1932

Abstract

Bacterial protein synthesis rates have evolved to maintain preferred stoichiometries at striking precision, from the components of protein complexes to constituents of entire pathways. Setting relative protein production rates to be well within a factor of two requires concerted tuning of transcription, RNA turnover, and translation, allowing many potential regulatory strategies to achieve the preferred output. The last decade has seen a greatly expanded capacity for precise interrogation of each step of the central dogma genome-wide. Here, we summarize how these technologies have shaped the current understanding of diverse bacterial regulatory architectures underpinning stoichiometric protein synthesis. We focus on the emerging expanded view of bacterial operons, which encode diverse primary and secondary mRNA structures for tuning protein stoichiometry. Emphasis is placed on how quantitative tuning is achieved. We discuss the challenges and open questions in the application of quantitative, genome-wide methodologies to the problem of precise protein production.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-micro-041921-012646
2021-10-08
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/micro/75/1/annurev-micro-041921-012646.html?itemId=/content/journals/10.1146/annurev-micro-041921-012646&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Ades SE, Connolly LE, Alba BM, Gross CA. 1999. The Escherichia coli σE-dependent extracytoplasmic stress response is controlled by the regulated proteolysis of an anti-σ factor. Genes Dev 13:2449–61
    [Google Scholar]
  2. 2. 
    Adhya S. 2003. Suboperonic regulatory signals. Sci. STKE 2003:185pe22
    [Google Scholar]
  3. 3. 
    Aebersold R, Mann M. 2016. Mass-spectrometric exploration of proteome structure and function. Nature 537:7620347–55
    [Google Scholar]
  4. 4. 
    Ames BN, Garry B. 1959. Coordinate repression of the synthesis of four histidine biosynthetic enzymes by histidine. PNAS 45:101453–61
    [Google Scholar]
  5. 5. 
    Apirion D, Lassar AB. 1978. A conditional lethal mutant of Escherichia coli which affects the processing of ribosomal RNA. J. Biol. Chem. 253:51738–42
    [Google Scholar]
  6. 6. 
    Bakshi S, Choi H, Weisshaar JC. 2015. The spatial biology of transcription and translation in rapidly growing Escherichia coli.. Front. Microbiol. 6:636
    [Google Scholar]
  7. 7. 
    Bandyra KJ, Wandzik JM, Luisi BF. 2018. Substrate recognition and autoinhibition in the central ribonuclease RNase E. Mol. Cell 72:2275–85.e4
    [Google Scholar]
  8. 8. 
    Barnes SL, Belliveau NM, Ireland WT, Kinney JB, Phillips R. 2019. Mapping DNA sequence to transcription factor binding energy in vivo. PLOS Comput. Biol. 15:2e1006226
    [Google Scholar]
  9. 9. 
    Barquist L, Vogel J. 2015. Accelerating discovery and functional analysis of small RNAs with new technologies. Annu. Rev. Genet. 49:367–94
    [Google Scholar]
  10. 10. 
    Bechhofer DH, Deutscher MP. 2019. Bacterial ribonucleases and their roles in RNA metabolism. Crit. Rev. Biochem. Mol. Biol. 54:3242–300
    [Google Scholar]
  11. 11. 
    Belliveau NM, Barnes SL, Ireland WT, Jones DL, Sweredoski MJ et al. 2018. Systematic approach for dissecting the molecular mechanisms of transcriptional regulation in bacteria. PNAS 115:21E4796–805
    [Google Scholar]
  12. 12. 
    Bentele K, Saffert P, Rauscher R, Ignatova Z, Blüthgen N. 2013. Efficient translation initiation dictates codon usage at gene start. Mol. Syst. Biol. 9:675
    [Google Scholar]
  13. 13. 
    Bhattacharyya S, Jacobs WM, Adkar BV, Yan J, Zhang W, Shakhnovich EI. 2018. Accessibility of the Shine-Dalgarno sequence dictates N-terminal codon bias in E. coli. Mol. Cell 70:5894–905.e5
    [Google Scholar]
  14. 14. 
    Bintu L, Buchler NE, Garcia HG, Gerland U, Hwa T et al. 2005. Transcriptional regulation by the numbers: models. Curr. Opin. Genet. Dev. 15:2116–24
    [Google Scholar]
  15. 15. 
    Blinkowa AL, Walker JR. 1990. Programmed ribosomal frameshifting generates the Escherichia coli DNA polymerase III gamma subunit from within the tau subunit reading frame. Nucleic Acids Res 18:71725–29
    [Google Scholar]
  16. 16. 
    Block DHS, Hussein R, Liang LW, Lim HN. 2012. Regulatory consequences of gene translocation in bacteria. Nucleic Acids Res 40:188979–92
    [Google Scholar]
  17. 17. 
    Boël G, Letso R, Neely H, Price WN, Wong K-H et al. 2016. Codon influence on protein expression in E. coli correlates with mRNA levels. Nature 529:7586358–63
    [Google Scholar]
  18. 18. 
    Borujeni AE, Salis HM. 2016. Translation initiation is controlled by RNA folding kinetics via a ribosome drafting mechanism. J. Am. Chem. Soc. 138:227016–23
    [Google Scholar]
  19. 19. 
    Brar GA, Weissman JS. 2015. Ribosome profiling reveals the what, when, where and how of protein synthesis. Nat. Rev. Mol. Cell Biol. 16:651–64
    [Google Scholar]
  20. 20. 
    Brewster RC, Jones DL, Phillips R. 2012. Tuning promoter strength through RNA polymerase binding site design in Escherichia coli. PLOS Comput. Biol. 8:12e1002811
    [Google Scholar]
  21. 21. 
