Skip to main content
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1990 Jan;172(1):305–309. doi: 10.1128/jb.172.1.305-309.1990

Autogenous control is not sufficient to ensure steady-state growth rate-dependent regulation of the S10 ribosomal protein operon of Escherichia coli.

L Lindahl 1, J M Zengel 1
PMCID: PMC208433  PMID: 2152906

Abstract

The regulation of the S10 ribosomal protein operon of Escherichia coli was studied by using a lambda prophage containing the beginning of the S10 operon (including the promoter, leader, and first one and one-half structural genes) fused to lacZ. The synthesis of the lacZ fusion protein encoded by the phage showed the expected inhibition during oversynthesis of ribosomal protein L4, the autogenous regulatory protein of the S10 operon. Moreover, the fusion gene responded to a nutritional shift-up in the same way that genuine ribosomal protein genes did. However, the gene did not exhibit the expected growth rate-dependent regulation during steady-state growth. Thus, the genetic information carried on the prophage is sufficient for L4-mediated autogenous control and a normal nutritional shift-up response but is not sufficient for steady-state growth rate-dependent control. These results suggest that, at least for the 11-gene S10 ribosomal protein operon, additional regulatory processes are required to coordinate the synthesis of ribosomal proteins with cell growth rate and, furthermore, that sequences downstream of the proximal one and one-half genes of the operon are involved in this control.

Full text

PDF
305

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Chen C. Y., Beatty J. T., Cohen S. N., Belasco J. G. An intercistronic stem-loop structure functions as an mRNA decay terminator necessary but insufficient for puf mRNA stability. Cell. 1988 Feb 26;52(4):609–619. doi: 10.1016/0092-8674(88)90473-4. [DOI] [PubMed] [Google Scholar]
  2. Cole J. R., Nomura M. Changes in the half-life of ribosomal protein messenger RNA caused by translational repression. J Mol Biol. 1986 Apr 5;188(3):383–392. doi: 10.1016/0022-2836(86)90162-2. [DOI] [PubMed] [Google Scholar]
  3. Cole J. R., Nomura M. Translational regulation is responsible for growth-rate-dependent and stringent control of the synthesis of ribosomal proteins L11 and L1 in Escherichia coli. Proc Natl Acad Sci U S A. 1986 Jun;83(12):4129–4133. doi: 10.1073/pnas.83.12.4129. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Dennis P. P., Bremer H. Differential rate of ribosomal protein synthesis in Escherichia coli B/r. J Mol Biol. 1974 Apr 15;84(3):407–422. doi: 10.1016/0022-2836(74)90449-5. [DOI] [PubMed] [Google Scholar]
  5. Dennis P. P. In vivo stability, maturation and relative differential synthesis rates of individual ribosomal proteins in Escherichia coli B/r. J Mol Biol. 1974 Sep 5;88(1):25–41. doi: 10.1016/0022-2836(74)90293-9. [DOI] [PubMed] [Google Scholar]
  6. Dennis P. P., Nomura M. Regulation of the expression of ribosomal protein genes in Escherichia coli. J Mol Biol. 1975 Sep 5;97(1):61–76. doi: 10.1016/s0022-2836(75)80022-2. [DOI] [PubMed] [Google Scholar]
  7. Dennis P. P. Synthesis of individual ribosomal proteins in Escherichia coli B/r. J Mol Biol. 1974 Oct 15;89(1):223–232. [PubMed] [Google Scholar]
  8. Freedman L. P., Zengel J. M., Archer R. H., Lindahl L. Autogenous control of the S10 ribosomal protein operon of Escherichia coli: genetic dissection of transcriptional and posttranscriptional regulation. Proc Natl Acad Sci U S A. 1987 Sep;84(18):6516–6520. doi: 10.1073/pnas.84.18.6516. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Freedman L. P., Zengel J. M., Lindahl L. Genetic dissection of stringent control and nutritional shift-up response of the Escherichia coli S10 ribosomal protein operon. J Mol Biol. 1985 Oct 20;185(4):701–712. doi: 10.1016/0022-2836(85)90055-5. [DOI] [PubMed] [Google Scholar]
  10. Gausing K. Regulation of ribosome production in Escherichia coli: synthesis and stability of ribosomal RNA and of ribosomal protein messenger RNA at different growth rates. J Mol Biol. 1977 Sep 25;115(3):335–354. doi: 10.1016/0022-2836(77)90158-9. [DOI] [PubMed] [Google Scholar]
  11. Guidi-Rontani C., Danchin A., Ullmann A. Transcriptional control of polarity in Escherichia coli by cAMP. Mol Gen Genet. 1984;195(1-2):96–100. doi: 10.1007/BF00332730. [DOI] [PubMed] [Google Scholar]
  12. Lindahl L., Archer R. H., McCormick J. R., Freedman L. P., Zengel J. M. Translational coupling of the two proximal genes in the S10 ribosomal protein operon of Escherichia coli. J Bacteriol. 1989 May;171(5):2639–2645. doi: 10.1128/jb.171.5.2639-2645.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Lindahl L., Archer R., Zengel J. M. Transcription of the S10 ribosomal protein operon is regulated by an attenuator in the leader. Cell. 1983 May;33(1):241–248. doi: 10.1016/0092-8674(83)90353-7. [DOI] [PubMed] [Google Scholar]
  14. Lindahl L., Zengel J. M. Operon-specific regulation of ribosomal protein synthesis in Escherichia coli. Proc Natl Acad Sci U S A. 1979 Dec;76(12):6542–6546. doi: 10.1073/pnas.76.12.6542. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Lindahl L., Zengel J. M. Ribosomal genes in Escherichia coli. Annu Rev Genet. 1986;20:297–326. doi: 10.1146/annurev.ge.20.120186.001501. [DOI] [PubMed] [Google Scholar]
  16. Mizusawa S., Ward D. F. A bacteriophage lambda vector for cloning with BamHI and Sau3A. Gene. 1982 Dec;20(3):317–322. doi: 10.1016/0378-1119(82)90200-1. [DOI] [PubMed] [Google Scholar]
  17. Singer P., Nomura M. Stability of ribosomal protein mRNA and translational feedback regulation in Escherichia coli. Mol Gen Genet. 1985;199(3):543–546. doi: 10.1007/BF00330773. [DOI] [PubMed] [Google Scholar]
  18. Yates J. L., Nomura M. E. coli ribosomal protein L4 is a feedback regulatory protein. Cell. 1980 Sep;21(2):517–522. doi: 10.1016/0092-8674(80)90489-4. [DOI] [PubMed] [Google Scholar]
  19. Zengel J. M., Archer R. H., Freedman L. P., Lindahl L. Role of attenuation in growth rate-dependent regulation of the S10 r-protein operon of E. coli. EMBO J. 1984 Jul;3(7):1561–1565. doi: 10.1002/j.1460-2075.1984.tb02011.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Zengel J. M., Lindahl L. Transcription of ribosomal genes during a nutritional shift-up of Escherichia coli. J Bacteriol. 1986 Sep;167(3):1095–1097. doi: 10.1128/jb.167.3.1095-1097.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Zengel J. M., Mueckl D., Lindahl L. Protein L4 of the E. coli ribosome regulates an eleven gene r protein operon. Cell. 1980 Sep;21(2):523–535. doi: 10.1016/0092-8674(80)90490-0. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES