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. 1995 Jul;177(14):4152–4156. doi: 10.1128/jb.177.14.4152-4156.1995

rRNA operon multiplicity in Escherichia coli and the physiological implications of rrn inactivation.

C Condon 1, D Liveris 1, C Squires 1, I Schwartz 1, C L Squires 1
PMCID: PMC177152  PMID: 7608093

Abstract

Here we present evidence that only five of the seven rRNA operons present in Escherichia coli are necessary to support near-optimal growth on complex media. Seven rrn operons are necessary, however, for rapid adaptation to nutrient and temperature changes, suggesting it is the ability to adapt quickly to changing environmental conditions that has provided the selective pressure for the persistence of seven rrn operons in E. coli. We have also found that one consequence of rrn operon inactivation is a miscoordination of the concentrations of initiation factor IF3 and ribosomes.

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Selected References

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  1. Beresford T., Condon S. Cloning and partial characterization of genes for ribosomal ribonucleic acid in Lactococcus lactis subsp. lactis. FEMS Microbiol Lett. 1991 Mar 1;62(2-3):319–323. doi: 10.1016/0378-1097(91)90178-d. [DOI] [PubMed] [Google Scholar]
  2. Boros I., Kiss A., Venetianer P. Physical map of the seven ribosomal RNA genes of Escherichia coli. Nucleic Acids Res. 1979;6(5):1817–1830. doi: 10.1093/nar/6.5.1817. [DOI] [PMC free article] [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. Brosius J., Dull T. J., Sleeter D. D., Noller H. F. Gene organization and primary structure of a ribosomal RNA operon from Escherichia coli. J Mol Biol. 1981 May 15;148(2):107–127. doi: 10.1016/0022-2836(81)90508-8. [DOI] [PubMed] [Google Scholar]
  5. Carbon P., Ehresmann C., Ehresmann B., Ebel J. P. The complete nucleotide sequence of the ribosomal 16-S RNA from Excherichia coli. Experimental details and cistron heterogeneities. Eur J Biochem. 1979 Oct 15;100(2):399–410. doi: 10.1111/j.1432-1033.1979.tb04183.x. [DOI] [PubMed] [Google Scholar]
  6. Condon C., French S., Squires C., Squires C. L. Depletion of functional ribosomal RNA operons in Escherichia coli causes increased expression of the remaining intact copies. EMBO J. 1993 Nov;12(11):4305–4315. doi: 10.1002/j.1460-2075.1993.tb06115.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Condon C., Philips J., Fu Z. Y., Squires C., Squires C. L. Comparison of the expression of the seven ribosomal RNA operons in Escherichia coli. EMBO J. 1992 Nov;11(11):4175–4185. doi: 10.1002/j.1460-2075.1992.tb05511.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Dennis P. P., Bremer H. Macromolecular composition during steady-state growth of Escherichia coli B-r. J Bacteriol. 1974 Jul;119(1):270–281. doi: 10.1128/jb.119.1.270-281.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Ellwood M., Nomura M. Chromosomal locations of the genes for rRNA in Escherichia coli K-12. J Bacteriol. 1982 Feb;149(2):458–468. doi: 10.1128/jb.149.2.458-468.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Ellwood M., Nomura M. Deletion of a ribosomal ribonucleic acid operon in Escherichia coli. J Bacteriol. 1980 Aug;143(2):1077–1080. doi: 10.1128/jb.143.2.1077-1080.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. French S. Consequences of replication fork movement through transcription units in vivo. Science. 1992 Nov 20;258(5086):1362–1365. doi: 10.1126/science.1455232. [DOI] [PubMed] [Google Scholar]
  12. Garnier T., Canard B., Cole S. T. Cloning, mapping, and molecular characterization of the rRNA operons of Clostridium perfringens. J Bacteriol. 1991 Sep;173(17):5431–5438. doi: 10.1128/jb.173.17.5431-5438.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Gold L., Stormo G., Saunders R. Escherichia coli translational initiation factor IF3: a unique case of translational regulation. Proc Natl Acad Sci U S A. 1984 Nov;81(22):7061–7065. doi: 10.1073/pnas.81.22.7061. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Gourse R. L., de Boer H. A., Nomura M. DNA determinants of rRNA synthesis in E. coli: growth rate dependent regulation, feedback inhibition, upstream activation, antitermination. Cell. 1986 Jan 17;44(1):197–205. doi: 10.1016/0092-8674(86)90498-8. [DOI] [PubMed] [Google Scholar]
