Pervasive transcription: Illuminating the dark matter of bacterial transcriptomes

Nature Reviews Microbiology

Volumn 12, Issue 9, 2014, Pages 647-653

  Wade, Joseph T ^a,b   Grainger, David C ^c  

^a NEW YORK STATE DEPARTMENT OF HEALTH   (United States)

^b STATE UNIVERSITY OF NEW YORK   (United States)

^c UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL RNA; HISTONE LIKE NUCLEOID STRUCTURING PROTEIN; MESSENGER RNA; RIBOSOME RNA; SIGMA FACTOR; SPACER DNA; TRANSCRIPTOME; TRANSFER RNA; UNTRANSLATED RNA;

ARTIFACT; BACTERIAL CHROMOSOME; BACTERIAL GENOME; CHROMOSOME REARRANGEMENT; DNA DAMAGE; DNA REPLICATION; DNA STRAND; GENE CONTROL; GENE FUNCTION; GENE MAPPING; GENE REGULATORY NETWORK; GENETIC REGULATION; GENETIC TRANSCRIPTION; GENOME ANALYSIS; GENOMIC INSTABILITY; MOLECULAR EVOLUTION; NONHUMAN; NONSENSE MUTATION; OVERLAPPING GENE; PHYLOGENY; PLEIOTROPY; PRIORITY JOURNAL; PROMOTER REGION; REVIEW; RNA DEGRADATION; RNA PROCESSING; RNA STRUCTURE; RNA TRANSLATION; TRANSCRIPTION ELONGATION; TRANSCRIPTION INITIATION; TRANSCRIPTION INITIATION SITE;

BACTERIA; BACTERIAL PROTEINS; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION, BACTERIAL; GENOME, BACTERIAL; RNA STABILITY; RNA, ANTISENSE; RNA, BACTERIAL; RNA, MESSENGER; RNA, UNTRANSLATED; TRANSCRIPTION INITIATION SITE; TRANSCRIPTION, GENETIC; TRANSCRIPTOME;

EID: 84906316682     PISSN: 17401526     EISSN: 17401534     Source Type: Journal    
DOI: 10.1038/nrmicro3316     Document Type: Review

References (60)

