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. 1980 Sep;143(3):1332–1344. doi: 10.1128/jb.143.3.1332-1344.1980

Synthesis and function of ribonucleic acid polymerase and ribosomes in Escherichia coli B/r after a nutritional shift-up.

N Shepherd, G Churchward, H Bremer
PMCID: PMC294508  PMID: 6157673

Abstract

The syntheses of stable ribosomal ribonucleic acid (RNA) and transfer RNA in bacteria depend on the concentration and activity of RNA polymerase and on the fraction of active RNA polymerase synthesizing stable RNA. These parameters were measured in Escherichia coli B/r after a nutritional shift-up from succinate-minimal to glucose-amino acids medium and were found to change in complex patterns during a 1- to 2-h period after the shift-up before reaching a final steady-state level characteristic for the postshift growth medium. The combined effect of these changes was an immediate, one-step increase in the exponential rate of stable RNA synthesis and thus of ribosome synthesis. This suggests that the distribution of transcribing RNA polymerase over ribosomal and nonribosomal genes and the polymerase activity are continuously adjusted during postshift growth to some growth-limiting reaction whose rate increases exponentially. It is proposed that this reaction is the production of amino-acylated transfer RNA and that is exponentially increasing rate results in part from a gradually increasing concentration of aminoacyl transfer RNA synthetases after a shift-up. This idea was tested and is supported by a computer simulation of a nutritional shift-up.

