Translational Components in Prokaryotes: Genetics and Regulation of Ribosomes

Abstract

The regulation of the biosynthesis of ribosomes, which constitute the catalytic organelles for the translation reaction, is central for the adaptation of bacteria to different growth conditions. The synthesis of the different ribosomal ribonucleic acid (rRNA) and ribosomal protein (RP) components is controlled and coordinated by a complex network of regulatory mechanisms to adjust the translational capacity to the required cell demands. Regulation of rRNA transcription plays a key role in ribosome formation. Quality control steps are operated during processing and assembly to ensure functionally competent particles and to avoid the accumulation of defective products and waste of energy and resources.

Key concepts:

  • Bacterial growth rates depend on the number of ribosomes.

  • Ribosome synthesis is adapted to environmental changes.

  • Biosynthesis of ribosomes involves quality control steps.

  • Ribosome synthesis is determined by the rate of rRNA transcription.

  • Synthesis of many ribosomal proteins is adjusted to the amount of free rRNA by a translational feedback mechanism.

  • Many ribosomal proteins have extra‚Äźribosomal functions in the cell.

  • A limited number of sequence heterogeneities in the redundantly encoded rRNA genes provide the potential for the formation of specialized ribosomes.

  • The stringent control is one of the major mechanisms for the adaptation of ribosomes in response to nutritional changes.

Keywords: ribosome biogenesis; ribosomal proteins; ribosomal RNA; regulation; quality control

Figure 1.

Location and organization of ribosomal components on the E. coli chromosome. (a) Location of ribosomal RNA and ribosomal protein transcription units on the chromosomal map of E. coli. Transcription directions are indicated by arrows; oriC denotes the origin of replication (reproduced from Wagner R (2000) Transcription Regulation in Prokaryotes. By permission of Oxford University Press. www.oup.com). (b) rRNA operon gene arrangements. The upstream‐activating sequence (UAS) and the tandem promoters (P1, P2) are shown in red and the transcription terminators (T1, T2) are in blue. Structural genes are shown as green boxes. The position of the leader and spacer sequences are marked. Elements in square brackets are not present in all seven rRNA operons.

Figure 2.

Translational feedback regulation for the synthesis of RPs. (a) Mechanism for translational feedback of the S10 operon. L4, 1 of 11 genes of the S10 operon serves as translational repressor. At excess 23S rRNA it binds to the rRNA and enables ribosome formation. Under those conditions the S10 operon is continuously translated. If there is not enough 23S rRNA in the cell L4 accumulates and now binds to a target site within the leader region of the S10 operon. Binding to this site inhibits translation of the complete S10 operon. Hence, translation of the RP genes depends on the availability of rRNAs (reproduced from Wagner R (2000) Transcription Regulation in Prokaryotes. By permission of Oxford University Press. www.oup.com). (b) Ribosomal protein operons regulated by translational feedback. The name of each operon is given. P denotes the transcription start site. Individual genes of the operon are shown as green boxes and labelled according to the gene product. The regulatory product is indicated by a blue box. Genes labelled with + are under translational feedback regulation; genes indicated by − are not. In case of the L10 operon the regulator is a complex of L10(L7/L12)4.

Figure 3.

Schematic distribution of sequence heterogeneities among the seven E. colirRNA operons. Red lines indicate the approximate positions of sequence heterogeneities between the different operons with respect to the rrnB operon, which is taken as reference. Changes occur in all rRNAs with the exception of the 16S rRNA from the rrnE operon, the 5S rRNA from the rrnE operon and the 23S rRNA from the rrnG operon, which are identical with the respective rrnB sequences.

Figure 4.

Transcriptional control elements within a ribosomal RNA transcription unit. The upper line represents a typical rRNA transcription unit, as shown in 1. In the lower part the regulatory region is shown enlarged. The promoter recognition elements (−10, −35) and the transcription start sites (+1) are shown for the P1 and P2 promoter. The UP element, which contacts the RNA polymerase α subunit during transcription initiation, and the discriminator sequence responsible for stringent and growth rate regulation are indicated as grey boxes. Binding sites for the activator protein FIS are shown in green, whereas sites for the repressing transcription factors H‐NS and LRP are given in red or magenta, respectively. The position of the nut‐like leader sequence involved in antitermination and ribosome biogenesis is shown as a grey box. UAS, upstream‐activating sequence.

close

References

Al Refaii A and Alix JH (2009) Ribosome biogenesis is temperature‐dependent and delayed in E. coli lacking the chaperones DnaK or DnaJ. Molecular Microbiology 71(3): 748–762.

