1887

Abstract

Factor-dependent termination of transcription in bacteria relies on the activity of a specific RNA helicase, the termination factor Rho. Rho is nearly ubiquitous in bacteria, but the extent to which its physiological functions are conserved throughout the different phyla remains unknown. Most of our current knowledge concerning the mechanism of Rho's activity and its physiological roles comes from the model micro-organism , where Rho is essential and involved in the control of several important biological processes. However, the rather comprehensive knowledge about the general mechanisms of action and activities of Rho based on the paradigm cannot be directly extrapolated to other bacteria. Recent studies performed in different species favour the view that Rho-dependent termination plays a significant role even in bacteria where Rho is not essential. Here, we summarize the current state of the ever-increasing knowledge about the various aspects of the physiological functions of Rho, such as limitation of deleterious foreign DNA expression, control of gene expression, suppression of pervasive transcription, prevention of R-loops and maintenance of chromosome integrity, focusing on similarities and differences of the activities of Rho in various bacterial species.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.000244
2016-03-01
2019-10-20
Loading full text...

Full text loading...

/deliver/fulltext/micro/162/3/433.html?itemId=/content/journal/micro/10.1099/mic.0.000244&mimeType=html&fmt=ahah

References

  1. Aguilera A. , García-Muse T. . ( 2012;). R loops: from transcription by products to threats to genome stability. Mol Cell 46: 115–124 [CrossRef] [PubMed].
    [Google Scholar]
  2. Babitzke P. , Gollnick P. . ( 2001;). Posttranscription initiation control of tryptophan metabolism in Bacillus subtilis by the trp RNA-binding attenuation protein (TRAP), anti-TRAP, and RNA structure. J Bacteriol 183: 5795–5802 [CrossRef] [PubMed].
    [Google Scholar]
  3. Bogden C. E. , Fass D. , Bergman N. , Nichols M. D. , Berger J. M. . ( 1999;). The structural basis for terminator recognition by the Rho transcription termination factor. Mol Cell 3: 487–493 [CrossRef] [PubMed].
    [Google Scholar]
  4. Borukhov S. , Lee J. , Laptenko O. . ( 2005;). Bacterial transcription elongation factors: new insights into molecular mechanism of action. Mol Microbiol 55: 1315–1324 [CrossRef] [PubMed].
    [Google Scholar]
  5. Bossi L. , Schwartz A. , Guillemardet B. , Boudvillain M. , Figueroa-Bossi N. . ( 2012;). A role for Rho-dependent polarity in gene regulation by a noncoding small RNA. Genes Dev 26: 1864–1873 [CrossRef] [PubMed].
    [Google Scholar]
  6. Boubakri H. , de Septenville A. L. , Viguera E. , Michel B. . ( 2010;). The helicases DinG, Rep and UvrD cooperate to promote replication across transcription units in vivo . EMBO J 29: 145–157 [CrossRef] [PubMed].
    [Google Scholar]
  7. Boudvillain M. , Figueroa-Bossi N. , Bossi L. . ( 2013;). Terminator still moving forward: expanding roles for Rho factor. Curr Opin Microbiol 16: 118–124 [CrossRef] [PubMed].
    [Google Scholar]
  8. Bubunenko M. , Baker T. , Court D. L. . ( 2007;). Essentiality of ribosomal and transcription antitermination proteins analyzed by systematic gene replacement in Escherichia coli . J Bacteriol 189: 2844–2853 [CrossRef] [PubMed].
    [Google Scholar]
  9. Burmann B. M. , Schweimer K. , Luo X. , Wahl M. C. , Stitt B. L. , Gottesman M. E. , Rösch P. . ( 2010;). A NusE : NusG complex links transcription and translation. Science 328: 501–504 [CrossRef] [PubMed].
    [Google Scholar]
  10. Burns C. M. , Richardson L. V. , Richardson J. P. . ( 1998;). Combinatorial effects of NusA and NusG on transcription elongation and Rho-dependent termination in Escherichia coli . J Mol Biol 278: 307–316 [CrossRef] [PubMed].
    [Google Scholar]
  11. Butland G. , Peregrín-Alvarez J. M. , Li J. , Yang W. , Yang X. , Canadien V. , Starostine A. , Richards D. , Beattie B. , other authors . ( 2005;). Interaction network containing conserved and essential protein complexes in Escherichia coli . Nature 433: 531–537 [CrossRef] [PubMed].
    [Google Scholar]
  12. Cardinale C. J. , Washburn R. S. , Tadigotla V. R. , Brown L. M. , Gottesman M. E. , Nudler E. . ( 2008;). Termination factor Rho and its cofactors NusA and NusG silence foreign DNA in E. coli . Science 320: 935–938 [CrossRef] [PubMed].
    [Google Scholar]
  13. Chandraprakash D. , Seshasayee A. S. . ( 2014;). 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 [CrossRef] [PubMed].
    [Google Scholar]
  14. Ciampi M. S. . ( 2006;). Rho-dependent terminators and transcription termination. Microbiology 152: 2515–2528 [CrossRef] [PubMed].
    [Google Scholar]
  15. Cole S. T. , Brosch R. , Parkhill J. , Garnier T. , Churcher C. , Harris D. , Gordon S. V. , Eiglmeier K. , Gas S. , other authors . ( 1998;). Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393: 537–544 [CrossRef] [PubMed].
