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Annual Review of Microbiology

Volume 76, 2022

Interdependency and Redundancy Add Complexity and Resilience to Biogenesis of Bacterial Ribosomes

Abstract

The pace and efficiency of ribosomal subunit production directly impact the fitness of bacteria. Biogenesis demands more than just the union of ribosomal components, including RNA and proteins, to form this functional ribonucleoprotein particle. Extra-ribosomal protein factors play a fundamental role in the efficiency and efficacy of ribosomal subunit biogenesis. A paucity of data on intermediate steps, multiple and overlapping pathways, and the puzzling number of functions that extra-ribosomal proteins appear to play in vivo make unraveling the formation of this macromolecular assemblage difficult. In this review, we outline with examples the multinodal landscape of factor-assisted mechanisms that influence ribosome synthesis in bacteria. We discuss in detail late-stage events that mediate correct ribosome formation and the transition to translation initiation and thereby ensure high-fidelity protein synthesis.

Keyword(s): assembly, biogenesis, maturation, quality control, ribosomal intermediates, ribosomal subunit
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2022-09-08
2024-05-13
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Literature Cited

  1. 1.
    Adilakshmi T, Bellur DL, Woodson SA. 2008. Concurrent nucleation of 16S folding and induced fit in 30S ribosome assembly. Nature 455:1268–72
     [Google Scholar]
  2. 2.
    Arai T, Ishiguro K, Kimura S, Sakaguchi Y, Suzuki T, Suzuki T. 2015. Single methylation of 23S rRNA triggers late steps of 50S ribosomal subunit assembly. PNAS 112:E4707–16
     [Google Scholar]
  3. 3.
    Awano N, Inouye M, Phadtare S. 2008. RNase activity of polynucleotide phosphorylase is critical at low temperature in Escherichia coli and is complemented by RNase II. J. Bacteriol. 190:5924–33
     [Google Scholar]
  4. 4.
    Balakrishnan R, Oman K, Shoji S, Bundschuh R, Fredrick K. 2014. The conserved GTPase LepA contributes mainly to translation initiation in Escherichia coli. Nucleic Acids Res 42:13370–83
     [Google Scholar]
  5. 5.
    Baumgardt K, Gilet L, Figaro S, Condon C. 2018. The essential nature of YqfG, a YbeY homologue required for 3′ maturation of Bacillus subtilis 16S ribosomal RNA is suppressed by deletion of RNase R. Nucleic Acids Res 46:8605–15
     [Google Scholar]
  6. 6.
    Belotserkovsky JM, Isak GI, Isaksson LA. 2011. Suppression of a cold-sensitive mutant initiation factor 1 by alterations in the 23S rRNA maturation region. FEBS J. 278:1745–56
     [Google Scholar]
  7. 7.
    Bharat A, Blanchard JE, Brown ED. 2013. A high-throughput screen of the GTPase activity of Escherichia coli EngA to find an inhibitor of bacterial ribosome biogenesis. J. Biomol. Screen. 18:830–36
     [Google Scholar]
  8. 8.
    Britton RA. 2009. Role of GTPases in bacterial ribosome assembly. Annu. Rev. Microbiol. 63:155–76
     [Google Scholar]
  9. 9.
    Bubunenko M, Court DL, Al Refaii A, Saxena S, Korepanov A et al. 2013. Nus transcription elongation factors and RNase III modulate small ribosome subunit biogenesis in Escherichia coli. Mol. Microbiol. 87:382–93
     [Google Scholar]
  10. 10.
    Bylund GO, Wipemo LC, Lundberg LA, Wikstrom PM. 1998. RimM and RbfA are essential for efficient processing of 16S rRNA in Escherichia coli. J. Bacteriol. 180:73–82
     [Google Scholar]
  11. 11.
    Campbell TL, Brown ED. 2008. Genetic interaction screens with ordered overexpression and deletion clone sets implicate the Escherichia coli GTPase YjeQ in late ribosome biogenesis. J. Bacteriol. 190:2537–45
     [Google Scholar]
  12. 12.