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Selected References

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

  1. Bachmann B. J., Low K. B., Taylor A. L. Recalibrated linkage map of Escherichia coli K-12. Bacteriol Rev. 1976 Mar;40(1):116–167. doi: 10.1128/br.40.1.116-167.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bremer H., Churchward G., Young R. Relation between growth and replication in bacteria. J Theor Biol. 1979 Dec 7;81(3):533–545. doi: 10.1016/0022-5193(79)90051-1. [DOI] [PubMed] [Google Scholar]
  3. Bremer H. Parameters affecting the rate of synthesis of ribosomes and RNA polymerase in bacteria. J Theor Biol. 1975 Sep;53(1):115–124. doi: 10.1016/0022-5193(75)90106-x. [DOI] [PubMed] [Google Scholar]
  4. Bremer H., Yuan D. RNA chain growth-rate in Escherichia coli. J Mol Biol. 1968 Dec 14;38(2):163–180. doi: 10.1016/0022-2836(68)90404-x. [DOI] [PubMed] [Google Scholar]
  5. Brunschede H., Dove T. L., Bremer H. Establishment of exponential growth after a nutritional shift-up in Escherichia coli B/r: accumulation of deoxyribonucleic acid, ribonucleic acid, and protein. J Bacteriol. 1977 Feb;129(2):1020–1033. doi: 10.1128/jb.129.2.1020-1033.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cashel M. The control of ribonucleic acid synthesis in Escherichia coli. IV. Relevance of unusual phosphorylated compounds from amino acid-starved stringent strains. J Biol Chem. 1969 Jun 25;244(12):3133–3141. [PubMed] [Google Scholar]
  7. Dalbow D. G., Bremer H. Metabolic regulation of beta-galactosidase synthesis in Escherichia coli. A test for constitutive ribosome synthesis. Biochem J. 1975 Jul;150(1):1–8. doi: 10.1042/bj1500001b. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. 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]
  9. Dennis P. P., Bremer H. Regulation of ribonucleic acid synthesis in Escherichia coli B-r: an analysis of a shift-up. 1. Ribosomal RNA chain growth rates. J Mol Biol. 1973 Mar 25;75(1):145–159. doi: 10.1016/0022-2836(73)90535-4. [DOI] [PubMed] [Google Scholar]
  10. Dennis P. P. Regulation of ribosomal and transfer ribonucleic acid synthesis in Escherichia coli B-r. J Biol Chem. 1972 May 10;247(9):2842–2845. [PubMed] [Google Scholar]
  11. 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]
  12. Dennis P. P. Transcription patterns of adjacent segments on the chromosome of Escherichia coli containing genes coding for four 50S ribosomal proteins and the beta and beta' subunits of RNA polymerase. J Mol Biol. 1977 Oct 5;115(4):603–625. doi: 10.1016/0022-2836(77)90105-x. [DOI] [PubMed] [Google Scholar]
  13. Donachie W. D. Relationship between cell size and time of initiation of DNA replication. Nature. 1968 Sep 7;219(5158):1077–1079. doi: 10.1038/2191077a0. [DOI] [PubMed] [Google Scholar]
  14. Fiil N. P., von Meyenburg K., Friesen J. D. Accumulation and turnover of guanosine tetraphosphate in Escherichia coli. J Mol Biol. 1972 Nov 28;71(3):769–783. doi: 10.1016/s0022-2836(72)80037-8. [DOI] [PubMed] [Google Scholar]
  15. Fukuda R., Taketo M., Ishihama A. Autogenous regulation of RNA polymerase beta subunit synthesis in vitro. J Biol Chem. 1978 Jul 10;253(13):4501–4504. [PubMed] [Google Scholar]
  16. Haseltine W. A., Block R., Gilbert W., Weber K. MSI and MSII made on ribosome in idling step of protein synthesis. Nature. 1972 Aug 18;238(5364):381–384. doi: 10.1038/238381a0. [DOI] [PubMed] [Google Scholar]
  17. Haseltine W. A., Block R. Synthesis of guanosine tetra- and pentaphosphate requires the presence of a codon-specific, uncharged transfer ribonucleic acid in the acceptor site of ribosomes. Proc Natl Acad Sci U S A. 1973 May;70(5):1564–1568. doi: 10.1073/pnas.70.5.1564. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Iwakura Y., Ishihama A. Biosynthesis of RNA polymerase in Escherichia coli. II. control of RNA polymerase synthesis during nutritional shift up and down. Mol Gen Genet. 1975 Dec 23;142(1):67–84. [PubMed] [Google Scholar]
  19. Iwakura Y., Ito K., Ishihama A. Biosynthesis of RNA polymerase in Escherichia coli. I. Control of RNA polymerase content at various growth rates. Mol Gen Genet. 1974;133(1):1–23. doi: 10.1007/BF00268673. [DOI] [PubMed] [Google Scholar]