    Broglia L, Lécrivain A-L, Renault TT, Hahnke K, Ahmed-Begrich R et al. 2020. An RNA-seq based comparative approach reveals the transcriptome-wide interplay between 3′-to-5′ exoRNases and RNase Y. Nat. Commun. 11:1587
    [Google Scholar]
  22. 22. 
    Bryant JA, Sellars LE, Busby SJW, Lee DJ. 2014. Chromosome position effects on gene expression in Escherichia coli K-12. Nucleic Acids Res 42:1811383–92
    [Google Scholar]
  23. 23. 
    Buccitelli C, Selbach M. 2020. mRNAs, proteins and the emerging principles of gene expression control. Nat. Rev. Genet. 21:10630–44
    [Google Scholar]
  24. 24. 
    Burkhardt DH, Rouskin S, Zhang Y, Li G-W, Weissman JS, Gross CA. 2017. Operon mRNAs are organized into ORF-centric structures that predict translation efficiency. eLife 6:e22037
    [Google Scholar]
  25. 25. 
    Burton ZF, Gross CA, Watanabe KK, Burgess RR. 1983. The operon that encodes the sigma subunit of RNA polymerase also encodes ribosomal protein S21 and DNA primase in E. coli K12. Cell 32:2335–49
    [Google Scholar]
  26. 26. 
    Cam K, Rome G, Krisch HM, Bouché JP. 1996. RNase E processing of essential cell division genes mRNA in Escherichia coli. Nucleic Acids Res 24:153065–70
    [Google Scholar]
  27. 27. 
    Cambray G, Guimaraes JC, Arkin AP. 2018. Evaluation of 244,000 synthetic sequences reveals design principles to optimize translation in Escherichia coli. Nat. Biotechnol. 36:101005–15
    [Google Scholar]
  28. 28. 
    Cambray G, Guimaraes JC, Mutalik VK, Lam C, Mai Q-A et al. 2013. Measurement and modeling of intrinsic transcription terminators. Nucleic Acids Res 41:95139–48
    [Google Scholar]
  29. 29. 
    Chao Y, Li L, Girodat D, Förstner KU, Said N et al. 2017. In vivo cleavage map illuminates the central role of RNase E in coding and non-coding RNA pathways. Mol. Cell 65:139–51
    [Google Scholar]
  30. 30. 
    Chemla Y, Peeri M, Heltberg ML, Eichler J, Jensen MH et al. 2020. A possible universal role for mRNA secondary structure in bacterial translation revealed using a synthetic operon. Nat. Commun. 11:14827
    [Google Scholar]
  31. 31. 
    Chen H, Shiroguchi K, Ge H, Xie XS. 2015. Genome-wide study of mRNA degradation and transcript elongation in Escherichia coli. Mol. Syst. Biol. 11:781
    [Google Scholar]
  32. 32. 
    Chen Y-J, Liu P, Nielsen AAK, Brophy JAN, Clancy K et al. 2013. Characterization of 582 natural and synthetic terminators and quantification of their design constraints. Nat. Methods 10:7659–64
    [Google Scholar]
  33. 33. 
    Cho B-K, Zengler K, Qiu Y, Park YS, Knight EM et al. 2009. The transcription unit architecture of the Escherichia coli genome. Nat. Biotechnol. 27:111043–49
    [Google Scholar]
  34. 34. 
    Clarke JE, Kime L, Romero AD, McDowall KJ. 2014. Direct entry by RNase E is a major pathway for the degradation and processing of RNA in Escherichia coli. Nucleic Acids Res 42:1811733–51
    [Google Scholar]
  35. 35. 
    Commichau FM, Rothe FM, Herzberg C, Wagner E, Hellwig D et al. 2009. Novel activities of glycolytic enzymes in Bacillus subtilis: interactions with essential proteins involved in mRNA processing. Mol. Cell. Proteom. 8:61350–60
    [Google Scholar]
  36. 36. 
    Condon C. 2007. Maturation and degradation of RNA in bacteria. Curr. Opin. Microbiol. 10:271–78
    [Google Scholar]
  37. 37. 
    Conway T, Creecy JP, Maddox SM, Grissom JE, Conkle TL et al. 2014. Unprecedented high-resolution view of bacterial operon architecture revealed by RNA sequencing. mBio 5:4e01442-14
    [Google Scholar]
  38. 38. 
    Cooper S, Helmstetter CE. 1968. Chromosome replication and the division cycle of Escherichia coli Br. J. Mol. Biol. 31:3519–40
    [Google Scholar]
  39. 39. 
    Craigen WJ, Caskey CT. 1986. Expression of peptide chain release factor 2 requires high-efficiency frameshift. Nature 322:6076273–75
    [Google Scholar]
  40. 40. 
    Creecy JP, Conway T. 2015. Quantitative bacterial transcriptomics with RNA-seq. Curr. Opin. Microbiol. 23:133–40
    [Google Scholar]
  41. 41. 
    Dai X, Zhu M, Warren M, Balakrishnan R, Patsalo V et al. 2016. Reduction of translating ribosomes enables Escherichia coli to maintain elongation rates during slow growth. Nat. Microbiol. 2:16231
    [Google Scholar]
  42. 42. 
    Dame RT, Rashid F-ZM, Grainger DC. 2020. Chromosome organization in bacteria: mechanistic insights into genome structure and function. Nat. Rev. Genet. 21:4227–42
    [Google Scholar]
  43. 43. 
    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]
  44. 44. 
    Dar D, Sorek R. 2018. Extensive reshaping of bacterial operons by programmed mRNA decay. PLOS Genet 14:4e1007354
    [Google Scholar]
  45. 45. 
    Deana A, Celesnik H, Belasco JG. 2008. The bacterial enzyme RppH triggers messenger RNA degradation by 5′ pyrophosphate removal. Nature 451:355–58
    [Google Scholar]
  46. 46. 