Artsimovitch I, Patlan V, Sekine S et al. (2004) Structural basis for transcription regulation by alarmone ppGpp. Cell 117(3): 299–310.

Bremer H and Ehrenberg M (1995) Guanosine tetraphosphate as a global regulator of bacterial RNA synthesis: a model involving RNA polymerase pausing and queuing. Biochimica et Biophysica Acta 1262: 15–36.

Cheng ZF and Deutscher MP (2003) Quality control of ribosomal RNA mediated by polynucleotide phosphorylase and RNase R. Proceedings of the National Academy of Sciences of the USA 100(11): 6388–6393.

Condon C, French S, Squires C and Squires CL (1993) Depletion of functional ribosomal RNA operons in E. coli causes increased expression of the remaining intact copies. EMBO Journal 12: 4305–4315.

Dennis PP, Ehrenberg M and Bremer H (2004) Control of rRNA synthesis in E. coli: a systems biology approach. Microbiology and Molecular Biology Reviews 63: 639–668.

Deutscher MP (2009) Chapter 9 maturation and degradation of ribosomal RNA in bacteria. Progress in Molecular Biology and Translational Sciences 85: 369–391.

Gaal T, Bartlett MS, Ross W, Turnbough C and Gourse RL (1997) Transcription regulation by initiating NTP concentration: rRNA synthesis in bacteria. Science 278: 2092–2097.

Gunderson JH, Sogin ML, Wollett G et al. (1987) Structurally distinct, stage specific ribosomes occur in Plasmodium. Science 238: 933–937.

Haugen SP, Ross W, Manrique M and Gourse RL (2008) Fine structure of the promoter‐{sigma} region 1.2 interaction. Proceedings of the National Academy of Sciences of the USA 105: 3292–3297.

Heinemann M and Wagner R (1997) Guanosine 3’,5’‐bis(diphosphate) (ppGpp)‐dependent inhibition of transcription from stringently controlled E. coli promoters can be explained by an altered initiation pathway that traps RNA polymerase. European Journal of Biochemistry 247: 990–999.

Hillebrand A, Wurm R, Menzel A and Wagner R (2005) The seven E. coli ribosomal RNA operon upstream regulatory regions differ in structure and transcription factor binding efficiencies. Biological Chemistry 386: 523–534.

Jensen KF and Pedersen S (1990) Metabolic growth rate control in E. coli may be a consequence of subsaturation of the macromolecular biosynthetic apparatus with substrates and catalytic components. Microbiological Reviews 54: 89–100.

Jinks‐Robertson S, Gourse RL and Nomura M (1983) Expression of rRNA and tRNA genes in E. coli: evidence for feedback regulation by products of rRNA operons. Cell 33: 865–867.

Kim HL, Shin EK, Kim HM et al. (2007) Heterogeneous rRNAs are differentially expressed during the morphological development of Streptomyces coelicolor. FEMS Microbiology Letters 275(1): 146–152.

Krasny L and Gourse RL (2004) An alternative strategy for bacterial ribosome synthesis: Bacillus subtilis rRNA transcription regulation. EMBO Journal 23(22): 4473–4483.

Krohn M and Wagner R (1996) Transcriptional pausing of RNA polymerase in the presence of guanosine tetraphosphate depends on the promoter and gene sequence. Journal of Biological Chemistry 271: 23884–23894.

Lindahl L and Zengel JM (1986) Ribosomal genes in E. coli. Annual Review of Genetics 20: 297–326.

Lopez‐Lopez A, Benlloch S, Bonfa M, Rodriguez‐Valera F and Mira A (2007) j Intragenomic 16S rDNA divergence in Haloarcula marismortui is an adaptation to different temperatures. Journal of Molecular Evolution 65(6): 687–696.

Mason SW and Greenblatt J (1991) Assembly of transcription elongation complexes containing the N protein of phage λ and the E. coli elongation factors NusA, NusB, NusG and S10. Genes & Development 5: 1504–1512.

Meng W, Belyaeva T, Savery NJ et al. (2001) UP element‐dependent transcription at the Echerichia coli rrnB P1 promoter: positional requirements and role of the RNA polymerase α subunit linker. Nucleic Acids Research 29: 4166–4178.

