Abstract
We studied the effects of carbon starvation and of varying the growth rate on the activity of each of the two tandem ribosomal RNA promoters from the rrnA operon of Escherichia coli. The cellular abundance of plasmid-encoded transcripts arising at promoters P1 and P2 and terminating at the ribosomal RNA terminator in promoter-terminator fusions, together with transcript turnover rates, was used to estimate promoter activities. The rate of synthesis of the P1-promoted transcript was found to increase exponentially with growth rate and predominate at fast growth rates. The activity of the downstream promoter (P2) changed only slightly at different growth rates. Upon carbon starvation, little or no activity of the upstream promoter was detectable, while P2 activity persisted. We interpret this to mean that the dual promoters are differentially regulated so as to have separate adaptive and maintenance functions. This model simplifies most features of rRNA regulation known in E. coli.
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- Adhya S., Miller W. Modulation of the two promoters of the galactose operon of Escherichia coli. Nature. 1979 Jun 7;279(5713):492–494. doi: 10.1038/279492a0. [DOI] [PubMed] [Google Scholar]
- Chaloner-Larsson G., Yamazaki H. Adjustment of RNA content during temperature upshift in Escherichia coli. Biochem Biophys Res Commun. 1977 Jul 25;77(2):503–508. doi: 10.1016/s0006-291x(77)80008-9. [DOI] [PubMed] [Google Scholar]
- Churchward G., Bremer H., Young R. Transcription in bacteria at different DNA concentrations. J Bacteriol. 1982 May;150(2):572–581. doi: 10.1128/jb.150.2.572-581.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Clewell D. B. Nature of Col E 1 plasmid replication in Escherichia coli in the presence of the chloramphenicol. J Bacteriol. 1972 May;110(2):667–676. doi: 10.1128/jb.110.2.667-676.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Csordás-Tóth E., Boros I., Venetianer P. Structure of the promoter region for the rrnB gene in Escherichia coli. Nucleic Acids Res. 1979 Dec 20;7(8):2189–2197. doi: 10.1093/nar/7.8.2189. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gallant J. A. Stringent control in E. coli. Annu Rev Genet. 1979;13:393–415. doi: 10.1146/annurev.ge.13.120179.002141. [DOI] [PubMed] [Google Scholar]
- Gallant J., Palmer L., Pao C. C. Anomalous synthesis of ppGpp in growing cells. Cell. 1977 May;11(1):181–185. doi: 10.1016/0092-8674(77)90329-4. [DOI] [PubMed] [Google Scholar]
- 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]
- Glaser G., Cashel M. In vitro transcripts from the rrn B ribosomal RNA cistron originate from two tandem promoters. Cell. 1979 Jan;16(1):111–121. doi: 10.1016/0092-8674(79)90192-2. [DOI] [PubMed] [Google Scholar]
- Glaser G., Sarmientos P., Cashel M. Functional interrelationship between two tandem E. coli ribosomal RNA promoters. Nature. 1983 Mar 3;302(5903):74–76. doi: 10.1038/302074a0. [DOI] [PubMed] [Google Scholar]
- Gourse R. L., Stark M. J., Dahlberg A. E. Regions of DNA involved in the stringent control of plasmid-encoded rRNA in vivo. Cell. 1983 Apr;32(4):1347–1354. doi: 10.1016/0092-8674(83)90315-x. [DOI] [PubMed] [Google Scholar]
- Hansen M. T., Pato M. L., Molin S., Fill N. P., von Meyenburg K. Simple downshift and resulting lack of correlation between ppGpp pool size and ribonucleic acid accumulation. J Bacteriol. 1975 May;122(2):585–591. doi: 10.1128/jb.122.2.585-591.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ikemura T., Nomura M. Expression of spacer tRNA genes in ribosomal RNA transcription units carried by hybrid Col E1 plasmids in E. coli. Cell. 1977 Aug;11(4):779–793. doi: 10.1016/0092-8674(77)90291-4. [DOI] [PubMed] [Google Scholar]
- Koch A. L. The adaptive responses of Escherichia coli to a feast and famine existence. Adv Microb Physiol. 1971;6:147–217. doi: 10.1016/s0065-2911(08)60069-7. [DOI] [PubMed] [Google Scholar]
- Lazzarini R. A., Cashel M., Gallant J. On the regulation of guanosine tetraphosphate levels in stringent and relaxed strains of Escherichia coli. J Biol Chem. 1971 Jul 25;246(14):4381–4385. [PubMed] [Google Scholar]
- Miura A., Krueger J. H., Itoh S., de Boer H. A., Nomura M. Growth-rate-dependent regulation of ribosome synthesis in E. coli: expression of the lacZ and galK genes fused to ribosomal promoters. Cell. 1981 Sep;25(3):773–782. doi: 10.1016/0092-8674(81)90185-9. [DOI] [PubMed] [Google Scholar]
- Nierlich D. P. Regulation of bacterial growth, RNA, and protein synthesis. Annu Rev Microbiol. 1978;32:393–432. doi: 10.1146/annurev.mi.32.100178.002141. [DOI] [PubMed] [Google Scholar]
- Norris T. E., Koch A. L. Effect of growth rate on the relative rates of synthesis of messenger, ribosomal and transfer RNA in Escherichia coli. J Mol Biol. 1972 Mar 14;64(3):633–649. doi: 10.1016/0022-2836(72)90088-5. [DOI] [PubMed] [Google Scholar]
- Ota Y., Kikuchi A., Cashel M. Gene expression of an Escherichia coli ribosomal RNA promoter fused to structural genes of the galactose operon. Proc Natl Acad Sci U S A. 1979 Nov;76(11):5799–5803. doi: 10.1073/pnas.76.11.5799. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ryals J., Little R., Bremer H. Control of rRNA and tRNA syntheses in Escherichia coli by guanosine tetraphosphate. J Bacteriol. 1982 Sep;151(3):1261–1268. doi: 10.1128/jb.151.3.1261-1268.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sarmientos P., Sylvester J. E., Contente S., Cashel M. Differential stringent control of the tandem E. coli ribosomal RNA promoters from the rrnA operon expressed in vivo in multicopy plasmids. Cell. 1983 Apr;32(4):1337–1346. doi: 10.1016/0092-8674(83)90314-8. [DOI] [PubMed] [Google Scholar]
- Shen V., Bremer H. Chloramphenicol-induced changes in the synthesis of ribosomal, transfer, and messenger ribonucleic acids in Escherichia coli B/r. J Bacteriol. 1977 Jun;130(3):1098–1108. doi: 10.1128/jb.130.3.1098-1108.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shen W. F., Squires C., Squires C. L. Nucleotide sequence of the rrnG ribosomal RNA promoter region of Escherichia coli. Nucleic Acids Res. 1982 May 25;10(10):3303–3313. doi: 10.1093/nar/10.10.3303. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Stueber D., Bujard H. Transcription from efficient promoters can interfere with plasmid replication and diminish expression of plasmid specified genes. EMBO J. 1982;1(11):1399–1404. doi: 10.1002/j.1460-2075.1982.tb01329.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Young R. A., Steitz J. A. Tandem promoters direct E. coli ribosomal RNA synthesis. Cell. 1979 May;17(1):225–234. doi: 10.1016/0092-8674(79)90310-6. [DOI] [PubMed] [Google Scholar]
- de Boer H. A., Gilbert S. F., Nomura M. DNA sequences of promoter regions for rRNA operons rrnE and rrnA in E. coli. Cell. 1979 May;17(1):201–209. doi: 10.1016/0092-8674(79)90308-8. [DOI] [PubMed] [Google Scholar]