6S RNA, a global regulator of transcription in escherichia coli, bacillus subtilis, and beyond

Annual Review of Microbiology

Volumn 68, Issue , 2014, Pages 45-60

  Cavanagh, Amy T ^a   Wassarman, Karen M ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Global regulation; PRNA; SRNA; ssrS; Stationary phase; Stress response

Indexed keywords

BACTERIAL RNA; RNA 6S; RNA POLYMERASE; SMALL UNTRANSLATED RNA; UNCLASSIFIED DRUG; 6S RNA; UNTRANSLATED RNA;

BACILLUS SUBTILIS; DOWN REGULATION; ESCHERICHIA COLI; GENE FUNCTION; INTERACTIONS WITH RNA; NONHUMAN; NUTRIENT LIMITATION; REVIEW; RNA SYNTHESIS; SURVIVAL; TRANSCRIPTION REGULATION; BACTERIUM; GENE EXPRESSION REGULATION; GENETICS; METABOLISM;

BACILLUS SUBTILIS; BACTERIA; ESCHERICHIA COLI; GENE EXPRESSION REGULATION, BACTERIAL; RNA, BACTERIAL; RNA, UNTRANSLATED;

EID: 84907029678     PISSN: 00664227     EISSN: 15453251     Source Type: Book Series    
DOI: 10.1146/annurev-micro-092611-150135     Document Type: Review

References (80)