    Del Campo C, Bartholomäus A, Fedyunin I, Ignatova Z. 2015. Secondary structure across the bacterial transcriptome reveals versatile roles in mRNA regulation and function. PLOS Genet 11:10e1005613
    [Google Scholar]
  47. 47. 
    DeLoughery A, Dengler V, Chai Y, Losick R. 2016. Biofilm formation by Bacillus subtilis requires an endoribonuclease-containing multisubunit complex that controls mRNA levels for the matrix gene repressor SinR. Mol. Microbiol. 99:2425–37
    [Google Scholar]
  48. 48. 
    DeLoughery A, Lalanne J-B, Losick R, Li G-W. 2018. Maturation of polycistronic mRNAs by the endoribonuclease RNase Y and its associated Y-complex in Bacillus subtilis. PNAS 115:E5585–94
    [Google Scholar]
  49. 49. 
    DiChiara JM, Liu B, Figaro S, Condon C, Bechhofer DH. 2016. Mapping of internal monophosphate 5′ ends of Bacillus subtilis messenger RNAs and ribosomal RNAs in wild-type and ribonuclease-mutant strains. Nucleic Acids Res 44:73373–89
    [Google Scholar]
  50. 50. 
    Dong H, Nilsson L, Kurland CG. 1996. Co-variation of tRNA abundance and codon usage in Escherichia coli at different growth rates. J. Mol. Biol. 260:5649–63
    [Google Scholar]
  51. 51. 
    Dorléans A, de la Sierra-Gallay IL, Piton J, Zig L, Gilet L et al. 2011. Molecular basis for the recognition and cleavage of RNA by the bifunctional 5′-3′ exo/endoribonuclease RNase J. Structure 19:1252–61
    [Google Scholar]
  52. 52. 
    Dorman CJ. 2006. DNA supercoiling and bacterial gene expression. Sci. Prog. 89:Part 3–4151–66
    [Google Scholar]
  53. 53. 
    Durand S, Gilet L, Bessières P, Nicolas P, Condon C 2012. Three essential ribonucleases—RNase Y, J1, and III—control the abundance of a majority of Bacillus subtilis mRNAs. PLOS Genet 8:e1002520
    [Google Scholar]
  54. 54. 
    Eisen MB, Spellman PT, Brown PO, Botstein D. 1998. Cluster analysis and display of genome-wide expression patterns. PNAS 95:2514863–68 Erratum 1999. PNAS 96:1910943
    [Google Scholar]
  55. 55. 
    Elf J, Nilsson D, Tenson T, Ehrenberg M. 2003. Selective charging of tRNA isoacceptors explains patterns of codon usage. Science 300:56261718–22
    [Google Scholar]
  56. 56. 
    Epshtein V, Nudler E. 2003. Cooperation between RNA polymerase molecules in transcription elongation. Science 300:5620801–5
    [Google Scholar]
  57. 57. 
    Borujeni AE, Cetnar D, Farasat I, Smith A, Lundgren N, Salis HM 2017. Precise quantification of translation inhibition by mRNA structures that overlap with the ribosomal footprint in N-terminal coding sequences. Nucleic Acid Res 45:5437–48
    [Google Scholar]
  58. 58. 
    Eyre-Walker A, Bulmer M 1993. Reduced synonymous substitution rate at the start of enterobacterial genes. Nucleic Acids Res 21:194599–603
    [Google Scholar]
  59. 59. 
    Farabaugh PJ. 1996. Programmed translational frameshifting. Annu. Rev. Genet. 30:507–28
    [Google Scholar]
  60. 60. 
    Ferrin MA, Subramaniam AR. 2017. Kinetic modeling predicts a stimulatory role for ribosome collisions at elongation stall sites in bacteria. eLife 6:e23629
    [Google Scholar]
  61. 61. 
    Figaro S, Durand S, Gilet L, Cayet N, Sachse M, Condon C. 2013. Bacillus subtilis mutants with knockouts of the genes encoding ribonucleases RNase Y and RNase J1 are viable, with major defects in cell morphology, sporulation, and competence. J. Bacteriol. 195:2340–48
    [Google Scholar]
  62. 62. 
    Flower AM, McHenry CS. 1990. The gamma subunit of DNA polymerase III holoenzyme of Escherichia coli is produced by ribosomal frameshifting. PNAS 87:103713–17
    [Google Scholar]
  63. 63. 
    Foley PL, Hsieh P-K, Luciano DJ, Belasco JG. 2015. Specificity and evolutionary conservation of the Escherichia coli RNA pyrophosphohydrolase RppH. J. Biol. Chem. 290:159478–86
    [Google Scholar]
  64. 64. 
    Forcier TL, Ayaz A, Gill MS, Jones D, Phillips R, Kinney JB. 2018. Measuring cis-regulatory energetics in living cells using allelic manifolds. eLife 7:e40618
    [Google Scholar]
  65. 65. 
    Fremin BJ, Sberro H, Bhatt AS. 2020. MetaRibo-Seq measures translation in microbiomes. Nat. Commun. 11:13268
    [Google Scholar]
  66. 66. 
    Frindert J, Zhang Y, Nübel G, Kahloon M, Kolmar L et al. 2018. Identification, biosynthesis, and decapping of NAD-capped RNAs in B. subtilis. Cell Rep 24:1890–901.e8
    [Google Scholar]
  67. 67. 
    Garmendia E, Brandis G, Hughes D. 2018. Transcriptional regulation buffers gene dosage effects on a highly expressed operon in Salmonella. mBio 9:e01446-18
    [Google Scholar]
  68. 68. 