1. Pearson, H. What is a gene? Nature 441, 398-401 (2006).
2. Kapranov, P. et al. RNA maps reveal new RNA classes and a possible function for pervasive transcription. Science 316, 1484-1488 (2007).
3. Okazaki, Y. et al. Analysis of the mouse transcriptome based on functional annotation of 60,770 full-length cDNAs. Nature 420, 563-573 (2002).
4. Velculescu, V. E. et al. Characterization of the yeast transcriptome. Cell 88, 243-251 (1997).
5. Selinger, D. W. et al. RNA expression analysis using a 30 base pair resolution Escherichia coli genome array. Nature Biotech. 18, 1262-1268 (2000).
6. Slonczewski, J. L. Concerns about recently identified widespread antisense transcription in Escherichia coli. mBio 1, e00106-10 (2010).
7. Robertson, M. The evolution of gene regulation, the RNA universe, and the vexed questions of artefact and noise. BMC Biol. 8, 97 (2010).
8. Robinson, R. Dark matter transcripts: Sound and fury, signifying nothing? PLoS Biol. 8, e1000370 (2010).
9. van Bakel, H., Nislow, C., Blencowe, B. J. & Hughes, T. R. Most 'dark matter' transcripts are associated with known genes. PLoS Biol. 8, e1000371 (2010).
10. Dornenburg, J. E., Devita, A. M., Palumbo, M. J. & Wade, J. T. Widespread antisense transcription in Escherichia coli. mBio 1, e00024-10 (2010).
11. Sharma, C. M. et al. The primary transcriptome of the major human pathogen Helicobacter pylori. Nature 464, 250-255 (2010).
12. Mitschke, J. et al. An experimentally anchored map of transcriptional start sites in the model cyanobacterium Synechocystis sp. PCC6803. Proc. Natl Acad. Sci. USA 108, 2124-2129 (2011).
13. Raghavan, R., Sloan, D. B. & Ochman, H. Antisense transcription is pervasive but rarely conserved in enteric bacteria. mBio 3, e00156-12 (2012).
14. Lasa, I. et al. Genome-wide antisense transcription drives mRNA processing in bacteria. Proc. Natl Acad. Sci. USA 108, 20172-20177 (2011).
15. Kawano, M., Storz, G., Rao, B. S., Rosner, J. L. & Martin, R. G. Detection of low-level promoter activity within open reading frame sequences of Escherichia coli. Nucleic Acids Res. 33, 6268-6276 (2005).
16. Reppas, N. B., Wade, J. T., Church, G. M. & Struhl, K. The transition between transcriptional initiation and elongation in E. coli is highly variable and often rate limiting. Mol. Cell 24, 747-757 (2006).
17. Wade, J. T. et al. Extensive functional overlap between sigma factors in Escherichia coli. Nature Struct. Mol. Biol. 13, 806-814 (2006).
18. Mooney, R. A. et al. Regulator trafficking on bacterial transcription units in vivo. Mol. Cell 33, 97-108 (2009).
19. Singh, S. S. et al. Widespread suppression of intragenic transcription initiation by H NS. Genes Dev. 28, 214-219 (2014).
20. Shimada, T., Yamazaki, Y., Tanaka, K. & Ishihama, A. The whole set of constitutive promoters recognized by RNA polymerase RpoD holoenzyme of Escherichia coli. PLoS ONE 9, e90447 (2014).
21. Jensen, T. H., Jacquier, A. & Libri, D. Dealing with pervasive transcription. Mol. Cell 52, 473-484 (2013).
22. Lee, D. J., Minchin, S. D. & Busby, S. J. Activating transcription in bacteria. Annu. Rev. Microbiol. 66, 125-152 (2012).
23. Epshtein, V., Dutta, D., Wade, J. & Nudler, E. An allosteric mechanism of Rho-dependent transcription termination. Nature 463, 245-249 (2010).
24. Ciampi, M. S. Rho-dependent terminators and transcription termination. Microbiology 152, 2515-2528 (2006).
25. Singh, N. & Wade, J. T. Identification of regulatory RNA in bacterial genomes by genome-scale mapping of transcription start sites. Methods Mol. Biol. 1103, 1-10 (2014).
26. Kim, D. et al. Comparative analysis of regulatory elements between Escherichia coli and Klebsiella pneumoniae by genome-wide transcription start site profiling. PLoS Genet. 8, e1002867 (2012).
27. Cho, B. K., Kim, D., Knight, E. M., Zengler, K. & Palsson, B. O. Genome-scale reconstruction of the sigma factor network in Escherichia coli: Topology and functional states. BMC Biol. 12, 4 (2014).
28. Cho, B. K. et al. The transcription unit architecture of the Escherichia coli genome. Nature Biotech. 27, 1043-1049 (2009).
29. Stringer, A. M. et al. Genome-scale analyses of Escherichia coli and Salmonella enterica AraC reveal noncanonical targets and an expanded core regulon. J. Bacteriol. 196, 660-671 (2014).
30. Chen, Y. J. et al. Characterization of 582 natural and synthetic terminators and quantification of their design constraints. Nature Methods 10, 659-664 (2013).
31. Nicolas, P. et al. Condition-dependent transcriptome reveals high-level regulatory architecture in Bacillus subtilis. Science 335, 1103-1106 (2012).