    [Google Scholar]
  16. Czyz A. , Mooney R. A. , Iaconi A. , Landick R. . ( 2014;). Mycobacterial RNA polymerase requires a U-tract at intrinsic terminators and is aided by NusG at suboptimal terminators. MBio 5: e00931–e00e14 [CrossRef] [PubMed].
    [Google Scholar]
  17. D'Heygère F. , Rabhi M. , Boudvillain M. . ( 2013;). Phyletic distribution and conservation of the bacterial transcription termination factor Rho. Microbiology 159: 1423–1436 [CrossRef] [PubMed].
    [Google Scholar]
  18. D'Heygère F. , Schwartz A. , Coste F. , Castaing B. , Boudvillain M. . ( 2015;). ATP-dependent motor activity of the transcription termination factor Rho from Mycobacterium tuberculosis . Nucleic Acids Res 43: 6099–6111 [CrossRef] [PubMed].
    [Google Scholar]
  19. de Hoon M. J. , Makita Y. , Nakai K. , Miyano S. . ( 2005;). Prediction of transcriptional terminators in Bacillus subtilis and related species. PLoS Comput Biol 1: e25 [CrossRef] [PubMed].
    [Google Scholar]
  20. De Septenville A. L. , Duigou S. , Boubakri H. , Michel B. . ( 2012;). Replication fork reversal after replication-transcription collision. PLoS Genet 8: e1002622 [CrossRef] [PubMed].
    [Google Scholar]
  21. Doherty G. P. , Meredith D. H. , Lewis P. J. . ( 2006;). Subcellular partitioning of transcription factors in Bacillus subtilis . J Bacteriol 188: 4101–4110 [CrossRef] [PubMed].
    [Google Scholar]
  22. Dornenburg J. E. , Devita A. M. , Palumbo M. J. , Wade J. T. . ( 2010;). Widespread antisense transcription in Escherichia coli . MBio 1: e00024–e00e10 [CrossRef] [PubMed].
    [Google Scholar]
  23. Drolet M. , Broccoli S. , Rallu F. , Hraiky C. , Fortin C. , Massé E. , Baaklini I. . ( 2003;). The problem of hypernegative supercoiling and R-loop formation in transcription. Front Biosci 8: d210–d221 [CrossRef] [PubMed].
    [Google Scholar]
  24. Dutta D. , Shatalin K. , Epshtein V. , Gottesman M. E. , Nudler E. . ( 2011;). Linking RNA polymerase backtracking to genome instability in E. coli . Cell 146: 533–543 [CrossRef] [PubMed].
    [Google Scholar]
  25. Epshtein V. , Cardinale C. J. , Ruckenstein A. E. , Borukhov S. , Nudler E. . ( 2007;). An allosteric path to transcription termination. Mol Cell 28: 991–1001 [CrossRef] [PubMed].
    [Google Scholar]
  26. Epshtein V. , Dutta D. , Wade J. , Nudler E. . ( 2010;). An allosteric mechanism of Rho-dependent transcription termination. Nature 463: 245–249 [CrossRef] [PubMed].
    [Google Scholar]
  27. Figueroa-Bossi N. , Schwartz A. , Guillemardet B. , D'Heygère F. , Bossi L. , Boudvillain M. . ( 2014;). RNA remodeling by bacterial global regulator CsrA promotes Rho-dependent transcription termination. Genes Dev 28: 1239–1251 [CrossRef] [PubMed].
    [Google Scholar]
  28. Gan W. , Guan Z. , Liu J. , Gui T. , Shen K. , Manley J. L. , Li X. . ( 2011;). R-loop-mediated genomic instability is caused by impairment of replication fork progression. Genes Dev 25: 2041–2056 [CrossRef] [PubMed].
    [Google Scholar]
  29. Georg J. , Hess W. R. . ( 2011;). cis-Antisense RNA, another level of gene regulation in bacteria. Microbiol Mol Biol Rev 75: 286–300 [CrossRef] [PubMed].
    [Google Scholar]
  30. Gocheva V. , Le Gall A. , Boudvillain M. , Margeat E. , Nollmann M. . ( 2015;). Direct observation of the translocation mechanism of transcription termination factor Rho. Nucleic Acids Res 43: 2367–2377 [CrossRef] [PubMed].
    [Google Scholar]
  31. Gomelsky M. , Kaplan S. . ( 1996;). The Rhodobacter sphaeroides 2.4.1 rho gene: expression and genetic analysis of structure and function. J Bacteriol 178: 1946–1954 [PubMed].
    [Google Scholar]
  32. Gowrishankar J. , Harinarayanan R. . ( 2004;). Why is transcription coupled to translation in bacteria?. Mol Microbiol 54: 598–603 [CrossRef] [PubMed].
    [Google Scholar]
  33. Gowrishankar J. , Leela J. K. , Anupama K. . ( 2013;). R-loops in bacterial transcription: their causes and consequences. Transcription 4: 153–157 [CrossRef] [PubMed].
    [Google Scholar]
  34. Griffin J. E. , Gawronski J. D. , Dejesus M. A. , Ioerger T. R. , Akerley B. J. , Sassetti C. M. . ( 2011;). High-resolution phenotypic profiling defines genes essential for mycobacterial growth and cholesterol catabolism. PLoS Pathog 7: e1002251 [CrossRef] [PubMed].