    Champney WS. 2020. Antibiotics targeting bacterial ribosomal subunit biogenesis. J. Antimicrob. Chemother. 75:787–806
     [Google Scholar]
  13. 13.
    Cheng ZF, Zuo Y, Li Z, Rudd KE, Deutscher MP. 1998. The vacB gene required for virulence in Shigella flexneri and Escherichia coli encodes the exoribonuclease RNase R. J. Biol. Chem. 273:14077–80
     [Google Scholar]
  14. 14.
    Choi E, Jeon H, Oh JI, Hwang J. 2019. Overexpressed L20 rescues 50S ribosomal subunit assembly defects of bipA-deletion in Escherichia coli. Front. Microbiol. 10:2982
     [Google Scholar]
  15. 15.
    Choudhury P, Flower AM. 2015. Efficient assembly of ribosomes is inhibited by deletion of bipA in Escherichia coli. J. Bacteriol. 197:1819–27
     [Google Scholar]
  16. 16.
    Connolly K, Culver G. 2013. Overexpression of RbfA in the absence of the KsgA checkpoint results in impaired translation initiation. Mol. Microbiol. 87:968–81
     [Google Scholar]
  17. 17.
    Connolly K, Rife JP, Culver G. 2008. Mechanistic insight into the ribosome biogenesis functions of the ancient protein KsgA. Mol. Microbiol. 70:1062–75
     [Google Scholar]
  18. 18.
    Cunningham PR, Weitzmann CJ, Nurse K, Masurel R, Van Knippenberg PH, Ofengand J. 1990. Site-specific mutation of the conserved m62A m62A residues of E. coli 16S ribosomal RNA: effects on ribosome function and activity of the ksgA methyltransferase. Biochim. Biophys. Acta 1050:18–26
     [Google Scholar]
  19. 19.
    Datta PP, Wilson DN, Kawazoe M, Swami NK, Kaminishi T et al. 2007. Structural aspects of RbfA action during small ribosomal subunit assembly. Mol. Cell 28:434–45
     [Google Scholar]
  20. 20.
    Davies BW, Kohrer C, Jacob AI, Simmons LA, Zhu J et al. 2010. Role of Escherichia coli YbeY, a highly conserved protein, in rRNA processing. Mol. Microbiol. 78:506–18
     [Google Scholar]
  21. 21.
    Davis JH, Williamson JR. 2017. Structure and dynamics of bacterial ribosome biogenesis. Philos. Trans. R. Soc. Lond. B 372:171620160181
     [Google Scholar]
  22. 22.
    Deutscher MP. 2009. Maturation and degradation of ribosomal RNA in bacteria. Prog. Mol. Biol. Transl. Sci. 85:369–91
     [Google Scholar]
  23. 23.
    Earnest TM, Lai J, Chen K, Hallock MJ, Williamson JR, Luthey-Schulten Z. 2015. Toward a whole-cell model of ribosome biogenesis: kinetic modeling of SSU assembly. Biophys. J. 109:1117–35
     [Google Scholar]
  24. 24.
    Foster C, Champney WS. 2008. Characterization of a 30S ribosomal subunit assembly intermediate found in Escherichia coli cells growing with neomycin or paromomycin. Arch. Microbiol. 189:441–49
     [Google Scholar]
  25. 25.
    Frazier AD, Champney WS. 2013. Inhibition of ribosomal subunit synthesis in Escherichia coli by the vanadyl ribonucleoside complex. Curr. Microbiol. 67:226–33
     [Google Scholar]
  26. 26.
    Ghosal A, Babu VMP, Walker GC. 2018. Elevated levels of era GTPase improve growth, 16S rRNA processing, and 70S ribosome assembly of Escherichia coli lacking highly conserved multifunctional YbeY endoribonuclease. J. Bacteriol. 200:17e00278–18
     [Google Scholar]
  27. 27.
    Gibbs MR, Moon KM, Chen M, Balakrishnan R, Foster LJ, Fredrick K. 2017. Conserved GTPase LepA (Elongation Factor 4) functions in biogenesis of the 30S subunit of the 70S ribosome. PNAS 114:980–85
     [Google Scholar]
  28. 28.