1. Ando Y, Asari S, Suzuma S, Yamane K, Nakamura K. 2002. Expression of a small RNA, BS203 RNA, from the yocI-yocJ intergenic region of Bacillus subtilis genome. FEMS Microbiol. Lett. 207:29-33
2. Axmann IM, Holtzendorff J, Vos B, Kensche P, Hess WR. 2007. Two distinct types of 6S RNA in Prochlorococcus. Gene 406:69-78
3. Barrick JE, Sudarsan N, Weinberg Z, Ruzzo WL, Breaker RR. 2005. 6S RNA is a widespread regulator of eubacterial RNA polymerase that resembles an open promoter. RNA 11:774-84
4. Battesti A, Majdalani N, Gottesman S. 2011. The RpoS-mediated general stress response in Escherichia coli. Annu. Rev. Microbiol. 65:189-213
5. Beckmann BM, Burenina OY, Hoch PG, Kubareva EA, Sharma CM, Hartmann RK. 2011. In vivo and in vitro analysis of 6S RNA-templated short transcripts in Bacillus subtilis. RNA Biol. 8:839-49
6. Beckmann BM, Hoch PG, Marz M, Willkomm DK, Salas M, Hartmann RK. 2012. A pRNA-induced structural rearrangement triggers 6S-1 RNA release from RNA polymerase in Bacillus subtilis. EMBO J. 31:1727-38
7. Beisel CL, Storz G. 2010. Base pairing small RNAs and their roles in global regulatory networks. FEMS Microbiol. Rev. 34:866-82
8. Berghoff BA, Glaeser J, Sharma CM, Vogel J, Klug G. 2009. Photooxidative stress-induced and abundant small RNAs in Rhodobacter sphaeroides. Mol. Microbiol. 74:1497-512
9. Blattner FR, PlunkettG3rd, BlochCA, PernaNT, BurlandV, et al. 1997. The complete genome sequence of Escherichia coli K-12. Science 277:1453-62
10. Burenina OY, Hoch PG,Damm K, Salas M, ZatsephinTS, et al. 2014. Mechanistic comparison of Bacillus subtilis 6S-1 and 6S-2 RNAs-commonalities and differences. RNA 20:348-59
11. Cabrera-Ostertag IJ, Cavanagh AT, Wassarman KM. 2013. Initiating nucleotide identity determines efficiency of RNA synthesis from 6S RNA templates in Bacillus subtilis but not Escherichia coli. Nucleic Acids Res. 41:7501-11
12. Cavanagh AT, Chandrangsu P, Wassarman KM. 2010. 6S RNA regulation of relA alters ppGpp levels in early stationary phase. Microbiology 156:3791-800
13. Cavanagh AT, Klocko AD, Liu X, Wassarman KM. 2008. Promoter specificity for 6S RNA regulation of transcription is determined by core promoter sequences and competition for region 4.2 of σ70. Mol. Microbiol. 67:1242-56
14. Cavanagh AT, Sperger JM,Wassarman KM. 2012. Regulation of 6S RNA by pRNA synthesis is required for efficient recovery from stationary phase in E. coli and B. subtilis. Nucleic Acids Res. 40:2234-46
15. Cavanagh AT,Wassarman KM. 2013. 6S-1 RNA function leads to a delay in sporulation in Bacillus subtilis. J. Bacteriol. 195:2079-86
16. Chae H, Han K, Kim KS, Park H, Lee J, Lee Y. 2011. Rho-dependent termination of ssrS (6S RNA) transcription in Escherichia coli: implication for 3 processing of 6S RNA and expression of downstream ygfA (putative 5-formyl-tetrahydrofolate cyclo-ligase). J. Biol. Chem. 286:114-22
17. Chen Y, Indurthi DC, Jones SW, Papoutsakis ET. 2011. Small RNAs in the genus Clostridium. MBio 2:e00340-10
18. Darby AC, Armstrong SD, Bah GS,KaurG,Hughes MA, et al. 2012. Analysis of gene expression from the Wolbachia genome of a filarial nematode supports bothmetabolic and defensive roles within the symbiosis. Genome Res. 22:2467-77
19. Faucher SP, Friedlander G, Livny J, Margalit H, Shuman HA. 2010. Legionella pneumophila 6S RNA optimizes intracellular multiplication. Proc. Natl. Acad. Sci. USA 107:7533-38
20. Faucher SP, Shuman HA. 2011. Small regulatory RNA and Legionella pneumophila. Front. Microbiol. 2:98
21. GildehausN,Neuser T,Wurm R,Wagner R. 2007. Studies on the function of the riboregulator 6S RNA from E. coli: RNA polymerase binding, inhibition of in vitro transcription and synthesis of RNA-directed de novo transcripts. Nucleic Acids Res. 35:1885-96
22. Gruber TM, Gross CA. 2003. Multiple σ subunits and the partitioning of bacterial transcription space. Annu. Rev. Microbiol. 57:441-66
23. Hengge-Aronis R. 2002. Signal transduction and regulatory mechanisms involved in control of the σS (RpoS) subunit of RNA polymerase. Microbiol. Mol. Biol. Rev. 66:373-95
24. Higgins D, Dworkin J. 2012. Recent progress in Bacillus subtilis sporulation. FEMS Microbiol. Rev. 36:131-48
25. Hindley J. 1967. Fractionation of 32P-labelled ribonucleic acids on polyacrylamide gels and their characterization by fingerprinting. J. Mol. Biol. 30:125-36
26. Hsu LM, Zagorski J,Wang Z, Fournier MJ. 1985. Escherichia coli 6S RNA gene is part of a dual-function transcription unit. J. Bacteriol. 161:1162-70