    [Google Scholar]
  35. Gusarov I. , Nudler E. . ( 1999;). The mechanism of intrinsic transcription termination. Mol Cell 3: 495–504 [CrossRef] [PubMed].
    [Google Scholar]
  36. Gutiérrez P. , Kozlov G. , Gabrielli L. , Elias D. , Osborne M. J. , Gallouzi I. E. , Gehring K. . ( 2007;). Solution structure of YaeO, a Rho-specific inhibitor of transcription termination. J Biol Chem 282: 23348–23353 [CrossRef] [PubMed].
    [Google Scholar]
  37. Hämmerle H. , Amman F. , Večerek B. , Stülke J. , Hofacker I. , Bläsi U. . ( 2014;). Impact of Hfq on the Bacillus subtilis transcriptome. PLoS One 9: e98661 [CrossRef] [PubMed].
    [Google Scholar]
  38. Harinarayanan R. , Gowrishankar J. . ( 2003;). Host factor titration by chromosomal R-loops as a mechanism for runaway plasmid replication in transcription termination-defective mutants of Escherichia coli . J Mol Biol 332: 31–46 [CrossRef] [PubMed].
    [Google Scholar]
  39. Hollands K. , Proshkin S. , Sklyarova S. , Epshtein V. , Mironov A. , Nudler E. , Groisman E. A. . ( 2012;). Riboswitch control of Rho-dependent transcription termination. Proc Natl Acad Sci U S A 109: 5376–5381 [CrossRef] [PubMed].
    [Google Scholar]
  40. Hollands K. , Sevostiyanova A. , Groisman E. A. . ( 2014;). Unusually long-lived pause required for regulation of a Rho-dependent transcription terminator. Proc Natl Acad Sci U S A 111: E1999–E2007 [CrossRef] [PubMed].
    [Google Scholar]
  41. Ingham C. J. . ( 1999;). Characterisation of the enzymatic and RNA-binding properties of the Rhodobacter sphaeroides 2.4.1.Rho homologue. Biochim Biophys Acta 1446: 115–125 [CrossRef].
    [Google Scholar]
  42. Ingham C. J. , Hunter I. S. , Smith M. C. . ( 1996;). Isolation and sequencing of the rho gene from Streptomyces lividans ZX7 and characterization of the RNA-dependent NTPase activity of the overexpressed protein. J Biol Chem 271: 21803–21807 [CrossRef] [PubMed].
    [Google Scholar]
  43. Ingham C. J. , Dennis J. , Furneaux P. A. . ( 1999;). Autogenous regulation of transcription termination factor Rho and the requirement for Nus factors in Bacillus subtilis . Mol Microbiol 31: 651–663 [CrossRef] [PubMed].
    [Google Scholar]
  44. Irnov I. , Sharma C. M. , Vogel J. , Winkler W. C. . ( 2010;). Identification of regulatory RNAs in Bacillus subtilis . Nucleic Acids Res 38: 6637–6651 [CrossRef] [PubMed].
    [Google Scholar]
  45. Italiani V. C. , Marques M. V. . ( 2005;). The transcription termination factor Rho is essential and autoregulated in Caulobacter crescentus . J Bacteriol 187: 4290–4294 [CrossRef] [PubMed].
    [Google Scholar]
  46. Jäger S. , Fuhrmann O. , Heck C. , Hebermehl M. , Schiltz E. , Rauhut R. , Klug G. . ( 2001;). An mRNA degrading complex in Rhodobacter capsulatus . Nucleic Acids Res 29: 4581–4588 [CrossRef] [PubMed].
    [Google Scholar]
  47. Jäger S. , Hebermehl M. , Schiltz E. , Klug G. . ( 2004;). Composition and activity of the Rhodobacter capsulatus degradosome vary under different oxygen concentrations. J Mol Microbiol Biotechnol 7: 148–154 [CrossRef] [PubMed].
    [Google Scholar]
  48. Kalarickal N. C. , Ranjan A. , Kalyani B. S. , Wal M. , Sen R. . ( 2010;). A bacterial transcription terminator with inefficient molecular motor action but with a robust transcription termination function. J Mol Biol 395: 966–982 [CrossRef] [PubMed].
    [Google Scholar]
  49. Kalyani B. S. , Kunamneni R. , Wal M. , Ranjan A. , Sen R. . ( 2015;). A NusG paralogue from Mycobacterium tuberculosis, Rv0639, has evolved to interact with ribosomal protein S10 (Rv0700) but not to function as a transcription elongation-termination factor. Microbiology 161: 67–83 [CrossRef] [PubMed].
    [Google Scholar]
  50. Kamarthapu V. , Nudler E. . ( 2015;). Rethinking transcription coupled DNA repair. Curr Opin Microbiol 24: 15–20 [CrossRef] [PubMed].
    [Google Scholar]
  51. Kapranov P. , Cheng J. , Dike S. , Nix D. A. , Duttagupta R. , Willingham A. T. , Stadler P. F. , Hertel J. , Hackermüller J. , other authors . ( 2007;). RNA maps reveal new RNA classes and a possible function for pervasive transcription. Science 316: 1484–1488 [CrossRef] [PubMed].
