1932

Abstract

In bacteria, transcription and translation take place in the same cellular compartment. Therefore, a messenger RNA can be translated as it is being transcribed, a process known as transcription-translation coupling. This process was already recognized at the dawn of molecular biology, yet the interplay between the two key players, the RNA polymerase and ribosome, remains elusive. Genetic data indicate that an RNA sequence can be translated shortly after it has been transcribed. The closer both processes are in time, the less accessible the RNA sequence is between the RNA polymerase and ribosome. This temporal coupling has important consequences for gene regulation. Biochemical and structural studies have detailed several complexes between the RNA polymerase and ribosome. The in vivo relevance of this physical coupling has not been formally demonstrated. We discuss how both temporal and physical coupling may mesh to produce the phenomenon we know as transcription-translation coupling.

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2022-11-30
2024-04-15
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Literature Cited

  1. 1.
    Abe H, Abo T, Aiba H. 1999. Regulation of intrinsic terminator by translation in Escherichia coli: transcription termination at a distance downstream. Genes Cells 4:287–97
    [Google Scholar]
  2. 2.
    Adams P, Baniulyte G, Esnault C, Chegireddy K, Singh N et al. 2021. Regulatory roles of 5′ UTR and ORF-internal RNAs detected by 3′ end mapping. eLife 10:e62438
    [Google Scholar]
  3. 3.
    Arenz S, Ramu H, Gupta P, Berninghausen O, Beckmann R et al. 2014. Molecular basis for erythromycin-dependent ribosome stalling during translation of the ErmBL leader peptide. Nat. Commun. 5:3501
    [Google Scholar]
  4. 4.
    Bailey EJ, Gottesman ME, Gonzalez RL Jr. 2022. NusG-mediated coupling of transcription and translation enhances gene expression by suppressing RNA polymerase backtracking. J. Mol. Biol. 434:2167330
    [Google Scholar]
  5. 5.
    Bailey MJ, Hughes C, Koronakis V. 1996. Increased distal gene transcription by the elongation factor RfaH, a specialized homologue of NusG. Mol. Microbiol. 22:4729–37
    [Google Scholar]
  6. 6.
    Bailey MJA, Hughes C, Koronakis V. 1997. RfaH and the ops element, components of a novel system controlling bacterial transcription elongation. Mol. Microbiol. 26:5845–51
    [Google Scholar]
  7. 7.
    Bange G, Brodersen DE, Liuzzi A, Steinchen W. 2021. Two P or not two P: understanding regulation by the bacterial second messengers (p)ppGpp. Annu. Rev. Microbiol. 75:383–406
    [Google Scholar]
  8. 8.
    Baniulyte G, Singh N, Benoit C, Johnson R, Ferguson R et al. 2017. Identification of regulatory targets for the bacterial Nus factor complex. Nat. Commun. 8:12027
    [Google Scholar]
  9. 9.
    Bastet L, Turcotte P, Wade JT, Lafontaine DA. 2018. Maestro of regulation: Riboswitches orchestrate gene expression at the levels of translation, transcription and mRNA decay. RNA Biol 15:6679–82
    [Google Scholar]
  10. 10.
    Bidnenko V, Nicolas P, Grylak-Mielnicka A, Delumeau O, Auger S et al. 2017. Termination factor Rho: from the control of pervasive transcription to cell fate determination in Bacillus subtilis. PLOS Genet 13:7e1006909
    [Google Scholar]
  11. 11.
    Bladen HA, Byrne R, Levin JG, Nirenberg MW. 1965. An electron microscopic study of a DNA-ribosome complex formed in vitro. J. Mol. Biol. 11:78–83
    [Google Scholar]
  12. 12.
    Bonekamp F, Clemmesen K, Karlström O, Jensen KF. 1984. Mechanism of UTP-modulated attenuation at the pyrE gene of Escherichia coli: an example of operon polarity control through the coupling of translation to transcription. EMBO J 3:122857–61
    [Google Scholar]
  13. 13.
    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 26:161864–73
    [Google Scholar]
  14. 14.