32. Leela, J. K., Syeda, A. H., Anupama, K. & Gowrishankar, J. Rho-dependent transcription termination is essential to prevent excessive genome wide R loops in Escherichia coli. Proc. Natl Acad. Sci. USA 110, 258-223 (2013).
33. Gan, W. et al. R loop-mediated genomic instability is caused by impairment of replication fork progression. Genes Dev. 25, 2041-2056 (2011).
34. Dame, R. T., Noom, M. C. & Wuite, G. J. Bacterial chromatin organization by H NS protein unravelled using dual DNA manipulation. Nature 444, 387-390 (2006).
35. Peters, J. M. et al. Rho and NusG suppress pervasive antisense transcription in Escherichia coli. Genes Dev. 26, 2621-2633 (2012).
36. Chandraprakash, D. & Seshasayee, A. S. Inhibition of factor-dependent transcription termination in Escherichia coli might relieve xenogene silencing by abrogating H NS-DNA interactions in vivo. J. Biosci. 39, 53-61 (2014).
37. Durand, S., Gilet, L. & Condon, C. The essential function of B. subtilis RNase III is to silence foreign toxin genes. PLoS Genet. 8, e1003181 (2012).
38. Goldman, S. R. et al. NanoRNAs prime transcription initiation in vivo. Mol. Cell 42, 817-825 (2011).
39. Panyukov, V. V. & Ozoline, O. N. Promoters of Escherichia coli versus promoter islands: Function and structure comparison. PLoS ONE 8, e62601 (2013).
40. Mercer, T. R. et al. The human mitochondrial transcriptome. Cell 146, 645-658 (2011).
41. Shao, W., Price, M. N., Deutschbauer, A. M., Romine, M. F. & Arkin, A. P. Conservation of transcription start sites within genes across a bacterial genus. mBio 5, e01398-14 (2014).
42. Lybecker, M., Zimmermann, B., Bilusic, I., Tukhtubaeva, N. & Schroeder, R. The double-stranded transcriptome of Escherichia coli. Proc. Natl Acad. Sci. USA 111, 3134-3139 (2014).
43. Georg, J. & Hess, W. R. cis-Antisense RNA, another level of gene regulation in bacteria. Microbiol. Mol. Biol. Rev. 75, 286-300 (2011).
44. Brantl, S. & Wagner, E. G. An antisense RNA-mediated transcriptional attenuation mechanism functions in Escherichia coli. J. Bacteriol. 184, 2740-2747 (2002).
45. Lasa, I., Toledo-Arana, A. & Gingeras, T. R. An effort to make sense of antisense transcription in bacteria. RNA Biol. 9, 1039-1044 (2012).
46. Sesto, N., Wurtzel, O., Archambaud, C., Sorek, R. & Cossart, P. The excludon: A new concept in bacterial antisense RNA-mediated gene regulation. Nature Rev. Microbiol. 11, 75-82 (2013).
47. Wurtzel, O. et al. Comparative transcriptomics of pathogenic and non-pathogenic Listeria species. Mol. Syst. Biol. 8, 583 (2012).
48. Mutalik, V. K., Qi, L., Guimaraes, J. C., Lucks, J. B. & Arkin, A. P. Rationally designed families of orthogonal RNA regulators of translation. Nature Chem. Biol. 25, 447-454 (2012).
49. Navarre, W. W. et al. Selective silencing of foreign DNA with low GC content by the H NS protein in Salmonella. Science 313, 236-238 (2006).
50. Martincorena, I., Seshasayee, A. S. & Luscombe, N. M. Evidence of non-random mutation rates suggests an evolutionary risk management strategy. Nature 485, 95-98 (2012).
51. Epshtein, V. et al. UvrD facilitates DNA repair by pulling RNA polymerase backwards. Nature 505, 372-377 (2014).
52. Savery, N. J. The molecular mechanism of transcription-coupled DNA repair. Trends Microbiol. 15, 326-333 (2007).
53. Chao, Y., Papenfort, K., Reinhardt, R., Sharma, C. M. & Vogel, J. An atlas of Hfq-bound transcripts reveals 3? UTRs as a genomic reservoir of regulatory small RNAs. EMBO J. 31, 4005-4019 (2012).
54. Gibson, D. G. et al. Creation of a bacterial cell controlled by a chemically synthesized genome. Science 329, 52-56 (2010).
55. Wiser, M. J., Ribeck, N. & Lenski, R. E. Long-Term dynamics of adaptation in asexual populations. Science. 342, 1364-1367 (2013).
56. Herring, C. D. et al. Immobilization of Escherichia coli RNA polymerase and location of binding sites by use of chromatin immunoprecipitation and microarrays. J. Bacteriol. 187, 6166-6174 (2005).
57. Grainger, D. C., Hurd, D., Harrison, M., Holdstock, J. & Busby, S. J. Studies of the distribution of Escherichia coli cAMP-receptor protein and RNA polymerase along the E. coli chromosome. Proc. Natl Acad. Sci. USA 102, 17693-17698 (2005).
58. Streets, A. M. et al. Microfluidic single-cell whole-Transcriptome sequencing. Proc. Natl Acad. Sci. USA 111, 7048-7053 (2014).
59. Steuten, B. et al. Regulation of transcription by 6S RNAs: Insights from the Escherichia coli and Bacillus subtilis model systems. RNA Biol. http://dx.doi. org/10.4161/rna.28827 (2014).
60. Waters, L. S. & Storz, G. Regulatory RNAs in bacteria. Cell 136, 615-628 (2009)..