    [Google Scholar]
  52. Kawamura N. , Kurokawa K. , Ito T. , Hamamoto H. , Koyama H. , Kaito C. , Sekimizu K. . ( 2005;). Participation of Rho-dependent transcription termination in oxidative stress sensitivity caused by an rpoB mutation. Genes Cells 10: 477–487 [CrossRef] [PubMed].
    [Google Scholar]
  53. Kontur W. S. , Schackwitz W. S. , Ivanova N. , Martin J. , Labutti K. , Deshpande S. , Tice H. N. , Pennacchio C. , Sodergren E. , other authors . ( 2012;). Revised sequence and annotation of the Rhodobacter sphaeroides 2.4.1 genome. J Bacteriol 194: 7016–7017 [CrossRef] [PubMed].
    [Google Scholar]
  54. Koslover D. J. , Fazal F. M. , Mooney R. A. , Landick R. , Block S. M. . ( 2012;). Binding and translocation of termination factor rho studied at the single-molecule level. J Mol Biol 423: 664–676 [CrossRef] [PubMed].
    [Google Scholar]
  55. Kotlajich M. V. , Hron D. R. , Boudreau B. A. , Sun Z. , Lyubchenko Y. L. , Landick R. . ( 2015;). Bridged filaments of histone-like nucleoid structuring protein pause RNA polymerase and aid termination in bacteria. eLife 4: e04970 [CrossRef] [PubMed].
    [Google Scholar]
  56. Kriner M. A. , Groisman E. A. . ( 2015;). The bacterial transcription termination factor Rho coordinates Mg2+ homeostasis with translational signals. J Mol Biol 427: 3834–3849 [CrossRef] [PubMed].
    [Google Scholar]
  57. Laalami S. , Zig L. , Putzer H. . ( 2014;). Initiation of mRNA decay in bacteria. Cell Mol Life Sci 71: 1799–1828 [CrossRef] [PubMed].
    [Google Scholar]
  58. Landick R. , Wade J. T. , Grainger D. C. . ( 2015;). H-NS and RNA polymerase: a love-hate relationship?. Curt Opin Microbiol 24: 53–59.[CrossRef]
    [Google Scholar]
  59. Lasa I. , Toledo-Arana A. , Dobin A. , Villanueva M. , de los Mozos I. R. , Vergara-Irigaray M. , Segura V. , Fagegaltier D. , Penadés J. R. , other authors . ( 2011;). Genome-wide antisense transcription drives mRNA processing in bacteria. Proc Natl Acad Sci U S A 108: 20172–20177 [CrossRef] [PubMed].
    [Google Scholar]
  60. Leela J. K. , Syeda A. H. , Anupama K. , Gowrishankar J. . ( 2013;). Rho-dependent transcription termination is essential to prevent excessive genome-wide R-loops in Escherichia coli . Proc Natl Acad Sci U S A 110: 258–263 [CrossRef] [PubMed].
    [Google Scholar]
  61. Lewis P. J. , Doherty G. P. , Clarke J. . ( 2008;). Transcription factor dynamics. Microbiology 154: 1837–1844 [CrossRef] [PubMed].
    [Google Scholar]
  62. Li X. , Manley J. L. . ( 2006;). Cotranscriptional processes and their influence on genome stability. Genes Dev 20: 1838–1847 [CrossRef] [PubMed].
    [Google Scholar]
  63. Li G. W. , Burkhardt D. , Gross C. , Weissman J. S. . ( 2014;). Quantifying absolute protein synthesis rates reveals principles underlying allocation of cellular resources. Cell 157: 624–635 [CrossRef] [PubMed].
    [Google Scholar]
  64. Maass S. , Sievers S. , Zühlke D. , Kuzinski J. , Sappa P. K. , Muntel J. , Hessling B. , Bernhardt J. , Sietmann R. , other authors . ( 2011;). Efficient, global-scale quantification of absolute protein amounts by integration of targeted mass spectrometry and two-dimensional gel-based proteomics. Anal Chem 83: 2677–2684 [CrossRef] [PubMed].
    [Google Scholar]
  65. Mandal M. , Boese B. , Barrick J. E. , Winkler W. C. , Breaker R. R. . ( 2003;). Riboswitches control fundamental biochemical pathways in Bacillus subtilis and other bacteria. Cell 113: 577–586 [CrossRef] [PubMed].
    [Google Scholar]
  66. Mason S. W. , Li J. , Greenblatt J. . ( 1992;). Host factor requirements for processive antitermination of transcription and suppression of pausing by the N protein of bacteriophage lambda. J Biol Chem 267: 19418–19426 [PubMed].
    [Google Scholar]
  67. Mellin J. R. , Cossart P. . ( 2015;). Unexpected versatility in bacterial riboswitches. Trends Genet 31: 150–156 [CrossRef] [PubMed].
    [Google Scholar]
  68. Menouni R. , Champ S. , Espinosa L. , Boudvillain M. , Ansaldi M. . ( 2013;). Transcription termination controls prophage maintenance in Escherichia coli genomes. Proc Natl Acad Sci U S A 110: 14414–14419 [CrossRef] [PubMed].
    [Google Scholar]
  69. Merrikh H. , Zhang Y. , Grossman A. D. , Wang J. D. . ( 2012;). Replication-transcription conflicts in bacteria. Nat Rev Microbiol 10: 449–458 [PubMed].