27. IkemuraT,Dahlberg JE. 1973. Small ribonucleic acids of Escherichia coli. II. Noncoordinate accumulation during stringent control. J. Biol. Chem. 248:5033-41
28. Irnov I, Sharma CM, Vogel J, Winkler WC. 2010. Identification of regulatory RNAs in Bacillus subtilis. Nucleic Acids Res. 38:6637-51
29. Janssen BD, Hayes CS. 2012. The tmRNA ribosome-rescue system. Adv. Protein Chem. Struct. Biol. 86:151-91
30. Joly N, Engl C, Jovanovic G, Huvet M, Toni T, et al. 2010. Managing membrane stress: the phage shock protein (Psp) response, from molecular mechanisms to physiology. FEMS Microbiol. Rev. 34:797-827
31. Kim EY, Shin MS, Rhee JH, Choy HE. 2004. Factors influencing preferential utilization of RNA polymerase containing σ38 in stationary-phase gene expression in Escherichia coli. J. Microbiol. 42:103-10
32. Kim KS, Lee Y. 2004. Regulation of 6S RNA biogenesis by switching utilization of both σ factors and endoribonucleases. Nucleic Acids Res. 32:6057-68
33. Klauck E, Typas A, Hengge R. 2007. The σS subunit of RNA polymerase as a signal integrator and network master regulator in the general stress response in Escherichia coli. Sci. Prog. 90:103-27
34. Klocko AD, Wassarman KM. 2009. 6S RNA binding to Eσ70 requires a positively charged surface of σ70 region 4.2. Mol. Microbiol. 73:152-64
35. Kriel A, Bittner AN, Kim SH, Liu K, Tehranchi AK, et al. 2012. Direct regulation of GTP homeostasis by (p)ppGpp: a critical component of viability and stress resistance. Mol. Cell 48:231-41
36. Kuster B, Mann M. 1998. Identifying proteins and post-translationalmodifications by mass spectrometry. Curr. Opin. Struct. Biol. 8:393-400
37. Landt SG, Abeliuk E,McGrath PT, Lesley JA, McAdamsHH, Shapiro L. 2008. Small non-coding RNAs in Caulobacter crescentus. Mol. Microbiol. 68:600-14
38. Lee CA, Fournier MJ, Beckwith J. 1985. Escherichia coli 6S RNA is not essential for growth or protein secretion. J. Bacteriol. 161:1156-61
39. Lee JY, Park H, Bak G, Kim KS, Lee Y. 2013. Regulation of transcription from two ssrS promoters in 6S RNA biogenesis. Mol. Cells 36:227-34
40. Lee SY, Bailey SC, Apirion D. 1978. Small stable RNAs from Escherichia coli: evidence for the existence of new molecules and for a new ribonucleoprotein particle containing 6S RNA. J. Bacteriol. 133:1015-23
41. Li Z, Pandit S, DeutscherMP. 1998. 3′ exoribonucleolytic trimming is a commonfeature of thematuration of small, stable RNAs in Escherichia coli. Proc. Natl. Acad. Sci. USA 95:2856-61
42. Madhugiri R, Pessi G, Voss B, Hahn J, Sharma CM, et al. 2012. Small RNAs of the Bradyrhizobium/ Rhodopseudomonas lineage and their analysis. RNA Biol. 9:47-58
43. Magnusson LU, Farewell A, Nystrom T. 2005. ppGpp: a global regulator in Escherichia coli. Trends Microbiol. 13:236-42
44. Murakami KS. 2013. X-ray crystal structure of Escherichia coli RNA polymerase σ70 holoenzyme. J. Biol. Chem. 288:9126-34
45. MurrayHD, Schneider DA, Gourse RL. 2003. Control of rRNA expression by small molecules is dynamic and nonredundant. Mol. Cell 12:125-34
46. Neuser T, Gildehaus N, Wurm R, Wagner R. 2008. Studies on the expression of 6S RNA from E. coli: involvement of regulators important for stress and growth adaptation. Biol. Chem. 389:285-97
47. Neuser T, Polen T, Geisen R, Wagner R. 2010. Depletion of the non-coding regulatory 6S RNA in E. coli causes a surprising reduction in the expression of the translation machinery. BMC Genomics 11:165
48. Nitzan M, Wassarman KM, Biham O, Margalit H. 2014. Global regulation of transcription by a small RNA: a quantitative view. Biophys. J. 106:1205-14
49. Panchapakesan SS, Unrau PJ. 2012. E. coli 6S RNA release from RNA polymerase requires σ70 ejection by scrunching and is orchestrated by a conserved RNA hairpin. RNA 18:2251-59
50. Panek J, Bobek J, Mikulik K, Basler M, Vohradsky J. 2008. Biocomputational prediction of small noncoding RNAs in Streptomyces. BMC Genomics 9:217
51. Panek J, Krasny L, Bobek J, Jezkova E, Korelusova J, Vohradsky J. 2011. The suboptimal structures find the optimal RNAs: homology search for bacterial non-coding RNAs using suboptimal RNA structures. Nucleic Acids Res. 39:3418-26
52. PeetersE, SassA,MahenthiralingamE,Nelis H, Coenye T. 2010. Transcriptional response of Burkholderia cenocepacia J2315 sessile cells to treatments with high doses of hydrogen peroxide and sodium hypochlorite. BMC Genomics 11:90
53. Potrykus K, Cashel M. 2008. (p)ppGpp: still magical? Annu. Rev. Microbiol. 62:35-51