Paul BJ, Berkmen MB and Gourse RL (2005) DksA potentiates direct activation of amino acid promoters by ppGpp. Proceedings of the National Academy of Sciences of the USA 102(22): 7823–7828.

Perederina A, Svetlov V, Vassylyiva MN et al. (2004) Regulation through the secondary channel – structural framework for ppGpp‐DksA synergism during transcription. Cell 118: 297–309.

Pul Ü, Wurm R and Wagner R (2007) The role of LRP and H‐NS in transcription regulation: involvement of synergism, allostery and macromolecular crowding. Journal of Molecular Biology 366: 900–915.

Rutherford ST, Villers CL, Lee JH, Ross W and Gourse RL (2009) Allosteric control of E. coli rRNA promoter complexes by DksA. Genes & Development 23(2): 236–248.

Schäferkordt J and Wagner R (2001) Effects of base change mutations within an E. coli ribosomal RNA leader region on rRNA maturation and ribosome formation. Nucleic Acids Research 29: 3394–3403.

Singh D, Chang SJ, Lin PH et al. (2009) Regulation of ribonuclease E activity by the L4 ribosomal protein of E. coli. Proceedings of the National Academy of Sciences of the USA 106(3): 864–869.

Theissen G, Thelen L and Wagner R (1993) Some base substitutions in the leader of an E. coli ribosomal RNA operon affect the structure and function of ribosomes: evidence for a transient molecular scaffold‐like function of the rRNA leader. Journal of Molecular Biology 233: 203–218.

Vogel U and Jensen KF (1997) NusA is required for ribosomal antitermination and for modulation of the transcription elongation rate of both antiterminated RNA and mRNA. Journal of Biological Chemistry 272: 12265–12271.

Wool IG (1996) Extraribosomal functions of ribosomal proteins. Trends in Biochemical Sciences 21(5): 164–165.

Yoshida H, Yamamoto H, Uchiumi T and Wada A (2004) RMF inactivates ribosomes by covering the peptidyl transferase centre and entrance of peptide exit tunnel. Genes to Cells 9(4): 271–278.

Zacharias M, Göringer HU and Wagner R (1989) Influence of the GCGC discriminator motif introduced into the ribosomal RNA P2‐ and tac promoter on growth rate control and stringent sensitivity. EMBO Journal 11: 3357–3363.

Zengel JM and Lindahl L (1994) Diverse mechanisms for regulating ribosomal protein synthesis in E. coli. Progress in Nucleic Acid Research and Molecular Biology 47: 331–370.

Further Reading

Asato Y (2005) Control of ribosome synthesis during the cell division cycles of E. coli and Synechococcus. Current Issues in Molecular Biology 7(1): 109–117.

Condon C, Squires C and Squires CL (1995) Control of rRNA transcription in E. coli. Microbiological Reviews 59: 623–645.

Connolly K, Rife JP and Culver G (2008) Mechanistic insight into the ribosome biogenesis functions of the ancient protein KsgA. Molecular Microbiology 70(5): 1062–1075.

Kaczanovska M and Rydén‐Aulin M (2007) Ribosome Biogenesis and the translation process in E. coli. Microbiology and Molecular Biology Reviews 71: 477–494.

Maguire BA (2009) Inhibition of bacterial ribosome assembly: a suitable drug target? Microbiology and Molecular Biology Reviews 73(1): 22–35.

Paul BJ, Ross W, Gaal T and Gourse RL (2004) rRNA Transcription in E. coli. Annual Reviews of Genetics 38: 749–770.

Potrykus K and Cashel M (2008) (p)ppGpp: Still Magical? Annual Reviews of Microbiology 62: 35–51.

Wagner R (1994) The regulation of ribosomal RNA synthesis and bacterial cell growth. Archives of Microbiology 160: 100–109.

Wagner R (2000) Regulatory Networks, in Transcription Regulation in Prokaryotes, pp. 264–335. Oxford: Oxford University Press.

Wilson DN and Nierhaus KH (2007) The weird and wonderful world of bacterial ribosome regulation. Ctitical Reviews in Biochemistry and Molecular Biology 42: 187–219.

Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

How to Cite close
Wagner, Rolf(Dec 2009) Translational Components in Prokaryotes: Genetics and Regulation of Ribosomes. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0000538.pub2]