    [Google Scholar]
  70. Miloso M. , Limauro D. , Alifano P. , Rivellini F. , Lavitola A. , Gulletta E. , Bruni C. B. . ( 1993;). Characterization of the rho genes of Neisseria gonorrhoeae and Salmonella typhimurium . J Bacteriol 175: 8030–8037 [PubMed].
    [Google Scholar]
  71. Mitra A. , Nagaraja V. . ( 2012;). Under-representation of intrinsic terminators across bacterial genomic islands: Rho as a principal regulator of xenogenic DNA expression. Gene 508: 221–228 [CrossRef] [PubMed].
    [Google Scholar]
  72. Mitra A. , Angamuthu K. , Jayashree H. V. , Nagaraja V. . ( 2009;). Occurrence, divergence and evolution of intrinsic terminators across eubacteria. Genomics 94: 110–116 [CrossRef] [PubMed].
    [Google Scholar]
  73. Mitra A. , Kesarwani A. K. , Pal D. , Nagaraja V. . ( 2011;). WebGeSTer DB – a transcription terminator database. Nucleic Acids Res 39: (Database), D129–D135 [CrossRef] [PubMed].
    [Google Scholar]
  74. Mitra A. , Misquitta R. , Nagaraja V. . ( 2014;). Mycobacterium tuberculosis Rho is an NTPase with distinct kinetic properties and a novel RNA-binding subdomain. PLoS One 9: e107474 [CrossRef] [PubMed].
    [Google Scholar]
  75. Møller T. , Franch T. , Udesen C. , Gerdes K. , Valentin-Hansen P. . ( 2002;). Spot 42 RNA mediates discoordinate expression of the E. coli galactose operon. Genes Dev 16: 1696–1706 [CrossRef] [PubMed].
    [Google Scholar]
  76. Morita Y. , Narita S. , Tomida J. , Tokuda H. , Kawamura Y. . ( 2010;). Application of an inducible system to engineer unmarked conditional mutants of essential genes of Pseudomonas aeruginosa . J Microbiol Methods 82: 205–213 [CrossRef] [PubMed].
    [Google Scholar]
  77. Muntel J. , Fromion V. , Goelzer A. , Maaβ S. , Mäder U. , Büttner K. , Hecker M. , Becher D. . ( 2014;). Comprehensive absolute quantification of the cytosolic proteome of Bacillus subtilis by data independent, parallel fragmentation in liquid chromatography/mass spectrometry (LC/MS(E)). Mol Cell Proteomics 13: 1008–1019 [CrossRef] [PubMed].
    [Google Scholar]
  78. Muteeb G. , Dey D. , Mishra S. , Sen R. . ( 2012;). A multipronged strategy of an anti-terminator protein to overcome Rho-dependent transcription termination. Nucleic Acids Res 40: 11213–11228 [CrossRef] [PubMed].
    [Google Scholar]
  79. Nair D. , Memmi G. , Hernandez D. , Bard J. , Beaume M. , Gill S. , Francois P. , Cheung A. L. . ( 2011;). Whole-genome sequencing of Staphylococcus aureus strain RN4220, a key laboratory strain used in virulence research, identifies mutations that affect not only virulence factors but also the fitness of the strain. J Bacteriol 193: 2332–2335 [CrossRef] [PubMed].
    [Google Scholar]
  80. Nicolas P. , Mäder U. , Dervyn E. , Rochat T. , Leduc A. , Pigeonneau N. , Bidnenko E. , Marchadier E. , Hoebeke M. , other authors . ( 2012;). Condition-dependent transcriptome reveals high-level regulatory architecture in Bacillus subtilis . Science 335: 1103–1106 [CrossRef] [PubMed].
    [Google Scholar]
  81. Nowatzke W. L. , Richardson J. P. . ( 1996;). Characterization of an unusual Rho factor from the high G+C Gram-positive bacterium Micrococcus luteus . J Biol Chem 271: 742–747 [CrossRef] [PubMed].
    [Google Scholar]
  82. Nowatzke W. , Richardson L. , Richardson J. P. . ( 1996;). Purification of transcription termination factor Rho from Escherichia coli and Micrococcus luteus . Methods Enzymol 274: 353–363 [CrossRef] [PubMed].
    [Google Scholar]
  83. Nowatzke W. L. , Burns C. M. , Richardson J. P. . ( 1997a;). Function of the novel subdomain in the RNA binding domain of transcription termination factor Rho from Micrococcus luteus . J Biol Chem 272: 2207–2211 [CrossRef] [PubMed].
    [Google Scholar]
  84. Nowatzke W. L. , Keller E. , Koch G. , Richardson J. P. . ( 1997b;). Transcription termination factor Rho is essential for Micrococcus luteus . J Bacteriol 179: 5238–5240 [PubMed].
    [Google Scholar]
  85. Nudler E. . ( 2012;). RNA polymerase backtracking in gene regulation and genome instability. Cell 149: 1438–1445 [CrossRef] [PubMed].
    [Google Scholar]
  86. Nudler E. , Mustaev A. , Lukhtanov E. , Goldfarb A. . ( 1997;). The RNA-DNA hybrid maintains the register of transcription by preventing backtracking of RNA polymerase. Cell 89: 33–41 [CrossRef] [PubMed].
    [Google Scholar]
  87. Oliva G. , Sahr T. , Buchrieser C. . ( 2015;). Small RNAs, 5′ UTR elements and RNA-binding proteins in intracellular bacteria: impact on metabolism and virulence. FEMS Microbiol Rev 39: 331–349 [CrossRef] [PubMed].