    Gibbs MR, Moon KM, Warner BR, Chen M, Bundschuh R et al. 2020. Functional analysis of BipA in E. coli reveals the natural plasticity of 50S subunit assembly. J. Mol. Biol. 432:5259–72
     [Google Scholar]
  29. 29.
    Gonzalez YMJA, Colston MJ, Cox RA. 1996. The rRNA operons of Mycobacterium smegmatis and Mycobacterium tuberculosis: comparison of promoter elements and of neighbouring upstream genes. Microbiology 142:Part 3667–74
     [Google Scholar]
  30. 30.
    Goto S, Kato S, Kimura T, Muto A, Himeno H. 2011. RsgA releases RbfA from 30S ribosome during a late stage of ribosome biosynthesis. EMBO J 30:104–14
     [Google Scholar]
  31. 31.
    Gourse RL, Gaal T, Bartlett MS, Appleman JA, Ross W 1996. rRNA transcription and growth rate-dependent regulation of ribosome synthesis in Escherichia coli. Annu. Rev. Microbiol. 50:645–77
     [Google Scholar]
  32. 32.
    Green R, Noller HF. 1996. In vitro complementation analysis localizes 23S rRNA posttranscriptional modifications that are required for Escherichia coli 50S ribosomal subunit assembly and function. RNA 2:1011–21
     [Google Scholar]
  33. 33.
    Grinwald M, Ron EZ 2013. The Escherichia coli translation-associated heat shock protein YbeY is involved in rRNA transcription antitermination. PLOS ONE 8:e62297
     [Google Scholar]
  34. 34.
    Gupta N, Culver GM. 2014. Multiple in vivo pathways for Escherichia coli small ribosomal subunit assembly occur on one pre-rRNA. Nat. Struct. Mol. Biol. 21:937–43
     [Google Scholar]
  35. 35.
    Gutgsell NS, Jain C. 2012. Role of precursor sequences in the ordered maturation of E. coli 23S ribosomal RNA. RNA 18:345–53
     [Google Scholar]
  36. 36.
    Hajnsdorf E, Carpousis AJ, Regnier P. 1994. Nucleolytic inactivation and degradation of the RNase III processed pnp message encoding polynucleotide phosphorylase of Escherichia coli. J. Mol. Biol. 239:439–54
     [Google Scholar]
  37. 37.
    Hartmann RK, Erdmann VA. 1989. Thermus thermophilus 16S rRNA is transcribed from an isolated transcription unit. J. Bacteriol. 171:2933–41
     [Google Scholar]
  38. 38.
    Hwang J, Inouye M. 2008. RelA functionally suppresses the growth defect caused by a mutation in the G domain of the essential Der protein. J. Bacteriol. 190:3236–43
     [Google Scholar]
  39. 39.
    Inoue K, Alsina J, Chen J, Inouye M 2003. Suppression of defective ribosome assembly in a rbfA deletion mutant by overexpression of Era, an essential GTPase in Escherichia coli. Mol. Microbiol. 48:1005–16
     [Google Scholar]
  40. 40.
    Jacob AI, Kohrer C, Davies BW, RajBhandary UL, Walker GC. 2013. Conserved bacterial RNase YbeY plays key roles in 70S ribosome quality control and 16S rRNA maturation. Mol. Cell 49:427–38
     [Google Scholar]
  41. 41.
    Jagessar KL, Jain C. 2010. Functional and molecular analysis of Escherichia coli strains lacking multiple DEAD-box helicases. RNA 16:1386–92
     [Google Scholar]
  42. 42.
    Jain C. 2008. The E. coli RhlE RNA helicase regulates the function of related RNA helicases during ribosome assembly. RNA 14:381–89
     [Google Scholar]
  43. 43.
    Jain C. 2009. Identification and characterization of growth suppressors of Escherichia coli strains lacking phosphorolytic ribonucleases. J. Bacteriol. 191:5622–27
     [Google Scholar]
  44. 44.