    Goodman DB, Church GM, Kosuri S. 2013. Causes and effects of N-terminal codon bias in bacterial genes. Science 342:6157475–79
    [Google Scholar]
  69. 69. 
    Goormans AR, Snoeck N, Decadt H, Vermeulen K, Peters G et al. 2020. Comprehensive study on Escherichia coli genomic expression: Does position really matter?. Metab. Eng. 62:10–19
    [Google Scholar]
  70. 70. 
    Gorochowski TE, Chelysheva I, Eriksen M, Nair P, Pedersen S, Ignatova Z. 2019. Absolute quantification of translational regulation and burden using combined sequencing approaches. Mol. Syst. Biol. 15:5e8719
    [Google Scholar]
  71. 71. 
    Grünberger F, Knüppel R, Jüttner M, Fenk M, Borst A et al. 2020. Exploring prokaryotic transcription, operon structures, rRNA maturation and modifications using Nanopore-based native RNA sequencing. bioRxiv 2019.12.18.880849. https://doi.org/10.1101/2019.12.18.880849
    [Crossref]
  72. 72. 
    Güell M, van Noort V, Yus E, Chen W-H, Leigh-Bell J et al. 2009. Transcriptome complexity in a genome-reduced bacterium. Science 326:59571268–71
    [Google Scholar]
  73. 73. 
    Gusarov I, Nudler E. 2001. Control of intrinsic transcription termination by N and NusA: the basic mechanisms. Cell 107:437–49
    [Google Scholar]
  74. 74. 
    Hackett SR, Zanotelli VRT, Xu W, Goya J, Park JO et al. 2016. Systems-level analysis of mechanisms regulating yeast metabolic flux. Science 354:6311aaf2786
    [Google Scholar]
  75. 75. 
    Harden TT, Wells CD, Friedman LJ, Landick R, Hochschild A et al. 2016. Bacterial RNA polymerase can retain σ70 throughout transcription. PNAS 113:3602–7
    [Google Scholar]
  76. 76. 
    Hausser J, Mayo A, Keren L, Alon U 2019. Central dogma rates and the trade-off between precision and economy in gene expression. Nat. Commun. 10:168
    [Google Scholar]
  77. 77. 
    Hör J, Gorski SA, Vogel J. 2018. Bacterial RNA biology on a genome scale. Mol. Cell 70:785–99
    [Google Scholar]
  78. 78. 
    Hsieh P-K, Richards J, Liu Q, Belasco JG. 2013. Specificity of RppH-dependent RNA degradation in Bacillus subtilis. PNAS 110:228864–69
    [Google Scholar]
  79. 79. 
    Hudson AJ, Wieden H-J. 2019. Rapid generation of sequence-diverse terminator libraries and their parameterization using quantitative Term-Seq. Synth. Biol. 4:1ysz026
    [Google Scholar]
  80. 80. 
    Hui MP, Foley PL, Belasco JG. 2014. Messenger RNA degradation in bacterial cells. Annu. Rev. Genet. 48:537–59
    [Google Scholar]
  81. 81. 
    Ingolia NT, Ghaemmaghami S, Newman JRS, Weissman JS. 2009. Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling. Science 324:5924218–23
    [Google Scholar]
  82. 82. 
    Ireland WT, Beeler SM, Flores-Bautista E, McCarty NS, Röschinger T et al. 2020. Deciphering the regulatory genome of Escherichia coli, one hundred promoters at a time. eLife 9:e55308
    [Google Scholar]
  83. 83. 
    Jacob F, Monod J. 1961. Genetic regulatory mechanisms in the synthesis of proteins. J. Mol. Biol. 3:318–56
    [Google Scholar]
  84. 84. 
    Johnson GE, Lalanne J-B, Peters ML, Li G-W. 2020. Functionally uncoupled transcription-translation in Bacillus subtilis. Nature 585:124–28
    [Google Scholar]
  85. 85. 
    Ju X, Li D, Liu S. 2019. Full-length RNA profiling reveals pervasive bidirectional transcription terminators in bacteria. Nat. Microbiol. 4:111907–18
    [Google Scholar]
  86. 86. 
    Kelsic ED, Chung H, Cohen N, Park J, Wang HH, Kishony R. 2016. RNA structural determinants of optimal codons revealed by MAGE-Seq. Cell Syst 3:6563–71.e6
    [Google Scholar]
  87. 87. 
    Kennell D, Riezman H. 1977. Transcription and translation initiation frequencies of the Escherichia coli lac operon. J. Mol. Biol. 114:11–21
    [Google Scholar]
  88. 88. 
    Keren L, Hausser J, Lotan-Pompan M, Vainberg Slutskin I, Alisar H et al. 2016. Massively parallel interrogation of the effects of gene expression levels on fitness. Cell 166:51282–94.e18
    [Google Scholar]
  89. 89. 
    Khemici V, Prados J, Linder P, Redder P. 2015. Decay-initiating endoribonucleolytic cleavage by RNase Y is kept under tight control via sequence preference and sub-cellular localisation. PLOS Genet 11:e1005577
    [Google Scholar]
  90. 90. 
    Kim S, Beltran B, Irnov I, Jacobs-Wagner C. 2019. Long-distance cooperative and antagonistic RNA polymerase dynamics via DNA supercoiling. Cell 179:106–19.e16
    [Google Scholar]
  91. 91. 
    Kinney JB, McCandlish DM. 2019. Massively parallel assays and quantitative sequence-function relationships. Annu. Rev. Genomics Hum. Genet. 20:99–127
    [Google Scholar]
  92. 92. 
    Kinney JB, Murugan A, Callan CG Jr., Cox EC. 2010. Using deep sequencing to characterize the biophysical mechanism of a transcriptional regulatory sequence. PNAS 107:209158–63
    [Google Scholar]
  93. 93. 