    [Google Scholar]
  88. Opperman T. , Richardson J. P. . ( 1994;). Phylogenetic analysis of sequences from diverse bacteria with homology to the Escherichia coli rho gene. J Bacteriol 176: 5033–5043 [PubMed].
    [Google Scholar]
  89. Pani B. , Banerjee S. , Chalissery J. , Muralimohan A. , Loganathan R. M. , Suganthan R. B. , Sen R. . ( 2006;). Mechanism of inhibition of Rho-dependent transcription termination by bacteriophage P4 protein Psu. J Biol Chem 281: 26491–26500 [CrossRef] [PubMed].
    [Google Scholar]
  90. Park J. S. , Roberts J. W. . ( 2006;). Role of DNA bubble rewinding in enzymatic transcription termination. Proc Natl Acad Sci U S A 103: 4870–4875 [CrossRef] [PubMed].
    [Google Scholar]
  91. Patrick S. , Blakely G. W. , Houston S. , Moore J. , Abratt V. R. , Bertalan M. , Cerdeño-Tárraga A. M. , Quail M. A. , Corton N. , other authors . ( 2010;). Twenty-eight divergent polysaccharide loci specifying within- and amongst-strain capsule diversity in three strains of Bacteroides fragilis . Microbiology 156: 3255–3269 [CrossRef] [PubMed].
    [Google Scholar]
  92. Peters J. M. , Mooney R. A. , Kuan P. F. , Rowland J. L. , Keles S. , Landick R. . ( 2009;). Rho directs widespread termination of intragenic and stable RNA transcription. Proc Natl Acad Sci U S A 106: 15406–15411 [CrossRef] [PubMed].
    [Google Scholar]
  93. Peters J. M. , Vangeloff A. D. , Landick R. . ( 2011;). Bacterial transcription terminators: the RNA 3′-end chronicles. J Mol Biol 412: 793–813 [CrossRef] [PubMed].
    [Google Scholar]
  94. Peters J. M. , Mooney R. A. , Grass J. A. , Jessen E. D. , Tran F. , Landick R. . ( 2012;). Rho and NusG suppress pervasive antisense transcription in Escherichia coli . Genes Dev 26: 2621–2633 [CrossRef] [PubMed].
    [Google Scholar]
  95. Pradeepkiran J. A. , Kumar K. K. , Kumar Y. N. , Bhaskar M. . ( 2015;). Modeling, molecular dynamics, and docking assessment of transcription factor rho: a potential drug target in Brucella melitensis 16M. Drug Des Devel Ther 9: 1897–1912 [CrossRef] [PubMed].
    [Google Scholar]
  96. Proshkin S. , Rahmouni A. R. , Mironov A. , Nudler E. . ( 2010;). Cooperation between translating ribosomes and RNA polymerase in transcription elongation. Science 328: 504–508 [CrossRef] [PubMed].
    [Google Scholar]
  97. Proshkin S. , Mironov A. , Nudler E. . ( 2014;). Riboswitches in regulation of Rho-dependent transcription termination. Biochim Biophys Acta 1839: 974–977 [CrossRef] [PubMed].
    [Google Scholar]
  98. Quirk P. G. , Dunkley E. A. Jr. , Lee P. Jr. , Krulwich T. A. . ( 1993;). Identification of a putative Bacillus subtilis rho gene. J Bacteriol 175: 647–654 [PubMed].
    [Google Scholar]
  99. Rabhi M. , Espéli O. , Schwartz A. , Cayrol B. , Rahmouni A. R. , Arluison V. , Boudvillain M. . ( 2011;). The Sm-like RNA chaperone Hfq mediates transcription antitermination at Rho-dependent terminators. EMBO J 30: 2805–2816 [CrossRef] [PubMed].
    [Google Scholar]
  100. Raghavan R. , Sloan D. B. , Ochman H. . ( 2012;). Antisense transcription is pervasive but rarely conserved in enteric bacteria. MBio 3: e00156–e00e12 [CrossRef] [PubMed].
    [Google Scholar]
  101. Rajkumari K. , Gowrishankar J. . ( 2001;). In vivo expression from the RpoS-dependent P1 promoter of the osmotically regulated proU operon in Escherichia coli and Salmonella enterica serovar Typhimurium: activation by rho and hns mutations and by cold stress. J Bacteriol 183: 6543–6550 [CrossRef] [PubMed].
    [Google Scholar]
  102. Richardson J. P. . ( 1982;). Activation of rho protein ATPase requires simultaneous interaction at two kinds of nucleic acid-binding sites. J Biol Chem 257: 5760–5766 [PubMed].
    [Google Scholar]
  103. Richardson J. P. . ( 1991;). Preventing the synthesis of unused transcripts by Rho factor. Cell 64: 1047–1049 [CrossRef] [PubMed].
    [Google Scholar]
  104. Richardson J. P. . ( 2002;). Rho-dependent termination and ATPases in transcript termination. Biochim Biophys Acta 1577: 251–260 [CrossRef] [PubMed].
    [Google Scholar]
  105. Roberts J. W. . ( 1969;). Termination factor for RNA synthesis. Nature 224: 1168–1174 [CrossRef] [PubMed].
    [Google Scholar]
  106. Rochat T. , Delumeau O. , Figueroa-Bossi N. , Noirot P. , Bossi L. , Dervyn E. , Bouloc P. . ( 2015;). Tracking the elusive function of Bacillus subtilis Hfq. PLoS One 10: e0124977 [CrossRef] [PubMed].
