G, (2010) Bacterial Small RNA Regulators: Versatile Roles and Rapidly Evolving Variations. Cold Spring Harb Perspect Biol Epub ahead of print. pii doi:10.1101/cshperspect.a003798.
17. Toledo-Arana A, Dussurget O, Nikitas G, Sesto N, Guet-Revillet H, et al. (2009) The Listeria transcriptional landscape from saprophytism to virulence. Nature 459: 950-956.
18. Pfeiffer V, Sittka A, Tomer R, Tedin K, Brinkmann V, et al. (2007) A small non-coding RNA of the invasion gene island (SPI-1) represses outer membrane protein synthesis from the Salmonella core genome. Mol Microbiol 66: 1174-1191.
19. Pichon C, Felden B, (2005) Small RNA genes expressed from Staphylococcus aureus genomic and pathogenicity islands with specific expression among pathogenic strains. Proc Natl Acad Sci U S A 102: 14249-14254.
20. Mandin P, Repoila F, Vergassola M, Geissmann T, Cossart P, (2007) Identification of new noncoding RNAs in Listeria monocytogenes and prediction of mRNA targets. Nucleic Acids Res 35: 962-974.
21. Arnvig KB, Young DB, (2010) Regulation of pathogen metabolism by small RNA. Drug Discov Today Dis Mech 7: e19-e24.
22. Arnvig KB, Young DB, (2009) Identification of small RNAs in Mycobacterium tuberculosis. Mol Microbiol 73: 397-408.
23. Dichiara JM, Contreras-Martinez LM, Livny J, Smith D, McDonough KA, et al. (2010) Multiple small RNAs identified in Mycobacterium bovis BCG are also expressed in Mycobacterium tuberculosis and Mycobacterium smegmatis. Nucleic Acids Res 38: 4067-78.
24. Perkins TT, Kingsley RA, Fookes MC, Gardner PP, James KD, et al. (2009) A strand-specific RNA-Seq analysis of the transcriptome of the typhoid bacillus Salmonella typhi. PLoS Genet 5: e1000569.
25. Sharma CM, Hoffmann S, Darfeuille F, Reignier J, Findeiss S, et al. (2010) The primary transcriptome of the major human pathogen Helicobacter pylori. Nature 464: 250-255.
26. Sittka A, Lucchini S, Papenfort K, Sharma CM, Rolle K, et al. (2008) Deep sequencing analysis of small noncoding RNA and mRNA targets of the global post-transcriptional regulator, Hfq. PLoS Genet 4: e1000163.
27. Albrecht M, Sharma CM, Reinhardt R, Vogel J, Rudel T, (2010) Deep sequencing-based discovery of the Chlamydia trachomatis transcriptome. Nucleic Acids Res 38: 868-877.
28. Bohn C, Rigoulay C, Chabelskaya S, Sharma CM, Marchais A, et al. (2010) Experimental discovery of small RNAs in Staphylococcus aureus reveals a riboregulator of central metabolism. Nucleic Acids Res 38: 6620-6636.
29. Guell M, van Noort V, Yus E, Chen WH, Leigh-Bell J, et al. (2009) Transcriptome complexity in a genome-reduced bacterium. Science 326: 1268-1271.
30. Bitter W, Houben EN, Luirink J, Appelmelk BJ, (2009) Type VII secretion in mycobacteria: classification in line with cell envelope structure. Trends Microbiol 17: 337-338.
31. Pym AS, Brodin P, Brosch R, Huerre M, Cole ST, (2002) Loss of RD1 contributed to the attenuation of the live tuberculosis vaccines Mycobacterium bovis BCG and Mycobacterium microti. Mol Microbiol 46: 709-717.
32. Skjot RL, Oettinger T, Rosenkrands I, Ravn P, Brock I, et al. (2000) Comparative evaluation of low-molecular-mass proteins from Mycobacterium tuberculosis identifies members of the ESAT-6 family as immunodominant T-cell antigens. Infect Immun 68: 214-220.
33. Ramage HR, Connolly LE, Cox JS, (2009) Comprehensive functional analysis of Mycobacterium tuberculosis toxin-antitoxin systems: implications for pathogenesis, stress responses, and evolution. PLoS Genet 5: e1000767.
34. Rustad TR, Sherrid AM, Minch KJ, Sherman DR, (2009) Hypoxia: a window into Mycobacterium tuberculosis latency. Cell Microbiol 11: 1151-1159.
35. Rutherford K, Parkhill J, Crook J, Horsnell T, Rice P, et al. (2000) Artemis: sequence visualization and annotation. Bioinformatics 16: 944-945.