    Jain C. 2018. Role of ribosome assembly in Escherichia coli ribosomal RNA degradation. Nucleic Acids Res 46:11048–60
     [Google Scholar]
  45. 45.
    Karbstein K. 2007. Role of GTPases in ribosome assembly. Biopolymers 87:1–11
     [Google Scholar]
  46. 46.
    King TC, Schlessinger D. 1983. S1 nuclease mapping analysis of ribosomal RNA processing in wild type and processing deficient Escherichia coli. J. Biol. Chem. 258:12034–42
     [Google Scholar]
  47. 47.
    Kitahara K, Suzuki T. 2009. The ordered transcription of RNA domains is not essential for ribosome biogenesis in Escherichia coli. Mol. Cell 34:760–66
     [Google Scholar]
  48. 48.
    Krishnan K, Flower AM. 2008. Suppression of ΔbipA phenotypes in Escherichia coli by abolishment of pseudouridylation at specific sites on the 23S rRNA. J. Bacteriol. 190:7675–83
     [Google Scholar]
  49. 49.
    Leong V, Kent M, Jomaa A, Ortega J. 2013. Escherichia coli rimM and yjeQ null strains accumulate immature 30S subunits of similar structure and protein complement. RNA 19:789–802
     [Google Scholar]
  50. 50.
    Lindahl L. 1975. Intermediates and time kinetics of the in vivo assembly of Escherichia coli ribosomes. J. Mol. Biol. 92:15–37
     [Google Scholar]
  51. 51.
    Lovgren JM, Bylund GO, Srivastava MK, Lundberg LA, Persson OP et al. 2004. The PRC-barrel domain of the ribosome maturation protein RimM mediates binding to ribosomal protein S19 in the 30S ribosomal subunits. RNA 10:1798–812
     [Google Scholar]
  52. 52.
    Lu Q, Inouye M. 1998. The gene for 16S rRNA methyltransferase (ksgA) functions as a multicopy suppressor for a cold-sensitive mutant of era, an essential RAS-like GTP-binding protein in Escherichia coli. J. Bacteriol. 180:5243–46
     [Google Scholar]
  53. 53.
    Maguire BA. 2009. Inhibition of bacterial ribosome assembly: a suitable drug target?. Microbiol. Mol. Biol. Rev. 73:22–35
     [Google Scholar]
  54. 54.
    Moll I, Grill S, Grundling A, Blasi U. 2002. Effects of ribosomal proteins S1, S2 and the DeaD/CsdA DEAD-box helicase on translation of leaderless and canonical mRNAs in Escherichia coli. Mol. Microbiol. 44:1387–96
     [Google Scholar]
  55. 55.
    Naganathan A, Keltz R, Lyon H, Culver GM. 2021. Uncovering a delicate balance between endonuclease RNase III and ribosomal protein S15 in E. coli ribosome assembly. Biochimie 191:104–17
     [Google Scholar]
  56. 56.
    Naganathan A, Moore SD. 2013. Crippling the essential GTPase Der causes dependence on ribosomal protein L9. J. Bacteriol. 195:3682–91
     [Google Scholar]
  57. 57.
    Naganathan A, Wood MP, Moore SD. 2015. The large ribosomal subunit protein L9 enables the growth of EF-P deficient cells and enhances small subunit maturation. PLOS ONE 10:e0120060
     [Google Scholar]
  58. 58.
    Nashimoto H, Miura A, Saito H, Uchida H. 1985. Suppressors of temperature-sensitive mutations in a ribosomal protein gene, rpsL (S12), of Escherichia coli K12. Mol. Gen. Genet. 199:381–87
     [Google Scholar]
  59. 59.
    Nishi K, Schnier J. 1988. The phenotypic suppression of a mutation in the gene rplX for ribosomal protein L24 by mutations affecting the lon gene product for protease LA in Escherichia coli K12. Mol. Gen. Genet. 212:177–81
     [Google Scholar]
  60. 60.
    Nomura M, Traub P, Bechmann H. 1968. Hybrid 30S ribosomal particles reconstituted from components of different bacterial origins. Nature 219:793–99
     [Google Scholar]
  61. 61.