54. Rediger A, Geisen R, Steuten B, Heilmann B, Wagner R, Axmann IM. 2012. 6S RNA-An old issue became blue-green. Microbiology 158:2480-91
55. Romeo T, Vakulskas CA, Babitzke P. 2013. Post-transcriptional regulation on a global scale: form and function of Csr/Rsm systems. Environ. Microbiol. 15:313-24
56. Sharma CM, Hoffmann S, Darfeuille F, Reignier J, Findeiss S, et al. 2010. The primary transcriptome of the major human pathogen Helicobacter pylori. Nature 464:250-55
57. Shephard L,Dobson N, Unrau PJ. 2010. Binding and release of the 6S transcriptional control RNA. RNA 16:885-92
58. Soutourina OA, Monot M, Boudry P, Saujet L, Pichon C, et al. 2013. Genome-wide identification of regulatory RNAs in the human pathogen Clostridium difficile. PLoS Genet. 9:e1003493
59. Srivatsan A,Wang JD. 2008. Control of bacterial transcription, translation and replication by (p)ppGpp. Curr. Opin. Microbiol. 11:100-5
60. Steuten B, Schneider S, Wagner R. 2014. 6S RNA: recent answers-future questions. Mol. Microbiol. 91:641-48
61. Steuten B, Setny P, Zacharias M, Wagner R. 2013. Mapping the spatial neighborhood of the regulatory 6S RNA bound to Escherichia coli RNA polymerase holoenzyme. J. Mol. Biol. 425:3649-61
62. Steuten B, Wagner R. 2012. A conformational switch is responsible for the reversal of the 6S RNAdependent RNA polymerase inhibition in Escherichia coli. Biol. Chem. 393:1513-22
63. Storz G, Vogel J,Wassarman KM. 2011. Regulation by small RNAs in bacteria: expanding frontiers. Mol. Cell 43:880-91
64. Suzuma S, Asari S, Bunai K, Yoshino K, Ando Y, et al. 2002. Identification and characterization of novel small RNAs in the aspS-yrvM intergenic region of the Bacillus subtilis genome. Microbiology 148:2591-98
65. Trotochaud AE, Wassarman KM. 2004. 6S RNA function enhances long-term cell survival. J. Bacteriol. 186:4978-85
66. Trotochaud AE,Wassarman KM. 2005. A highly conserved 6S RNA structure is required for regulation of transcription. Nat. Struct. Mol. Biol. 12:313-19
67. Trotochaud AE, Wassarman KM. 2006. 6S RNA regulation of pspF transcription leads to altered cell survival at high pH. J. Bacteriol. 188:3936-43
68. Venkataramanan KP, Jones SW, McCormick KP, Kunjeti SG, Ralston MT, et al. 2013. The Clostridium small RNome that responds to stress: the paradigm and importance of toxic metabolite stress in C. acetobutylicum. BMC Genomics 14:849
69. Vogel DW, Hartmann RK, Struck JC, Ulbrich N, Erdmann VA. 1987. The sequence of the 6S RNA gene of Pseudomonas aeruginosa. Nucleic Acids Res. 15:4583-91
70. Voss B, Holscher M, Baumgarth B, Kalbfleisch A, Kaya C, et al. 2009. Expression of small RNAs in Rhizobiales and protection of a small RNA and its degradation products by Hfq in Sinorhizobium meliloti. Biochem. Biophys. Res. Commun. 390:331-36
71. Wassarman KM. 2011. 6S RNA: a regulator of transcription. In Regulatory RNA in Prokaryotes, ed.WR Hess, A Marchfelder, pp. 109-129. New York: SpringerWein
72. Wassarman KM, Saecker RM. 2006. Synthesis-mediated release of a small RNA inhibitor of RNA polymerase. Science 314:1601-3
73. Wassarman KM, Storz G. 2000. 6S RNA regulates E. coli RNA polymerase activity. Cell 101:613-23
74. Watanabe T, SugiuraM, Sugita M. 1997. A novel small stable RNA, 6Sa RNA, from the cyanobacterium Synechococcus sp. strain PCC6301. FEBS Lett. 416:302-6
75. Weissenmayer BA, Prendergast JG, Lohan AJ, Loftus BJ. 2011. Sequencing illustrates the transcriptional response of Legionella pneumophila during infection and identifies seventy novel small non-coding RNAs. PLoS ONE 6:e17570
76. Willkomm DK, Hartmann RK. 2005. 6S RNA-an ancient regulator of bacterial RNA polymerase rediscovered. Biol. Chem. 386:1273-77
77. Willkomm DK, Minnerup J, Huttenhofer A, Hartmann RK. 2005. Experimental RNomics in Aquifex aeolicus: identification of small non-coding RNAs and the putative 6S RNA homolog. Nucleic Acids Res. 33:1949-60
78. Windbichler N, von Pelchrzim F, Mayer O, Csaszar E, Schroeder R. 2008. Isolation of small RNAbinding proteins from E. coli: evidence for frequent interaction of RNAs with RNA polymerase. RNA Biol. 5:30-40
79. Wurm R, Neuser T,Wagner R. 2010. 6S RNA-dependent inhibition of RNA polymerase is released by RNA-dependent synthesis of small de novo products. Biol. Chem. 391:187-96
80. Yan Y, Su S,Meng X, Ji X, Qu Y, et al. 2013. Determination of sRNA expressions by RNA-seq in Yersinia pestis grown in vitro and during infection. PLoS ONE 8:e74495