    Botella L, Vaubourgeix J, Livny J, Schnappinger D. 2017. Depleting Mycobacterium tuberculosis of the transcription termination factor Rho causes pervasive transcription and rapid death. Nat. Commun. 8:114731
    [Google Scholar]
  15. 15.
    Burmann BM, Knauer SH, Sevostyanova A, Schweimer K, Mooney RA et al. 2012. An α helix to β barrel domain switch transforms the transcription factor RfaH into a translation factor. Cell 150:2291–303
    [Google Scholar]
  16. 16.
    Burmann BM, Schweimer K, Luo X, Wahl MC, Stitt BL et al. 2010. A NusE:NusG complex links transcription and translation. Science 328:5977501–4
    [Google Scholar]
  17. 17.
    Byrne R, Levin JG, Bladen HA, Nirenberg MW. 1964. The in vitro formation of a DNA-ribosome complex. PNAS 52:1140–48
    [Google Scholar]
  18. 18.
    Castro-Roa D, Zenkin N. 2015. Methodology for the analysis of transcription and translation in transcription-coupled-to-translation systems in vitro. Methods 86:51–59
    [Google Scholar]
  19. 19.
    Castro-Roa D, Zenkin N. 2015. Methods for the assembly and analysis of in vitro transcription-coupled-to-translation systems. Methods Mol. Biol. 1276:81–99
    [Google Scholar]
  20. 20.
    Chakrabarti SL, Gorini L. 1977. Interaction between mutations of ribosomes and RNA polymerase: a pair of strA and rif mutants individually temperature-insensitive but temperature-sensitive in combination. PNAS 74:31157–61
    [Google Scholar]
  21. 21.
    Chatterjee S, Chauvier A, Dandpat SS, Artsimovitch I, Walter NG. 2021. A translational riboswitch coordinates nascent transcription–translation coupling. PNAS 118:16e2023426118
    [Google Scholar]
  22. 22.
    Chen M, Fredrick K. 2018. Measures of single- versus multiple-round translation argue against a mechanism to ensure coupling of transcription and translation. PNAS 115:4210774–79
    [Google Scholar]
  23. 23.
    Clemmesen K, Bonekamp F, Karlström O, Jensen KF. 1985. Role of translation in the UTP-modulated attenuation at the pyrBI operon of Escherichia coli. Mol. Gen. Genet. 201:2247–51
    [Google Scholar]
  24. 24.
    Dar D, Shamir M, Mellin JR, Koutero M, Stern-Ginossar N et al. 2016. Term-seq reveals abundant ribo-regulation of antibiotics resistance in bacteria. Science 352:6282aad9822
    [Google Scholar]
  25. 25.
    Darst SA. 2001. Bacterial RNA polymerase. Curr. Opin. Struct. Biol. 11:2155–62
    [Google Scholar]
  26. 26.
    Das A, Court D, Adhya S. 1976. Isolation and characterization of conditional lethal mutants of Escherichia coli defective in transcription termination factor rho. PNAS 73:61959–63
    [Google Scholar]
  27. 27.
    de Smit MH, van Duin J. 2003. Translational standby sites: how ribosomes may deal with the rapid folding kinetics of mRNA. J. Mol. Biol. 331:4737–43
    [Google Scholar]
  28. 28.
    de Smit MH, Verlaan PWG, van Duin J, Pleij CWA. 2009. In vivo dynamics of intracistronic transcriptional polarity. J. Mol. Biol. 385:3733–47
    [Google Scholar]
  29. 29.
    Demo G, Rasouly A, Vasilyev N, Svetlov V, Loveland AB et al. 2017. Structure of RNA polymerase bound to ribosomal 30S subunit. eLife 6:e28560
    [Google Scholar]
  30. 30.
    D'Heygère F, Rabhi M, Boudvillain M. 2013. Phyletic distribution and conservation of the bacterial transcription termination factor Rho. Microbiology 159:Part 71423–36
    [Google Scholar]
  31. 31.
    Duval M, Korepanov A, Fuchsbauer O, Fechter P, Haller A et al. 2013. Escherichia coli ribosomal protein S1 unfolds structured mRNAs onto the ribosome for active translation initiation. PLOS Biol 11:12e1001731
    [Google Scholar]
  32. 32.