    Oerum S, Dendooven T, Catala M, Gilet L, Degut C et al. 2020. Structures of B. subtilis maturation RNases captured on 50S ribosome with pre-rRNAs. Mol. Cell 80:227–36.e5
     [Google Scholar]
  62. 62.
    O'Farrell HC, Xu Z, Culver GM, Rife JP. 2008. Sequence and structural evolution of the KsgA/Dim1 methyltransferase family. BMC Res. Notes 1:108
     [Google Scholar]
  63. 63.
    Ogle JM, Ramakrishnan V. 2005. Structural insights into translational fidelity. Annu. Rev. Biochem. 74:129–77
     [Google Scholar]
  64. 64.
    O'Hara EB, Chekanova JA, Ingle CA, Kushner ZR, Peters E, Kushner SR. 1995. Polyadenylylation helps regulate mRNA decay in Escherichia coli. PNAS 92:1807–11
     [Google Scholar]
  65. 65.
    Palade GE. 1955. A small particulate component of the cytoplasm. J. Biophys. Biochem. Cytol. 1:59–68
     [Google Scholar]
  66. 66.
    Poldermans B, Bakker H, Van Knippenberg PH. 1980. Studies on the function of two adjacent N6,N6-dimethyladenosines near the 3′ end of 16S ribosomal RNA of Escherichia coli. IV. The effect of the methylgroups on ribosomal subunit interaction. Nucleic Acids Res 8:143–51
     [Google Scholar]
  67. 67.
    Pulicherla N, Pogorzala LA, Xu Z, OF HC, Musayev FN et al. 2009. Structural and functional divergence within the Dim1/KsgA family of rRNA methyltransferases. J. Mol. Biol. 391:884–93
     [Google Scholar]
  68. 68.
    Ramakrishnan V, Moore PB. 2001. Atomic structures at last: the ribosome in 2000. Curr. Opin. Struct. Biol. 11:144–54
     [Google Scholar]
  69. 69.
    Razi A, Guarne A, Ortega J. 2017. The cryo-EM structure of YjeQ bound to the 30S subunit suggests a fidelity checkpoint function for this protein in ribosome assembly. PNAS 114:E3396–403
     [Google Scholar]
  70. 70.
    Roy-Chaudhuri B, Kirthi N, Culver GM. 2010. Appropriate maturation and folding of 16S rRNA during 30S subunit biogenesis are critical for translational fidelity. PNAS 107:4567–72
     [Google Scholar]
  71. 71.
    Roy-Chaudhuri B, Kirthi N, Kelley T, Culver GM. 2008. Suppression of a cold-sensitive mutation in ribosomal protein S5 reveals a role for RimJ in ribosome biogenesis. Mol. Microbiol. 68:1547–59
     [Google Scholar]
  72. 72.
    Seffouh A, Jain N, Jahagirdar D, Basu K, Razi A et al. 2019. Structural consequences of the interaction of RbgA with a 50S ribosomal subunit assembly intermediate. Nucleic Acids Res 47:10414–25
     [Google Scholar]
  73. 73.
    Sergeeva OV, Bogdanov AA, Sergiev PV. 2015. What do we know about ribosomal RNA methylation in Escherichia coli?. Biochimie 117:110–18
     [Google Scholar]
  74. 74.
    Sergiev PV, Golovina AY, Sergeeva OV, Osterman IA, Nesterchuk MV et al. 2012. How much can we learn about the function of bacterial rRNA modification by mining large-scale experimental datasets?. Nucleic Acids Res. 40:5694–705
     [Google Scholar]
  75. 75.
    Shajani Z, Sykes MT, Williamson JR. 2011. Assembly of bacterial ribosomes. Annu. Rev. Biochem. 80:501–26
     [Google Scholar]
  76. 76.
    Sharma IM, Woodson SA. 2020. RbfA and IF3 couple ribosome biogenesis and translation initiation to increase stress tolerance. Nucleic Acids Res 48:359–72
     [Google Scholar]
  77. 77.