  15. Gunderson J. H., Sogin M. L., Wollett G., Hollingdale M., de la Cruz V. F., Waters A. P., McCutchan T. F. Structurally distinct, stage-specific ribosomes occur in Plasmodium. Science. 1987 Nov 13;238(4829):933–937. doi: 10.1126/science.3672135. [DOI] [PubMed] [Google Scholar]
  16. Harvey S., Hill C. W., Squires C., Squires C. L. Loss of the spacer loop sequence from the rrnB operon in the Escherichia coli K-12 subline that bears the relA1 mutation. J Bacteriol. 1988 Mar;170(3):1235–1238. doi: 10.1128/jb.170.3.1235-1238.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Howe J. G., Hershey J. W. Initiation factor and ribosome levels are coordinately controlled in Escherichia coli growing at different rates. J Biol Chem. 1983 Feb 10;258(3):1954–1959. [PubMed] [Google Scholar]
  18. Hui I., Dennis P. P. Characterization of the ribosomal RNA gene clusters in Halobacterium cutirubrum. J Biol Chem. 1985 Jan 25;260(2):899–906. [PubMed] [Google Scholar]
  19. Kiss A., Sain B., Venetianer P. The number of rRNA genes in Escherichia coli. FEBS Lett. 1977 Jul 1;79(1):77–79. doi: 10.1016/0014-5793(77)80354-2. [DOI] [PubMed] [Google Scholar]
  20. LaFauci G., Widom R. L., Eisner R. L., Jarvis E. D., Rudner R. Mapping of rRNA genes with integrable plasmids in Bacillus subtilis. J Bacteriol. 1986 Jan;165(1):204–214. doi: 10.1128/jb.165.1.204-214.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Lewicki B. T., Margus T., Remme J., Nierhaus K. H. Coupling of rRNA transcription and ribosomal assembly in vivo. Formation of active ribosomal subunits in Escherichia coli requires transcription of rRNA genes by host RNA polymerase which cannot be replaced by bacteriophage T7 RNA polymerase. J Mol Biol. 1993 Jun 5;231(3):581–593. doi: 10.1006/jmbi.1993.1311. [DOI] [PubMed] [Google Scholar]
  22. Newlands J. T., Gaal T., Mecsas J., Gourse R. L. Transcription of the Escherichia coli rrnB P1 promoter by the heat shock RNA polymerase (E sigma 32) in vitro. J Bacteriol. 1993 Feb;175(3):661–668. doi: 10.1128/jb.175.3.661-668.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Nomura M., Morgan E. A. Genetics of bacterial ribosomes. Annu Rev Genet. 1977;11:297–347. doi: 10.1146/annurev.ge.11.120177.001501. [DOI] [PubMed] [Google Scholar]
  24. Plaskon R. R., Wartell R. M. Sequence distributions associated with DNA curvature are found upstream of strong E. coli promoters. Nucleic Acids Res. 1987 Jan 26;15(2):785–796. doi: 10.1093/nar/15.2.785. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Sarmientos P., Cashel M. Carbon starvation and growth rate-dependent regulation of the Escherichia coli ribosomal RNA promoters: differential control of dual promoters. Proc Natl Acad Sci U S A. 1983 Nov;80(22):7010–7013. doi: 10.1073/pnas.80.22.7010. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Sawada M., Osawa S., Kobayashi H., Hori H., Muto A. The number of ribosomal RNA genes in Mycoplasma capricolum. Mol Gen Genet. 1981;182(3):502–504. doi: 10.1007/BF00293942. [DOI] [PubMed] [Google Scholar]
  27. 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]
  28. Tulloch D. L., Finch L. R., Hillier A. J., Davidson B. E. Physical map of the chromosome of Lactococcus lactis subsp. lactis DL11 and localization of six putative rRNA operons. J Bacteriol. 1991 May;173(9):2768–2775. doi: 10.1128/jb.173.9.2768-2775.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Vogel U., Jensen K. F. The RNA chain elongation rate in Escherichia coli depends on the growth rate. J Bacteriol. 1994 May;176(10):2807–2813. doi: 10.1128/jb.176.10.2807-2813.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Widom R. L., Jarvis E. D., LaFauci G., Rudner R. Instability of rRNA operons in Bacillus subtilis. J Bacteriol. 1988 Feb;170(2):605–610. doi: 10.1128/jb.170.2.605-610.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]

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