    [Google Scholar]
  107. Santangelo T. J. , Artsimovitch I. . ( 2011;). Termination and antitermination: RNA polymerase runs a stop sign. Nat Rev Microbiol 9: 319–329 [CrossRef] [PubMed].
    [Google Scholar]
  108. Sassetti C. M. , Boyd D. H. , Rubin E. J. . ( 2003;). Genes required for mycobacterial growth defined by high density mutagenesis. Mol Microbiol 48: 77–84 [CrossRef] [PubMed].
    [Google Scholar]
  109. Saxena S. , Gowrishankar J. . ( 2011;). Compromised factor-dependent transcription termination in a nusA mutant of Escherichia coli: spectrum of termination efficiencies generated by perturbations of Rho, NusG, NusA, and H-NS family proteins. J Bacteriol 193: 3842–3850 [CrossRef] [PubMed].
    [Google Scholar]
  110. Schultze T. , Izar B. , Qing X. , Mannala G. K. , Hain T. . ( 2014;). Current status of antisense RNA-mediated gene regulation in Listeria monocytogenes . Front Cell Infect Microbiol 4: 135 [CrossRef] [PubMed].
    [Google Scholar]
  111. Schulz D. , Schwalb B. , Kiesel A. , Baejen C. , Torkler P. , Gagneur J. , Soeding J. , Cramer P. . ( 2013;). Transcriptome surveillance by selective termination of noncoding RNA synthesis. Cell 155: 1075–1087 [CrossRef] [PubMed].
    [Google Scholar]
  112. Seshasayee A. S. N. . ( 2014;). Gene expression homeostasis and chromosome architecture. BioArchitecture 4: 221–225 [CrossRef] [PubMed].
    [Google Scholar]
  113. Sevostyanova A. , Artsimovitch I. . ( 2010;). Functional analysis of Thermus thermophilus transcription factor NusG. Nucleic Acids Res 38: 7432–7445 [CrossRef] [PubMed].
    [Google Scholar]
  114. Sharma C. M. , Hoffmann S. , Darfeuille F. , Reignier J. , Findeiß S. , Sittka A. , Chabas S. , Reiche K. , Hackermüller J. , other authors . ( 2010;). The primary transcriptome of the major human pathogen Helicobacter pylori . Nature 464: 250–255 [CrossRef] [PubMed].
    [Google Scholar]
  115. Shashni R. , Qayyum M. Z. , Vishalini V. , Dey D. , Sen R. . ( 2014;). Redundancy of primary RNA-binding functions of the bacterial transcription terminator Rho. Nucleic Acids Res 42: 9677–9690 [CrossRef] [PubMed].
    [Google Scholar]
  116. Singh S. S. , Singh N. , Bonocora R. P. , Fitzgerald D. M. , Wade J. T. , Grainger D. C. . ( 2014;). Widespread suppression of intragenic transcription initiation by H-NS. Genes Dev 28: 214–219 [CrossRef] [PubMed].
    [Google Scholar]
  117. Skordalakes E. , Berger J. M. . ( 2003;). Structure of the Rho transcription terminator: mechanism of mRNA recognition and helicase loading. Cell 114: 135–146 [CrossRef] [PubMed].
    [Google Scholar]
  118. Skordalakes E. , Brogan A. P. , Park B. S. , Kohn H. , Berger J. M. . ( 2005;). Structural mechanism of inhibition of the Rho transcription termination factor by the antibiotic bicyclomycin. Structure 13: 99–109 [CrossRef] [PubMed].
    [Google Scholar]
  119. Sozhamannan S. , Stitt B. L. . ( 1997;). Effects on mRNA degradation by Escherichia coli transcription termination factor Rho and pBR322 copy number control protein Rop. J Mol Biol 268: 689–703 [CrossRef] [PubMed].
    [Google Scholar]
  120. Srivatsan A. , Tehranchi A. , MacAlpine D. M. , Wang J. D. . ( 2010;). Co-orientation of replication and transcription preserves genome integrity. PLoS Genet 6: e1000810 [CrossRef] [PubMed].
    [Google Scholar]
  121. Takemoto N. , Tanaka Y. , Inui M. . ( 2015;). Rho and RNase play a central role in FMN riboswitch regulation in Corynebacterium glutamicum . Nucleic Acids Res 43: 520–529 [CrossRef] [PubMed].
    [Google Scholar]
  122. Tanaka Y. , Teramoto H. , Inui M. . ( 2015;). Regulation of the expression of de novo pyrimidine biosynthesis genes in Corynebacterium glutamicum . J Bacteriol 197: 3307–3316 [CrossRef] [PubMed].
    [Google Scholar]
  123. Thomason M. K. , Storz G. . ( 2010;). Bacterial antisense RNAs: how many are there, and what are they doing?. Annu Rev Genet 44: 167–188 [CrossRef] [PubMed].
    [Google Scholar]
  124. Tomar S. K. , Artsimovitch I. . ( 2013;). NusG-Spt5 proteins - universal tools for transcription modification and communication. Chem Rev 113: 8604–8619 [CrossRef] [PubMed].