    Klumpp S, Dong J, Hwa T 2012. On ribosome load, codon bias and protein abundance. PLOS ONE 7:11e48542
    [Google Scholar]
  94. 94. 
    Kudla G, Murray AW, Tollervey D, Plotkin JB. 2009. Coding-sequence determinants of gene expression in Escherichia coli. Science 324:5924255–58
    [Google Scholar]
  95. 95. 
    Kuo S-T, Jahn R-L, Cheng Y-J, Chen Y-L, Lee Y-J et al. 2020. Global fitness landscapes of the Shine-Dalgarno sequence. Genome Res 30:5711–23
    [Google Scholar]
  96. 96. 
    Laalami S, Bessières P, Rocca A, Zig L, Nicolas P, Putzer H 2013. Bacillus subtilis RNase Y activity in vivo analysed by tiling microarrays. PLOS ONE 8:e54062
    [Google Scholar]
  97. 97. 
    Lalanne J-B, Parker DG, Li G-W. 2021. Spurious regulatory connections dictate the expression-fitness landscape of translation factors. Mol. Syst. Biol. 17:e10302
    [Google Scholar]
  98. 98. 
    Lalanne J-B, Taggart JC, Guo MS, Herzel L, Schieler A, Li G-W. 2018. Evolutionary convergence of pathway-specific enzyme expression stoichiometry. Cell 173:3749–61.e38
    [Google Scholar]
  99. 99. 
    Lehnik-Habrink M, Schaffer M, Mäder U, Diethmaier C, Herzberg C, Stülke J. 2011. RNA processing in Bacillus subtilis: identification of targets of the essential RNase Y. Mol. Microbiol. 81:1459–73
    [Google Scholar]
  100. 100. 
    Lemaux PG, Herendeen SL, Bloch PL, Neidhardt FC. 1978. Transient rates of synthesis of individual polypeptides in E. coli following temperature shifts. Cell 13:427–34
    [Google Scholar]
  101. 101. 
    Li G-W. 2015. How do bacteria tune translation efficiency?. Curr. Opin. Microbiol. 24:66–71
    [Google Scholar]
  102. 102. 
    Li G-W, Burkhardt D, Gross C, Weissman JS. 2014. Quantifying absolute protein synthesis rates reveals principles underlying allocation of cellular resources. Cell 157:624–35
    [Google Scholar]
  103. 103. 
    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]
  104. 104. 
    Li S, Dong X, Su Z 2013. Directional RNA-seq reveals highly complex condition-dependent transcriptomes in E. coli K12 through accurate full-length transcripts assembling. BMC Genomics 14:520
    [Google Scholar]
  105. 105. 
    Lodish HF. 1968. Bacteriophage f2 RNA: control of translation and gene order. Nature 220:5165345–50
    [Google Scholar]
  106. 106. 
    Luciano DJ, Hui MP, Deana A, Foley PL, Belasco KJ, Belasco JG. 2012. Differential control of the rate of 5′-end-dependent mRNA degradation in Escherichia coli. J. Bacteriol. 194:226233–39
    [Google Scholar]
  107. 107. 
    Luciano DJ, Vasilyev N, Richards J, Serganov A, Belasco JG. 2017. A novel RNA phosphorylation state enables 5′ end-dependent degradation in Escherichia coli. Mol. Cell 67:144–54.e6
    [Google Scholar]
  108. 108. 
    Mandell ZF, Oshiro RT, Yakhnin AV, Vishwakarma R, Kashlev M et al. 2021. NusG is an intrinsic transcription termination factor that stimulates motility and coordinates gene expression with NusA. eLife 10:e61880
    [Google Scholar]
  109. 109. 
    Marincola G, Schäfer T, Behler J, Bernhardt J, Ohlsen K et al. 2012. RNase Y of Staphylococcus aureus and its role in the activation of virulence genes. Mol. Microbiol. 85:817–32
    [Google Scholar]
  110. 110. 
    Marincola G, Wolz C. 2017. Downstream element determines RNase Y cleavage of the saePQRS operon in Staphylococcus aureus. Nucleic Acids Res 45:5980–94
    [Google Scholar]
  111. 111. 
    McCarthy JEG, Gualerzi C. 1990. Translational control of prokaryotic gene expression. Trends Genet 6:78–85
    [Google Scholar]
  112. 112. 
    McCormick DM, Lalanne J-B, Lan TCT, Rouskin S, Li G-W. 2021. Differential translation of mRNA isoforms transcribed with distinct sigma factors. RNA 27:791804
    [Google Scholar]
  113. 113. 
    McDowall KJ, Kaberdin VR, Wu SW, Cohen SN, Lin-Chao S. 1995. Site-specific RNase E cleavage of oligonucleotides and inhibition by stem-loops. Nature 374:6519287–90
    [Google Scholar]
  114. 114. 
    McDowall KJ, Lin-Chao S, Cohen SN. 1994. A+U content rather than a particular nucleotide order determines the specificity of RNase E cleavage. J. Biol. Chem. 269:1410790–96
    [Google Scholar]
  115. 115. 
    Mejía-Almonte C, Busby SJW, Wade JT, van Helden J, Arkin AP et al. 2020. Redefining fundamental concepts of transcription initiation in bacteria. Nat. Rev. Genet. 21:11699–714
    [Google Scholar]
  116. 116. 
    Mendoza-Vargas A, Olvera L, Olvera M, Grande R, Vega-Alvarado L et al. 2009. Genome-wide identification of transcription start sites, promoters and transcription factor binding sites in E. coli. PLOS ONE 4:10e7526
    [Google Scholar]
  117. 117. 