    Elgamal S, Artsimovitch I, Ibba M. 2016. Maintenance of transcription-translation coupling by elongation factor P. mBio 7:5e01373–16
    [Google Scholar]
  33. 33.
    Epshtein V, Dutta D, Wade J, Nudler E. 2010. An allosteric mechanism of Rho-dependent transcription termination. Nature 463:7278245–49
    [Google Scholar]
  34. 34.
    Fan H, Conn AB, Williams PB, Diggs S, Hahm J et al. 2017. Transcription–translation coupling: direct interactions of RNA polymerase with ribosomes and ribosomal subunits. Nucleic Acids Res 45:1911043–55
    [Google Scholar]
  35. 35.
    Franklin NC, Luria SE. 1961. Transduction by bacteriophage P1 and the properties of the lac genetic region in E. coli and S. dysenteriae. Virology 15:299–311
    [Google Scholar]
  36. 36.
    Guo X, Myasnikov AG, Chen J, Crucifix C, Papai G et al. 2018. Structural basis for NusA stabilized transcriptional pausing. Mol. Cell 69:5816–27.e4
    [Google Scholar]
  37. 37.
    Guo Z, Noller HF. 2012. Rotation of the head of the 30S ribosomal subunit during mRNA translocation. PNAS 109:5020391–94
    [Google Scholar]
  38. 38.
    Gusarov I, Nudler E. 1999. The mechanism of intrinsic transcription termination. Mol. Cell 3:4495–504
    [Google Scholar]
  39. 39.
    Hao Z, Epshtein V, Kim KH, Proshkin S, Svetlov V et al. 2021. Pre-termination transcription complex: structure and function. Mol. Cell 81:2281–92.e8
    [Google Scholar]
  40. 40.
    Herrero Del Valle A, Seip B, Cervera-Marzal I, Sacheau G, Seefeldt AC, Innis CA. 2020. Ornithine capture by a translating ribosome controls bacterial polyamine synthesis. Nat. Microbiol. 5:4554–61
    [Google Scholar]
  41. 41.
    Imamoto F. 1970. Evidence for premature termination of transcription of the tryptophan operon in polarity mutants of Escherichia coli. Nature 228:5268232–35
    [Google Scholar]
  42. 42.
    Imamoto F, Yanofsky C. 1967. Transcription of the tryptophan operon in polarity mutants of Escherichia coli: I. Characterization of the tryptophan messenger RNA of polar mutants. J. Mol. Biol. 28:11–23
    [Google Scholar]
  43. 43.
    Imamoto F, Yanofsky C. 1967. Transcription of the tryptophan operon in polarity mutants of Escherichia coli: II. Evidence for normal production of tryp-mRNA molecules and for premature termination of transcription. J. Mol. Biol. 28:125–35
    [Google Scholar]
  44. 44.
    Ingham CJ, Dennis J, Furneaux PA. 1999. Autogenous regulation of transcription termination factor Rho and the requirement for Nus factors in Bacillus subtilis. Mol. Microbiol. 31:2651–63
    [Google Scholar]
  45. 45.
    Ito K, Chiba S. 2013. Arrest peptides: cis-acting modulators of translation. Annu. Rev. Biochem. 82:171–202
    [Google Scholar]
  46. 46.
    Iyer S, Le D, Park BR, Kim M. 2018. Distinct mechanisms coordinate transcription and translation under carbon and nitrogen starvation in Escherichia coli. Nat. Microbiol. 3:6741–48
    [Google Scholar]
  47. 47.
    Johnson GE, Lalanne J-B, Peters ML, Li G-W. 2020. Functionally uncoupled transcription–translation in Bacillus subtilis. Nature 585:7823124–28
    [Google Scholar]
  48. 48.
    Johnston HM, Barnes WM, Chumley FG, Bossi L, Roth JR. 1980. Model for regulation of the histidine operon of Salmonella. PNAS 77:1508–12
    [Google Scholar]
  49. 49.
    Julián P, Milon P, Agirrezabala X, Lasso G, Gil D et al. 2011. The Cryo-EM structure of a complete 30S translation initiation complex from Escherichia coli. PLOS Biol 9:7e1001095
    [Google Scholar]
  50. 50.