36. Sorek R, Kunin V, Hugenholtz P, (2008) CRISPR--a widespread system that provides acquired resistance against phages in bacteria and archaea. Nat Rev Microbiol 6: 181-186.
37. Karginov FV, Hannon GJ, (2010) The CRISPR system: small RNA-guided defense in bacteria and archaea. Mol Cell 37: 7-19.
38. Gardner PP, Daub J, Tate JG, Nawrocki EP, Kolbe DL, et al. (2009) Rfam: updates to the RNA families database. Nucleic Acids Res 37: D136-140.
39. Stewart GR, Wernisch L, Stabler R, Mangan JA, Hinds J, et al. (2002) Dissection of the heat-shock response in Mycobacterium tuberculosis using mutants and microarrays. Microbiology 148: 3129-3138.
40. Torarinsson E, Lindgreen S, (2008) WAR: Webserver for aligning structural RNAs. Nucleic Acids Res 36: W79-84.
41. Lindahl L, Zengel JM, (1986) Ribosomal genes in Escherichia coli. Annu Rev Genet 20: 297-326.
42. Vitreschak AG, Mironov AA, Lyubetsky VA, Gelfand MS, (2008) Comparative genomic analysis of T-box regulatory systems in bacteria. Rna 14: 717-735.
43. Warner DF, Savvi S, Mizrahi V, Dawes SS, (2007) A riboswitch regulates expression of the coenzyme B12-independent methionine synthase in Mycobacterium tuberculosis: implications for differential methionine synthase function in strains H37Rv and CDC1551. J Bacteriol 189: 3655-3659.
44. Hobson RJ, McBride AJ, Kempsell KE, Dale JW, (2002) Use of an arrayed promoter-probe library for the identification of macrophage-regulated genes in Mycobacterium tuberculosis. Microbiology 148: 1571-1579.
45. Rickman L, Scott C, Hunt DM, Hutchinson T, Menendez MC, et al. (2005) A member of the cAMP receptor protein family of transcription regulators in Mycobacterium tuberculosis is required for virulence in mice and controls transcription of the rpfA gene coding for a resuscitation promoting factor. Mol Microbiol 56: 1274-1286.
46. Lun DS, Sherrid A, Weiner B, Sherman DR, Galagan JE, (2009) A blind deconvolution approach to high-resolution mapping of transcription factor binding sites from ChIP-seq data. Genome Biol 10: R142.
47. Raman K, Chandra N, (2008) Mycobacterium tuberculosis interactome analysis unravels potential pathways to drug resistance. BMC Microbiol 8: 234.
48. Manganelli R, Voskuil MI, Schoolnik GK, Smith I (2001) The Mycobacterium tuberculosis ECF sigma factor sigmaE: role in global gene expression and survival in macrophages. Mol Microbiol 41: 423-437.
49. Sun R, Converse PJ, Ko C, Tyagi S, Morrison NE, et al. (2004) Mycobacterium tuberculosis ECF sigma factor sigC is required for lethality in mice and for the conditional expression of a defined gene set. Mol Microbiol 52: 25-38.
50. Munoz-Elias EJ, Timm J, Botha T, Chan WT, Gomez JE, et al. (2005) Replication dynamics of Mycobacterium tuberculosis in chronically infected mice. Infect Immun 73: 546-551.
51. Gill WP, Harik NS, Whiddon MR, Liao RP, Mittler JE, et al. (2009) A replication clock for Mycobacterium tuberculosis. Nat Med 15: 211-214.
52. Rees RJ, Hart PD, (1961) Analysis of the host-parasite equilibrium in chronic murine tuberculosis by total and viable bacillary counts. Br J Exp Pathol 42: 83-88.
53. Chao MC, Rubin EJ, (2010) Letting sleeping dos lie: does dormancy play a role in tuberculosis? Annu Rev Microbiol 64: 293-311.
54. Komorowski M, Miekisz J, Kierzek AM, (2009) Translational repression contributes greater noise to gene expression than transcriptional repression. Biophys J 96: 372-384.
55. Vliet v, (2010) Next generation sequencing of microbial transcriptomes: challenges and opportunities. FEMS Microiol Lett 302: 1-7.
56. Jones GJ, Gordon SV, Hewinson RG, Vordermeier HM, (2010) Screening of predicted secreted antigens from Mycobacterium bovis reveals the immunodominance of the ESAT-6 protein family. Infect Immun 78: 1326-1332.