    Meydan S, Klepacki D, Karthikeyan S, Margus T, Thomas P et al. 2017. Programmed ribosomal frameshifting generates a copper transporter and a copper chaperone from the same gene. Mol. Cell 65:207–19
    [Google Scholar]
  118. 118. 
    Moffitt JR, Pandey S, Boettiger AN, Wang S, Zhuang X. 2016. Spatial organization shapes the turnover of a bacterial transcriptome. eLife 5:e13065
    [Google Scholar]
  119. 119. 
    Mohammad F, Green R, Buskirk AR. 2019. A systematically-revised ribosome profiling method for bacteria reveals pauses at single-codon resolution. eLife 8:e42591
    [Google Scholar]
  120. 120. 
    Mohanty BK, Kushner SR. 2016. Regulation of mRNA decay in bacteria. Annu. Rev. Microbiol. 70:25–44
    [Google Scholar]
  121. 121. 
    Mondal S, Yakhnin AV, Sebastian A, Albert I, Babitzke P 2016. NusA-dependent transcription termination prevents misregulation of global gene expression. Nat. Microbiol. 1:15007
    [Google Scholar]
  122. 122. 
    Mustoe AM, Busan S, Rice GM, Hajdin CE, Peterson BK et al. 2018. Pervasive regulatory functions of mRNA structure revealed by high-resolution SHAPE probing. Cell 173:1181–95.e18
    [Google Scholar]
  123. 123. 
    Mutalik VK, Guimaraes JC, Cambray G, Lam C, Christoffersen MJ et al. 2013. Precise and reliable gene expression via standard transcription and translation initiation elements. Nat. Methods 10:354–60
    [Google Scholar]
  124. 124. 
    Nakatogawa H, Ito K. 2001. Secretion monitor, SecM, undergoes self-translation arrest in the cytosol. Mol. Cell 7:1185–92
    [Google Scholar]
  125. 125. 
    Narayanan CS, Dubnau D. 1985. Evidence for the translational attenuation model: ribosome-binding studies and structural analysis with an in vitro run-off transcript of ermC. Nucleic Acids Res 13:7307–26
    [Google Scholar]
  126. 126. 
    Nomura M, Gourse R, Baughman G. 1984. Regulation of the synthesis of ribosomes and ribosomal components. Annu. Rev. Biochem. 53:75–117
    [Google Scholar]
  127. 127. 
    Oeschger MP, Nathans D. 1966. Differential synthesis of bacteriophage-specific proteins in MS2-infected Escherichia coli treated with actinomycin. J. Mol. Biol. 22:2235–47
    [Google Scholar]
  128. 128. 
    Ohtaka Y, Spiegelman S. 1963. Translational control of protein synthesis in a cell-free system directed by a polycistronic viral RNA. Science 142:493–97
    [Google Scholar]
  129. 129. 
    Opdyke JA, Fozo EM, Hemm MR, Storz G. 2011. RNase III participates in GadY-dependent cleavage of the gadX-gadW mRNA. J. Mol. Biol. 406:129–43
    [Google Scholar]
  130. 130. 
    Oromendia AB, Dodgson SE, Amon A. 2012. Aneuploidy causes proteotoxic stress in yeast. Genes Dev 26:242696–2708
    [Google Scholar]
  131. 131. 
    Papenfort K, Sun Y, Miyakoshi M, Vanderpool CK, Vogel J. 2013. Small RNA-mediated activation of sugar phosphatase mRNA regulates glucose homeostasis. Cell 153:426–37
    [Google Scholar]
  132. 132. 
    Parker DJ, Lalanne J-B, Kimura S, Johnson GE, Waldor MK, Li G-W. 2020. Growth-optimized aminoacyl-tRNA synthetase levels prevent maximal tRNA charging. Cell Syst 11:2121–30.e6
    [Google Scholar]
  133. 133. 
    Peters JM, Colavin A, Shi H, Czarny TL, Larson MH et al. 2016. A comprehensive, CRISPR-based functional analysis of essential genes in bacteria. Cell 165:61493–506
    [Google Scholar]
  134. 134. 
    Pette D, Luh W, Buecher T. 1962. A constant-proportion group in the enzyme activity pattern of the Embden-Meyerhof chain. Biochem. Biophys. Res. Commun. 7:419–24
    [Google Scholar]
  135. 135. 
    Pitt ME, Nguyen SH, Duarte TPS, Teng H, Blaskovich MAT et al. 2020. Evaluating the genome and resistome of extensively drug-resistant Klebsiella pneumoniae using native DNA and RNA Nanopore sequencing. Gigascience 9:giaa002
    [Google Scholar]
  136. 136. 
    Price MN. 2005. Operon formation is driven by co-regulation and not by horizontal gene transfer. Genome Res 15:809–19
    [Google Scholar]
  137. 137. 
    Quax TEF, Wolf YI, Koehorst JJ, Wurtzel O, van der Oost R et al. 2013. Differential translation tunes uneven production of operon-encoded proteins. Cell Rep 4:5938–44
    [Google Scholar]
  138. 138. 
    Rackham O, Chin JW. 2005. A network of orthogonal ribosome⋅mRNA pairs. Nat. Chem. Biol. 1:159–66
    [Google Scholar]
  139. 139. 
    Ray-Soni A, Bellecourt MJ, Landick R. 2016. Mechanisms of bacterial transcription termination: All good things must end. Annu. Rev. Biochem. 85:319–47
    [Google Scholar]
  140. 140. 
    Redder P. 2018. Mapping 5′-ends and their phosphorylation state with EMOTE, TSS-EMOTE, and nEMOTE. Methods Enzymol 612:361–91
    [Google Scholar]
  141. 141. 