    Kang JY, Mooney RA, Nedialkov Y, Saba J, Mishanina TV et al. 2018. Structural basis for transcript elongation control by NusG family universal regulators. Cell 173:71650–62.e14
    [Google Scholar]
  51. 51.
    Kohler R, Mooney RA, Mills DJ, Landick R, Cramer P. 2017. Architecture of a transcribing-translating expressome. Science 356:6334194–97
    [Google Scholar]
  52. 52.
    Komissarova N, Becker J, Solter S, Kireeva M, Kashlev M. 2002. Shortening of RNA:DNA hybrid in the elongation complex of RNA polymerase is a prerequisite for transcription termination. Mol. Cell 10:51151–62
    [Google Scholar]
  53. 53.
    Korn LJ, Yanofsky C. 1976. Polarity suppressors defective in transcription termination at the attenuator of the tryptophan operon of Escherichia coli have altered rho factor. J. Mol. Biol. 106:2231–41
    [Google Scholar]
  54. 54.
    Landick R, Carey J, Yanofsky C 1985. Translation activates the paused transcription complex and restores transcription of the trp operon leader region. PNAS 82:144663–67
    [Google Scholar]
  55. 55.
    Larson MH, Mooney RA, Peters JM, Windgassen T, Nayak D et al. 2014. A pause sequence enriched at translation start sites drives transcription dynamics in vivo. Science 344:61871042–47
    [Google Scholar]
  56. 56.
    Lee F, Yanofsky C. 1977. Transcription termination at the trp operon attenuators of Escherichia coli and Salmonella typhimurium: RNA secondary structure and regulation of termination. PNAS 74:104365–69
    [Google Scholar]
  57. 57.
    Leela JK, Syeda AH, Anupama K, Gowrishankar J. 2013. Rho-dependent transcription termination is essential to prevent excessive genome-wide R-loops in Escherichia coli. PNAS 110:1258–63
    [Google Scholar]
  58. 58.
    Li R, Zhang Q, Li J, Shi H. 2016. Effects of cooperation between translating ribosome and RNA polymerase on termination efficiency of the Rho-independent terminator. Nucleic Acids Res 44:62554–63
    [Google Scholar]
  59. 59.
    Maffioli SI, Zhang Y, Degen D, Carzaniga T, Del Gatto G et al. 2017. Antibacterial nucleoside-analog inhibitor of bacterial RNA polymerase. Cell 169:71240–48.e23
    [Google Scholar]
  60. 60.
    Miller OL, Hamkalo BA, Thomas CA. 1970. Visualization of bacterial genes in action. Science 169:3943392–95
    [Google Scholar]
  61. 61.
    Mooney RA, Davis SE, Peters JM, Rowland JL, Ansari AZ, Landick R. 2009. Regulator trafficking on bacterial transcription units in vivo. Mol. Cell 33:197–108
    [Google Scholar]
  62. 62.
    Mooney RA, Schweimer K, Rösch P, Gottesman M, Landick R. 2009. Two structurally independent domains of E. coli NusG create regulatory plasticity via distinct interactions with RNA polymerase and regulators. J. Mol. Biol. 391:2341–58
    [Google Scholar]
  63. 63.
    Morse DE, Primakoff P. 1970. Relief of polarity in E. coli by “suA.”. Nature 226:524028–31
    [Google Scholar]
  64. 64.
    Murakami KS. 2015. Structural biology of bacterial RNA polymerase. Biomolecules 5:2848–64
    [Google Scholar]
  65. 65.
    Neuman KC, Abbondanzieri EA, Landick R, Gelles J, Block SM. 2003. Ubiquitous transcriptional pausing is independent of RNA polymerase backtracking. Cell 115:4437–47
    [Google Scholar]
  66. 66.
    Nicolas P, Mäder U, Dervyn E, Rochat T, Leduc A et al. 2012. Condition-dependent transcriptome reveals high-level regulatory architecture in Bacillus subtilis. Science 335:60721103–6
    [Google Scholar]
  67. 67.
    Oh E, Becker AH, Sandikci A, Huber D, Chaba R et al. 2011. Selective ribosome profiling reveals the cotranslational chaperone action of trigger factor in vivo. Cell 147:91295–308
    [Google Scholar]
  68. 68.