57. Georg J, Hess WR, (2011) cis-antisense RNA, another level of gene regulation in bacteria. Microbiol Mol Biol Rev 75: 286-300.
58. Epshtein V, Cardinale CJ, Ruckenstein AE, Borukhov S, Nudler E, (2007) An allosteric path to transcription termination. Mol Cell 28: 991-1001.
59. Unniraman S, Prakash R, Nagaraja V, (2002) Conserved economics of transcription termination in eubacteria. Nucleic Acids Res 30: 675-684.
60. Mitra A, Angamuthu K, Nagaraja V, (2008) Genome-wide analysis of the intrinsic terminators of transcription across the genus Mycobacterium. Tuberculosis 88: 566-575.
61. Pul U, Wurm R, Arslan Z, Geissen R, Hofmann N, et al. (2010) Identification and characterization of E. coli CRISPR-cas promoters and their silencing by H-NS. Mol Microbiol 75: 1495-1512.
62. Choonee N, Even S, Zig L, Putzer H, (2007) Ribosomal protein L20 controls expression of the Bacillus subtilis infC operon via a transcription attenuation mechanism. Nucleic Acids Res 35: 1578-1588.
63. Homuth G, Mogk A, Schumann W, (1999) Post-transcriptional regulation of the Bacillus subtilis dnaK operon. Mol Microbiol 32: 1183-1197.
64. Jager S, Jager A, Klug G, (2004) CIRCE is not involved in heat-dependent transcription of groESL but in stabilization of the mRNA 5'-end in Rhodobacter capsulatus. Nucleic Acids Res 32: 386-396.
65. Datta P, Shi L, Bibi N, Balazsi G, Gennaro ML, (2011) Regulation of central metabolism genes of Mycobacterium tuberculosis by parallel feed-forward loops controlled by sigma factor E (σ(E)). J Bacteriol 193: 1154-1160.
66. Micklinghoff JC, Breitinger KJ, Schmidt M, Geffers R, Eikmanns BJ, et al. (2009) Role of the transcriptional regulator RamB (Rv0465c) in the control of the glyoxylate cycle in Mycobacterium tuberculosis. J Bacteriol 191: 7260-7269.
67. Boshoff HI, Myers TG, Copp BR, McNeil MR, Wilson MA, et al. (2004) The transcriptional responses of Mycobacterium tuberculosis to inhibitors of metabolism: novel insights into drug mechanisms of action. J Biol Chem 279: 40174-40184.
68. Trotochaud AE, Wassarman KM, (2005) A highly conserved 6S RNA structure is required for regulation of transcription. Nat Struct Mol Biol 12: 313-319.
69. Panek J, Krasny L, Bobek J, Jezkova E, Korelusova J, et al. (2011) The suboptimal structures find the optimal RNAs: homology search for bacterial non-coding RNAs using suboptimal RNA structures. Nucleic Acids Res 39: 3418-3426.
70. Keren I, Minami S, Rubin E, Lewis K, (2011) Characterization and Transcriptome Analysis of Mycobacterium tuberculosis Persisters. MBio 2: e00100-00111.
71. Papavinasasundaram KP, Anderson C, Brooks PC, Thomas NA, Movahedzadeh F, et al. (2001) Slow induction of RecA by DNA damage in Mycobacterium tuberculosis. Microbiology 147: 3271-3279.
72. Snapper SB, Melton RE, Mustafa S, Kieser T, Jacobs WRJ, (1990) Isolation and characterization of efficient plasmid transformation mutants of Mycobacterium smegmatis. Mol Microbiol 4: 1911-1919.
73. Croucher NJ, Fookes MC, Perkins TT, Turner DJ, Marguerat SB, et al. (2009) A simple method for directional transcriptome sequencing using Illumina technology. Nucleic Acids Res 37: e148.
74. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, et al. (2009) The Sequence Alignment/Map format and SAMtools. Bioinformatics 25: 2078-2079.
75. Hunt DM, Saldanha JW, Brennan JF, Benjamin P, Strom M, et al. (2008) Single nucleotide polymorphisms that cause structural changes in the cyclic AMP receptor protein transcriptional regulator of the tuberculosis vaccine strain Mycobacterium bovis BCG alter global gene expression without attenuating growth. Infect Immun 76: 2227-2234.
76. Benjamini Y, Hochberg Y, (1995) Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing. J R Stat Soc Series B Stat Methodol 57: 289-300.
77. Smoot ME, Ono K, Ruscheinski J, Wang PL, Ideker T, (2011) Cytoscape 2.8: new features for data integration and network visualization. Bioinformatics 27: 431-432.