    Richards J, Belasco JG. 2019. Obstacles to scanning by RNase E govern bacterial mRNA lifetimes by hindering access to distal cleavage sites. Mol. Cell 74:2284–95.e5
    [Google Scholar]
  142. 142. 
    Richards J, Liu Q, Pellegrini O, Celesnik H, Yao S et al. 2011. An RNA pyrophosphohydrolase triggers 5′-exonucleolytic degradation of mRNA in Bacillus subtilis. Mol. Cell 43:6940–49
    [Google Scholar]
  143. 143. 
    Rochat T, Bouloc P, Repoila F. 2013. Gene expression control by selective RNA processing and stabilization in bacteria. FEMS Microbiol. Lett. 344:2104–13
    [Google Scholar]
  144. 144. 
    Roland KL, Powell FE, Turnbough CL Jr. 1985. Role of translation and attenuation in the control of pyrBI operon expression in Escherichia coli K-12. J. Bacteriol. 163:3991–99
    [Google Scholar]
  145. 145. 
    Rouskin S, Zubradt M, Washietl S, Kellis M, Weissman JS. 2014. Genome-wide probing of RNA structure reveals active unfolding of mRNA structures in vivo. Nature 505:7485701–5
    [Google Scholar]
  146. 146. 
    Saito K, Green R, Buskirk AR. 2020. Ribosome recycling is not critical for translational coupling in Escherichia coli. eLife 9:e59974
    [Google Scholar]
  147. 147. 
    Saito K, Green R, Buskirk AR. 2020. Translational initiation in E. coli occurs at the correct sites genome-wide in the absence of mRNA-rRNA base-pairing. eLife 9:e55002
    [Google Scholar]
  148. 148. 
    Sampson LL, Hendrix RW, Huang WM, Casjens SR. 1988. Translation initiation controls the relative rates of expression of the bacteriophage lambda late genes. PNAS 85:155439–43
    [Google Scholar]
  149. 149. 
    Sastry AV, Gao Y, Szubin R, Hefner Y, Xu S et al. 2019. The Escherichia coli transcriptome mostly consists of independently regulated modules. Nat. Commun. 10:5536
    [Google Scholar]
  150. 150. 
    Scharff LB, Childs L, Walther D, Bock R 2011. Local absence of secondary structure permits translation of mRNAs that lack ribosome-binding sites. PLOS Genet 7:6e1002155
    [Google Scholar]
  151. 151. 
    Schmid MB, Roth JR. 1987. Gene location affects expression level in Salmonella typhimurium. J. Bacteriol. 169:62872–75
    [Google Scholar]
  152. 152. 
    Scholz SA, Diao R, Wolfe MB, Fivenson EM, Lin XN, Freddolino PL. 2019. High-resolution mapping of the Escherichia coli chromosome reveals positions of high and low transcription. Cell Syst 8:3212–25.e9
    [Google Scholar]
  153. 153. 
    Schrader JM, Zhou B, Li G-W, Lasker K, Childers WS et al. 2014. The coding and noncoding architecture of the Caulobacter crescentus genome. PLOS Genet 10:7e1004463
    [Google Scholar]
  154. 154. 
    Schümperli D, McKenney K, Sobieski DA, Rosenberg M. 1982. Translational coupling at an intercistronic boundary of the Escherichia coli galactose operon. Cell 30:3865–71
    [Google Scholar]
  155. 155. 
    Shahbabian K, Jamalli A, Zig L, Putzer H. 2009. RNase Y, a novel endoribonuclease, initiates riboswitch turnover in Bacillus subtilis. EMBO J 28:3523–33
    [Google Scholar]
  156. 156. 
    Sharma CM, Hoffmann S, Darfeuille F, Reignier J, Findeiss S et al. 2010. The primary transcriptome of the major human pathogen Helicobacter pylori. Nature 464:7286250–55
    [Google Scholar]
  157. 157. 
    Shen BA, Landick R. 2019. Transcription of bacterial chromatin. J. Mol. Biol. 431:4040–66
    [Google Scholar]
  158. 158. 
    Shieh Y-W, Minguez P, Bork P, Auburger JJ, Guilbride DL et al. 2015. Operon structure and cotranslational subunit association direct protein assembly in bacteria. Science 350:6261678–80
    [Google Scholar]
  159. 159. 
    Shine J, Dalgarno L. 1974. The 3′-terminal sequence of Escherichia coli 16S ribosomal RNA: complementarity to nonsense triplets and ribosome binding sites. PNAS 71:41342–46
    [Google Scholar]
  160. 160. 
    Sousa C, de Lorenzo V, Cebolla A. 1997. Modulation of gene expression through chromosomal positioning in Escherichia coli. Microbiology 143:Part 62071–78
    [Google Scholar]
  161. 161. 
    Stead MB, Marshburn S, Mohanty BK, Mitra J, Pena Castillo L et al. 2011. Analysis of Escherichia coli RNase E and RNase III activity in vivo using tiling microarrays. Nucleic Acids Res 39:83188–203
    [Google Scholar]
  162. 162. 
    Stern-Ginossar N, Weisburd B, Michalski A, Le VTK, Hein MY et al. 2012. Decoding human cytomegalovirus. Science 338:61101088–93
    [Google Scholar]
  163. 163. 
    Subramaniam AR, Zid BM, O'Shea EK 2014. An integrated approach reveals regulatory controls on bacterial translation elongation. Cell 159:51200–11
    [Google Scholar]
  164. 164. 
    Swain PS. 2004. Efficient attenuation of stochasticity in gene expression through post-transcriptional control. J. Mol. Biol. 344:4965–76
    [Google Scholar]
  165. 165. 
    Taggart JC, Li G-W. 2018. Production of protein-complex components is stoichiometric and lacks general feedback regulation in eukaryotes. Cell Syst 7:6580–89.e4
    [Google Scholar]
  166. 166. 