    O'Reilly FJ, Xue L, Graziadei A, Sinn L, Lenz S et al. 2020. In-cell architecture of an actively transcribing-translating expressome. Science 369:6503554–57
    [Google Scholar]
  69. 69.
    Peters JM, Mooney RA, Grass JA, Jessen ED, Tran F, Landick R. 2012. Rho and NusG suppress pervasive antisense transcription in Escherichia coli. Genes Dev 26:232621–33
    [Google Scholar]
  70. 70.
    Peters JM, Vangeloff AD, Landick R. 2011. Bacterial transcription terminators: the RNA 3′-end chronicles. J. Mol. Biol. 412:5793–813
    [Google Scholar]
  71. 71.
    Proshkin S, Rahmouni AR, Mironov A, Nudler E. 2010. Cooperation between translating ribosomes and RNA polymerase in transcription elongation. Science 328:5977504–8
    [Google Scholar]
  72. 72.
    Quirk PG, Dunkley EA, Lee P, Krulwich TA. 1993. Identification of a putative Bacillus subtilis rho gene. J. Bacteriol. 175:3647–54
    [Google Scholar]
  73. 73.
    Ratje AH, Loerke J, Mikolajka A, Brünner M, Hildebrand PW et al. 2010. Head swivel on the ribosome facilitates translocation by means of intra-subunit tRNA hybrid sites. Nature 468:7324713–16
    [Google Scholar]
  74. 74.
    Ratner D. 1976. Evidence that mutations in the suA polarity suppressing gene directly affect termination factor rho. Nature 259:5539151–53
    [Google Scholar]
  75. 75.
    Richardson JP, Grimley C, Lowery C. 1975. Transcription termination factor rho activity is altered in Escherichia coli with suA gene mutations. PNAS 72:51725–28
    [Google Scholar]
  76. 76.
    Roland KL, Liu CG, Turnbough CL Jr. 1988. Role of the ribosome in suppressing transcriptional termination at the pyrBI attenuator of Escherichia coli K-12. PNAS 85:197149–53
    [Google Scholar]
  77. 77.
    Ruteshouser EC, Richardson JP. 1989. Identification and characterization of transcription termination sites in the Escherichia coli lacZ gene. J. Mol. Biol. 208:123–43
    [Google Scholar]
  78. 78.
    Said N, Hilal T, Sunday ND, Khatri A, Bürger J et al. 2020. Steps toward translocation-independent RNA polymerase inactivation by terminator ATPase ρ. Science 371:6524eabd1673
    [Google Scholar]
  79. 79.
    Schuwirth BS, Borovinskaya MA, Hau CW, Zhang W, Vila-Sanjurjo A et al. 2005. Structures of the bacterial ribosome at 3.5 Å resolution. Science 310:5749827–34
    [Google Scholar]
  80. 80.
    Stevenson-Jones F, Woodgate J, Castro-Roa D, Zenkin N. 2020. Ribosome reactivates transcription by physically pushing RNA polymerase out of transcription arrest. PNAS 117:158462–67
    [Google Scholar]
  81. 81.
    Sukhodolets MV, Garges S. 2003. Interaction of Escherichia coli RNA polymerase with the ribosomal protein S1 and the Sm-like ATPase Hfq. Biochemistry 42:268022–34
    [Google Scholar]
  82. 82.
    Sukhodolets MV, Garges S, Adhya S. 2006. Ribosomal protein S1 promotes transcriptional cycling. RNA 12:81505–13
    [Google Scholar]
  83. 83.
    Turnbough CL. 2019. Regulation of bacterial gene expression by transcription attenuation. Microbiol. Mol. Biol. Rev. 83:3e00019–19
    [Google Scholar]
  84. 84.
    Valabhoju V, Agrawal S, Sen R. 2016. Molecular basis of NusG-mediated regulation of Rho-dependent transcription termination in bacteria. J. Biol. Chem. 291:4322386–403
    [Google Scholar]
  85. 85.
    van der Stel A-X, Gordon ER, Sengupta A, Martínez AK, Klepacki D et al. 2021. Structural basis for the tryptophan sensitivity of TnaC-mediated ribosome stalling. Nat. Commun. 12:15340
    [Google Scholar]
  86. 86.