    [Google Scholar]
  125. Tran L. , van Baarsel J. A. , Washburn R. S. , Gottesman M. E. , Miller J. H. . ( 2011;). Single-gene deletion mutants of Escherichia coli with altered sensitivity to bicyclomycin, an inhibitor of transcription termination factor Rho. J Bacteriol 193: 2229–2235 [CrossRef] [PubMed].
    [Google Scholar]
  126. Trautinger B. W. , Lloyd R. G. . ( 2002;). Modulation of DNA repair by mutations flanking the DNA channel through RNA polymerase. EMBO J 21: 6944–6953 [CrossRef] [PubMed].
    [Google Scholar]
  127. Tuckerman J. R. , Gonzalez G. , Gilles-Gonzalez M. A. . ( 2011;). Cyclic di-GMP activation of polynucleotide phosphorylase signal-dependent RNA processing. J Mol Biol 407: 633–639 [CrossRef] [PubMed].
    [Google Scholar]
  128. Turner R. J. , Lu Y. , Switzer R. L. . ( 1994;). Regulation of the Bacillus subtilis pyrimidine biosynthetic (pyr) gene cluster by an autogenous transcriptional attenuation mechanism. J Bacteriol 176: 3708–3722 [PubMed].
    [Google Scholar]
  129. Veeranagouda Y. , Husain F. , Tenorio E. L. , Wexler H. M. . ( 2014;). Identification of genes required for the survival of Bacteroides fragilis using massive parallel sequencing of a saturated transposon mutant library. BMC Genomics 15: 429 [CrossRef] [PubMed].
    [Google Scholar]
  130. Voigt K. , Sharma C. M. , Mitschke J. , Lambrecht S. J. , Voß B. , Hess W. R. , Steglich C. . ( 2014;). Comparative transcriptomics of two environmentally relevant cyanobacteria reveals unexpected transcriptome diversity. ISME J 8: 2056–2068 [CrossRef] [PubMed].
    [Google Scholar]
  131. Wade J. T. , Grainger D. C. . ( 2014;). Pervasive transcription: illuminating the dark matter of bacterial transcriptomes. Nat Rev Microbiol 12: 647–653 [CrossRef] [PubMed].
    [Google Scholar]
  132. Wang M. , Herrmann C. J. , Simonovic M. , Szklarczyk D. , von Mering C. . ( 2015a;). Version 4.0 of PaxDb: protein abundance data, integrated across model organisms, tissues, and cell-lines. Proteomics 15: 3163–3168 [CrossRef] [PubMed].
    [Google Scholar]
  133. Wang X. , Ji S. C. , Jeon H. J. , Lee Y. , Lim H. M. . ( 2015b;). Two-level inhibition of galK expression by Spot 42: degradation of mRNA mK2 and enhanced transcription termination before the galK gene. Proc Natl Acad Sci U S A 112: 7581–7586 [CrossRef] [PubMed].
    [Google Scholar]
  134. Washburn R. S. , Gottesman M. E. . ( 2011;). Transcription termination maintains chromosome integrity. Proc Natl Acad Sci U S A 108: 792–797 [CrossRef] [PubMed].
    [Google Scholar]
  135. Washburn R. S. , Gottesman M. E. . ( 2015;). Regulation of transcription elongation and termination. Biomolecules 5: 1063–1078 [CrossRef] [PubMed].
    [Google Scholar]
  136. Washburn R. S. , Marra A. , Bryant A. P. , Rosenberg M. , Gentry D. R. . ( 2001;). rho is not essential for viability or virulence in Staphylococcus aureus . Antimicrob Agents Chemother 45: 1099–1103 [CrossRef] [PubMed].
    [Google Scholar]
  137. Washio T. , Sasayama J. , Tomita M. . ( 1998;). Analysis of complete genomes suggests that many prokaryotes do not rely on hairpin formation in transcription termination. Nucleic Acids Res 26: 5456–5463 [CrossRef] [PubMed].
    [Google Scholar]
  138. Wimberly H. , Shee C. , Thornton P. C. , Sivaramakrishnan P. , Rosenberg S. M. , Hastings P. J. . ( 2013;). R-loops and nicks initiate DNA breakage and genome instability in non-growing Escherichia coli . Nat Commun 4: 2115 [CrossRef] [PubMed].
    [Google Scholar]
  139. Yakhnin H. , Babiarz J. E. , Yakhnin A. V. , Babitzke P. . ( 2001;). Expression of the Bacillus subtilis trpEDCFBA operon is influenced by translational coupling and Rho termination factor. J Bacteriol 183: 5918–5926 [CrossRef] [PubMed].
    [Google Scholar]
  140. Yakhnin A. V. , Yakhnin H. , Babitzke P. . ( 2008;). Function of the Bacillus subtilis transcription elongation factor NusG in hairpin-dependent RNA polymerase pausing in the trp leader. Proc Natl Acad Sci U S A 105: 16131–16136 [CrossRef] [PubMed].
    [Google Scholar]
  141. Yakhnin H. , Yakhnin A. V. , Babitzke P. . ( 2015;). Ribosomal protein L10(L12)4 autoregulates expression of the Bacillus subtilis rplJL operon by a transcription attenuation mechanism. Nucleic Acids Res 43: 7032–7043 [CrossRef] [PubMed].
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.000244
Loading
/content/journal/micro/10.1099/mic.0.000244
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error