  20. Jørgensen P., Collins J., Fiil N., von Meyenbourg K. A ribosomal RNA gene, rrnC, of Escherichia coli, mapped by specialized transducing lambdadilv and lambda drbs phages. Mol Gen Genet. 1978 Jul 11;163(2):223–228. doi: 10.1007/BF00267413. [DOI] [PubMed] [Google Scholar]
  21. Kenerley M. E., Morgan E. A., Post L., Lindahl L., Nomura M. Characterization of hybrid plasmids carrying individual ribosomal ribonucleic acid transcription units of Escherichia coli. J Bacteriol. 1977 Dec;132(3):931–949. doi: 10.1128/jb.132.3.931-949.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Lindahl L., Post L., Nomura M. DNA-dependent in vitro synthesis of fibosomal proteins, protein elongation factors, and RNA polymerase subunit alpha: inhibition by ppGpp. Cell. 1976 Nov;9(3):439–448. doi: 10.1016/0092-8674(76)90089-1. [DOI] [PubMed] [Google Scholar]
  23. Linn T., Scaife J. Identification of a single promoter in E. coli for rplJ, rplL and rpoBC. Nature. 1978 Nov 2;276(5683):33–37. doi: 10.1038/276033a0. [DOI] [PubMed] [Google Scholar]
  24. Maher D. L., Dennis P. P. In vivo transcription of E. coli genes coding for rRNA, ribosomal proteins and subunits of RNA polymerase: influence of the stringent control system. Mol Gen Genet. 1977 Oct 20;155(2):203–211. doi: 10.1007/BF00393161. [DOI] [PubMed] [Google Scholar]
  25. Matzura H., Hansen B. S., Zeuthen J. Biosynthesis of the beta and beta' subunits of RNA polymerase in Escherichia coli. J Mol Biol. 1973 Feb 15;74(1):9–20. doi: 10.1016/0022-2836(73)90350-1. [DOI] [PubMed] [Google Scholar]
  26. Neidhardt F. C., Bloch P. L., Pedersen S., Reeh S. Chemical measurement of steady-state levels of ten aminoacyl-transfer ribonucleic acid synthetases in Escherichia coli. J Bacteriol. 1977 Jan;129(1):378–387. doi: 10.1128/jb.129.1.378-387.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Neihardt F. C., Parker J., McKeever W. G. Function and regulation of aminoacyl-tRNA synthetases in prokaryotic and eukaryotic cells. Annu Rev Microbiol. 1975;29:215–250. doi: 10.1146/annurev.mi.29.100175.001243. [DOI] [PubMed] [Google Scholar]
  28. Newman A. J., Linn T. G., Hayward R. S. Evidence for co-transcription of the RNA polymerase genes rpoBC with a ribosomal protein gene of escherichia coli. Mol Gen Genet. 1979 Jan 31;169(2):195–204. doi: 10.1007/BF00271671. [DOI] [PubMed] [Google Scholar]
  29. 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]
  30. Pritchard R. H., Zaritsky A. Effect of thymine concentration on the replication velocity of DNA in a thymineless mutant of Escherichia coli. Nature. 1970 Apr 11;226(5241):126–131. doi: 10.1038/226126a0. [DOI] [PubMed] [Google Scholar]
  31. Reeh S., Pedersen S., Friesen J. D. Biosynthetic regulation of individual proteins in relA+ and relA strains of Escherichia coli during amino acid starvation. Mol Gen Genet. 1976 Dec 22;149(3):279–289. doi: 10.1007/BF00268529. [DOI] [PubMed] [Google Scholar]
  32. Reeh S., Pedersen S., Neidhardt F. C. Transient rates of synthesis of five amionacyl-transfer ribonucleic acid synthetases during a shift-up of Escherichia coli. J Bacteriol. 1977 Feb;129(2):702–706. doi: 10.1128/jb.129.2.702-706.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Rose J. K., Mosteller R. D., Yanofsky C. Tryptophan messenger ribonucleic acid elongation rates and steady-state levels of tryptophan operon enzymes under various growth conditions. J Mol Biol. 1970 Aug;51(3):541–550. doi: 10.1016/0022-2836(70)90007-0. [DOI] [PubMed] [Google Scholar]
  34. SPAHR P. F. Amino acid composition of ribosomes from Escherichia coli. J Mol Biol. 1962 May;4:395–406. doi: 10.1016/s0022-2836(62)80020-5. [DOI] [PubMed] [Google Scholar]
  35. 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]
  36. Shepherd N. S., Churchward G., Bremer H. Synthesis and activity of ribonucleic acid polymerase in Escherichia coli. J Bacteriol. 1980 Mar;141(3):1098–1108. doi: 10.1128/jb.141.3.1098-1108.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Travers A., Buckland R. Heterogeneity of E. coli RNA polymerase. Nat New Biol. 1973 Jun 27;243(130):257–260. doi: 10.1038/newbio243257a0. [DOI] [PubMed] [Google Scholar]
  38. Yamamoto M., Nomura M. Contranscription of genes for RNA polymerase subunits beta and beta' with genes for ribosomal proteins in Escherichia coli. Proc Natl Acad Sci U S A. 1978 Aug;75(8):3891–3895. doi: 10.1073/pnas.75.8.3891. [DOI] [PMC free article] [PubMed] [Google Scholar]

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