    Vogel U, Jensen KF. 1994. The RNA chain elongation rate in Escherichia coli depends on the growth rate. J. Bacteriol. 176:102807–13
    [Google Scholar]
  87. 87.
    Vvedenskaya IO, Vahedian-Movahed H, Bird JG, Knoblauch JG, Goldman SR et al. 2014. Interactions between RNA polymerase and the “core recognition element” counteract pausing. Science 344:61891285–89
    [Google Scholar]
  88. 88.
    Wang C, Molodtsov V, Firlar E, Kaelber JT, Blaha G et al. 2020. Structural basis of transcription-translation coupling. Science 369:65091359–65
    [Google Scholar]
  89. 89.
    Washburn RS, Zuber PK, Sun M, Hashem Y, Shen B et al. 2020. Escherichia coli NusG links the lead ribosome with the transcription elongation complex. iScience 23:8101352
    [Google Scholar]
  90. 90.
    Webster MW, Takacs M, Zhu C, Vidmar V, Eduljee A et al. 2020. Structural basis of transcription-translation coupling and collision in bacteria. Science 369:65091355–59
    [Google Scholar]
  91. 91.
    Webster MW, Weixlbaumer A. 2021. Macromolecular assemblies supporting transcription-translation coupling. Transcription 12:4103–25
    [Google Scholar]
  92. 92.
    Wen J-D, Lancaster L, Hodges C, Zeri A-C, Yoshimura SH et al. 2008. Following translation by single ribosomes one codon at a time. Nature 452:7187598–603
    [Google Scholar]
  93. 93.
    Wilson DN, Nierhaus KH. 2003. The ribosome through the looking glass. Angew. Chem. Int. Ed. Engl. 42:303464–86
    [Google Scholar]
  94. 94.
    Wright JJ, Hayward RS. 1987. Transcriptional termination at a fully rho-independent site in Escherichia coli is prevented by uninterrupted translation of the nascent RNA. EMBO J 6:41115–19
    [Google Scholar]
  95. 95.
    Yakhnin H, Babiarz JE, Yakhnin AV, Babitzke P. 2001. Expression of the Bacillus subtilis trpEDCFBA operon is influenced by translational coupling and Rho termination factor. J. Bacteriol. 183:205918–26
    [Google Scholar]
  96. 96.
    Yakhnin H, Yakhnin AV, Babitzke P. 2015. Ribosomal protein L10(L12)4 autoregulates expression of the Bacillus subtilis rplJL operon by a transcription attenuation mechanism. Nucleic Acids Res 43:147032–43
    [Google Scholar]
  97. 97.
    Yakhnin H, Yakhnin AV, Mouery BL, Mandell ZF, Karbasiafshar C et al. 2019. NusG-dependent RNA polymerase pausing and tylosin-dependent ribosome stalling are required for tylosin resistance by inducing 23S rRNA methylation in Bacillus subtilis. mBio 10:6e02665–19
    [Google Scholar]
  98. 98.
    Yanofsky C. 1988. Transcription attenuation. J. Biol. Chem. 263:2609–12
    [Google Scholar]
  99. 99.
    Zheng C, Friedman DI. 1994. Reduced Rho-dependent transcription termination permits NusA-independent growth of Escherichia coli. PNAS 91:167543–47
    [Google Scholar]
  100. 100.
    Zhu M, Mori M, Hwa T, Dai X 2019. Disruption of transcription–translation coordination in Escherichia coli leads to premature transcriptional termination. Nat. Microbiol. 4:122347–56
    [Google Scholar]
  101. 101.
    Zhu M, Mu H, Han F, Wang Q, Dai X 2021. Quantitative analysis of asynchronous transcription-translation and transcription processivity in Bacillus subtilis under various growth conditions. iScience 24:11103333
    [Google Scholar]
  102. 102.
    Zuber PK, Schweimer K, Rösch P, Artsimovitch I, Knauer SH. 2019. Reversible fold-switching controls the functional cycle of the antitermination factor RfaH. Nat. Commun. 10:1702
    [Google Scholar]
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