    Taggart JC, Zauber H, Selbach M, Li G-W, McShane E. 2020. Keeping the proportions of protein complex components in check. Cell Syst 10:2125–32
    [Google Scholar]
  167. 167. 
    Takada A, Nagai K, Wachi M. 2005. A decreased level of FtsZ is responsible for inviability of RNase E-deficient cells. Genes Cells 10:7733–41
    [Google Scholar]
  168. 168. 
    Tamura M, Lee K, Miller CA, Moore CJ, Shirako Y et al. 2006. RNase E maintenance of proper FtsZ/FtsA ratio required for nonfilamentous growth of Escherichia coli cells but not for colony-forming ability. J. Bacteriol. 188:5145–52
    [Google Scholar]
  169. 169. 
    Tejada-Arranz A, de Crécy-Lagard V, de Reuse H. 2020. Bacterial RNA degradosomes: molecular machines under tight control. Trends Biochem. Sci. 45:142–57
    [Google Scholar]
  170. 170. 
    Trinquier A, Durand S, Braun F, Condon C. 2020. Regulation of RNA processing and degradation in bacteria. Biochem. Biophys. Acta Gene Regul. Mech. 1863:194505
    [Google Scholar]
  171. 171. 
    Tsuchihashi Z, Kornberg A. 1990. Translational frameshifting generates the gamma subunit of DNA polymerase III holoenzyme. PNAS 87:72516–20
    [Google Scholar]
  172. 172. 
    Tuller T, Carmi A, Vestsigian K, Navon S, Dorfan Y et al. 2010. An evolutionarily conserved mechanism for controlling the efficiency of protein translation. Cell 141:2344–54
    [Google Scholar]
  173. 173. 
    Urtecho G, Insigne KD, Tripp AD, Brinck M, Lubock NB et al. 2020. Genome-wide functional characterization of Escherichia coli promoters and regulatory elements responsible for their function. bioRxiv 2020.01.04.894907. https://doi.org/10.1101/2020.01.04.894907
    [Crossref]
  174. 174. 
    Urtecho G, Tripp AD, Insigne KD, Kim H, Kosuri S. 2019. Systematic dissection of sequence elements controlling σ70 promoters using a genomically encoded multiplexed reporter assay in Escherichia coli. Biochemistry 58:111539–51
    [Google Scholar]
  175. 175. 
    Verma M, Choi J, Cottrell KA, Lavagnino Z, Thomas EN et al. 2019. A short translational ramp determines the efficiency of protein synthesis. Nat. Commun. 10:15774
    [Google Scholar]
  176. 176. 
    Vilar JMG, Leibler S. 2003. DNA looping and physical constraints on transcription regulation. J. Mol. Biol. 331:5981–89
    [Google Scholar]
  177. 177. 
    von Hippel PH, Yager TD. 1991. Transcript elongation and termination are competitive kinetic processes. PNAS 88:62307–11
    [Google Scholar]
  178. 178. 
    Vora T, Hottes AK, Tavazoie S. 2009. Protein occupancy landscape of a bacterial genome. Mol. Cell 35:2247–53
    [Google Scholar]
  179. 179. 
    Vvedenskaya IO, Zhang Y, Goldman SR, Valenti A, Visone V et al. 2015. Massively systematic transcript end readout, “MASTER”: transcription start site selection, transcriptional slippage, and transcript yields. Mol. Cell 60:6953–65
    [Google Scholar]
  180. 180. 
    Wikström PM, Lind LK, Berg DE, Björk GR. 1992. Importance of mRNA folding and start codon accessibility in the expression of genes in a ribosomal protein operon of Escherichia coli. J. Mol. Biol. 224:949–66
    [Google Scholar]
  181. 181. 
    Wurtzel O, Dori-Bachash M, Pietrokovski S, Jurkevitch E, Sorek R. 2010. Mutation detection with next-generation resequencing through a mediator genome. PLOS ONE 5:12e15628
    [Google Scholar]
  182. 182. 
    Yamaguchi Y, Park J-H, Inouye M. 2011. Toxin-antitoxin systems in bacteria and archaea. Annu. Rev. Genet. 45:61–79
    [Google Scholar]
  183. 183. 
    Yan B, Boitano M, Clark TA, Ettwiller L. 2018. SMRT-Cappable-seq reveals complex operon variants in bacteria. Nat. Commun. 9:13676
    [Google Scholar]
  184. 184. 
    Yao S, Richards J, Belasco JG, Bechhofer DH. 2011. Decay of a model mRNA in Bacillus subtilis by a combination of RNase J1 5′ exonuclease and RNase Y endonuclease activities. J. Bacteriol. 193:6384–86
    [Google Scholar]
  185. 185. 
    Yarchuk O, Jacques N, Guillerez J, Dreyfus M. 1992. Interdependence of translation, transcription and mRNA degradation in the lacZ gene. J. Mol. Biol. 226:3581–96
    [Google Scholar]
  186. 186. 
    Yim SS, Johns NI, Park J, Gomes AL, McBee RM et al. 2019. Multiplex transcriptional characterizations across diverse bacterial species using cell-free systems. Mol. Syst. Biol. 15:8e8875
    [Google Scholar]
  187. 187. 
    Zheng H, Bai Y, Jiang M, Tokuyasu TA, Huang X et al. 2020. General quantitative relations linking cell growth and the cell cycle in Escherichia coli. Nat. Microbiol. 5:8995–1001
    [Google Scholar]
/content/journals/10.1146/annurev-micro-041921-012646
Loading
/content/journals/10.1146/annurev-micro-041921-012646
Loading

Data & Media loading...

  • Article Type: Review Article
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