    Shetty S, Varshney U. 2016. An evolutionarily conserved element in initiator tRNAs prompts ultimate steps in ribosome maturation. PNAS 113:E6126–34
     [Google Scholar]
  78. 78.
    Siibak T, Peil L, Xiong L, Mankin A, Remme J, Tenson T. 2009. Erythromycin- and chloramphenicol-induced ribosomal assembly defects are secondary effects of protein synthesis inhibition. Antimicrob. Agents Chemother. 53:563–71
     [Google Scholar]
  79. 79.
    Smith BA, Gupta N, Denny K, Culver GM. 2018. Characterization of 16S rRNA processing with pre-30S subunit assembly intermediates from E. coli. J. Mol. Biol. 430:1745–59
     [Google Scholar]
  80. 80.
    Song W, Kim YH, Sim SH, Hwang S, Lee JH et al. 2014. Antibiotic stress-induced modulation of the endoribonucleolytic activity of RNase III and RNase G confers resistance to aminoglycoside antibiotics in Escherichia coli. Nucleic Acids Res 42:4669–81
     [Google Scholar]
  81. 81.
    Strunk BS, Loucks CR, Su M, Vashisth H, Cheng S et al. 2011. Ribosome assembly factors prevent premature translation initiation by 40S assembly intermediates. Science 333:1449–53
     [Google Scholar]
  82. 82.
    Strunk BS, Novak MN, Young CL, Karbstein K. 2012. A translation-like cycle is a quality control checkpoint for maturing 40S ribosome subunits. Cell 150:111–21
     [Google Scholar]
  83. 83.
    Tamura M, Kers JA, Cohen SN. 2012. Second-site suppression of RNase E essentiality by mutation of the deaD RNA helicase in Escherichia coli. J. Bacteriol. 194:1919–26
     [Google Scholar]
  84. 84.
    Tan J, Jakob U, Bardwell JC 2002. Overexpression of two different GTPases rescues a null mutation in a heat-induced rRNA methyltransferase. J. Bacteriol. 184:2692–98
     [Google Scholar]
  85. 85.
    Thurlow B, Davis JH, Leong V, Moraes TF, Williamson JR, Ortega J. 2016. Binding properties of YjeQ (RsgA), RbfA, RimM and Era to assembly intermediates of the 30S subunit. Nucleic Acids Res 44:9918–32
     [Google Scholar]
  86. 86.
    Tissieres A, Watson JD. 1958. Ribonucleoprotein particles from Escherichia coli. Nature 182:778–80
     [Google Scholar]
  87. 87.
    Toone WM, Rudd KE, Friesen JD. 1991. deaD, a new Escherichia coli gene encoding a presumed ATP-dependent RNA helicase, can suppress a mutation in rpsB, the gene encoding ribosomal protein S2. J. Bacteriol. 173:3291–302
     [Google Scholar]
  88. 88.
    Traub P, Nomura M. 1968. Structure and function of E. coli ribosomes. V. Reconstitution of functionally active 30S ribosomal particles from RNA and proteins. PNAS 59:777–84
     [Google Scholar]
  89. 89.
    Wilson DN. 2014. Ribosome-targeting antibiotics and mechanisms of bacterial resistance. Nat. Rev. Microbiol. 12:35–48
     [Google Scholar]
  90. 90.
    Yassin A, Fredrick K, Mankin AS. 2005. Deleterious mutations in small subunit ribosomal RNA identify functional sites and potential targets for antibiotics. PNAS 102:16620–25
     [Google Scholar]
  91. 91.
    Zou J, Zhang W, Zhang H, Zhang XD, Peng B, Zheng J. 2018. Studies on aminoglycoside susceptibility identify a novel function of KsgA to secure translational fidelity during antibiotic stress. Antimicrob. Agents Chemother. 62:10e00853–18
     [Google Scholar]
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Interdependency and Redundancy Add Complexity and Resilience to Biogenesis of Bacterial Ribosomes
Annual Review of Microbiology 76, 193 (2022); https://doi.org/10.1146/annurev-micro-041020-121806
/content/journals/10.1146/annurev-micro-041020-121806
/content/journals/10.1146/annurev-micro-041020-121806
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