Home LiteratureArticle Details
PMID: 1396599 Published · ppublish English Comparative Study Journal Article Research Support, U.S. Gov't, P.H.S.

Comparison of the expression of the seven ribosomal RNA operons in Escherichia coli.

The EMBO journal ·Vol. 11 ·No. 11 ·1992-11-00 ·Pages 4175-85

Condon C, Philips J, Fu ZY, Squires C, Squires CL

Abstract

We have compared the expression of the seven ribosomal RNA operons (rrn) of Escherichia coli and their responses to a variety of physiological and genetic perturbations. We used a set of rrn promoter fusion constructs in their native chromosomal positions to examine effects of chromosomal location on rrn operon expression and the same set of fusions on lambda lysogens to assay intrinsic promoter strengths independent of chromosome context. In its native chromosomal location, expression of the rrnH operon was significantly lower than expected. This effect was not attributable to weak promoter activity and was dependent on the growth medium. The rrnE operon had reduced promoter activity relative to the other ribosomal operons in minimal medium and thus appears to have abnormal growth rate regulation. The ribosomal RNA operons showed varied responses to amino acid starvation; expression of rrnD was inhibited most. There was only a slight increase in rrn transcription in response to a temperature shift (30 degrees C to 42 degrees C) and the differences between individual operons was very small. The rrnG operon showed a significantly lower response than the other ribosomal RNA operons to a depletion of the rrn transcription activator, Fis, and thus appears to have decreased Fis-mediated transactivation. Finally, the chromosomal fusion strains were used to study the effect on growth rate of inactivating each rrn operon. In fast growth conditions, loss of certain rrn operons caused subtle decreases in growth rate on complex medium.

Related Genes
MeSH Terms
Base Sequence Chloramphenicol O-Acetyltransferase/genetics,metabolism Chromosomes, Bacterial/physiology Cloning, Molecular DNA, Bacterial/genetics DNA, Ribosomal/genetics Escherichia coli/genetics,growth & development Gene Expression Genotype Hot Temperature Kinetics Molecular Sequence Data Oligodeoxyribonucleotides Operon Plasmids Polymerase Chain Reaction Promoter Regions, Genetic RNA, Ribosomal/genetics Transcription, Genetic Transduction, Genetic
Chemicals
DNA, Bacterial DNA, Ribosomal Oligodeoxyribonucleotides RNA, Ribosomal Chloramphenicol O-Acetyltransferase
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Condon C
Department of Biological Sciences, Columbia University, New York, NY 10027.
Philips J
Fu Z Y
Squires C
Squires C L
References (51)
51 references, click to expand
  1. A bacteriophage lambda vector for cloning with BamHI and Sau3A.
    Gene. 1982 Dec;20(3):317-22 PMID: 6299896
  2. Mapping of rRNA genes with integrable plasmids in Bacillus subtilis.
    J Bacteriol. 1986 Jan;165(1):204-14 PMID: 3079748
  3. The genetics and regulation of heat-shock proteins.
    Annu Rev Genet. 1984;18:295-329 PMID: 6442118
  4. Repeated genes in eukaryotes.
    Annu Rev Biochem. 1980;49:727-64 PMID: 6996571
  5. Archaebacterial phylogeny: perspectives on the urkingdoms.
    Syst Appl Microbiol. 1986;7:161-77 PMID: 11542063
  6. Translational coupling of the trpB and trpA genes in the Escherichia coli tryptophan operon.
    J Bacteriol. 1984 Feb;157(2):363-7 PMID: 6319355
  7. Evidence for antitermination in Escherichia coli RRNA transcription.
    J Bacteriol. 1984 Jul;159(1):260-4 PMID: 6330033
  8. Gene organization and primary structure of a ribosomal RNA operon from Escherichia coli.
    J Mol Biol. 1981 May 15;148(2):107-27 PMID: 7028991
  9. Tandem promoters direct E. coli ribosomal RNA synthesis.
    Cell. 1979 May;17(1):225-34 PMID: 110460
  10. A rapid alkaline extraction procedure for screening recombinant plasmid DNA.
    Nucleic Acids Res. 1979 Nov 24;7(6):1513-23 PMID: 388356
  11. A colony bank containing synthetic Col El hybrid plasmids representative of the entire E. coli genome.
    Cell. 1976 Sep;9(1):91-9 PMID: 788919
  12. The peculiar nature of codon usage in primates.
    Genet Eng (N Y). 1991;13:73-113 PMID: 1370052
  13. ClpB is the Escherichia coli heat shock protein F84.1.
    J Bacteriol. 1991 Jul;173(14):4254-62 PMID: 2066329
  14. E.coli Fis protein activates ribosomal RNA transcription in vitro and in vivo.
    EMBO J. 1990 Nov;9(11):3733-42 PMID: 2209559
  15. 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 PMID: 2416474
  16. Mutational analysis of a prokaryotic recombinational enhancer element with two functions.
    EMBO J. 1989 Feb;8(2):577-85 PMID: 2656257
  17. Instability of rRNA operons in Bacillus subtilis.
    J Bacteriol. 1988 Feb;170(2):605-10 PMID: 2828315
  18. Characterization of the ribosomal RNA gene clusters in Halobacterium cutirubrum.
    J Biol Chem. 1985 Jan 25;260(2):899-906 PMID: 2981849
  19. The physical map of the whole E. coli chromosome: application of a new strategy for rapid analysis and sorting of a large genomic library.
    Cell. 1987 Jul 31;50(3):495-508 PMID: 3038334
  20. 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):1235-8 PMID: 3277949
  21. Sequence distributions associated with DNA curvature are found upstream of strong E. coli promoters.
    Nucleic Acids Res. 1987 Jan 26;15(2):785-96 PMID: 3547329
  22. Antitermination by both the promoter and the leader regions of an Escherichia coli ribosomal RNA operon.
    Proc Natl Acad Sci U S A. 1985 Aug;82(15):5073-7 PMID: 3895228
  23. Regulation of phospholipid synthesis in Escherichia coli by guanosine tetraphosphate.
    J Bacteriol. 1973 Oct;116(1):355-66 PMID: 4583220
  24. Chromosomal locations of the genes for rRNA in Escherichia coli K-12.
    J Bacteriol. 1982 Feb;149(2):458-68 PMID: 6173374
  25. Regulation of the synthesis of ribosomes and ribosomal components.
    Annu Rev Biochem. 1984;53:75-117 PMID: 6206783
  26. Inversions between ribosomal RNA genes of Escherichia coli.
    Proc Natl Acad Sci U S A. 1981 Nov;78(11):7069-72 PMID: 6273909
  27. Physical map of the seven ribosomal RNA genes of Escherichia coli.
    Nucleic Acids Res. 1979;6(5):1817-30 PMID: 377232
  28. DNA sequences of promoter regions for rRNA operons rrnE and rrnA in E. coli.
    Cell. 1979 May;17(1):201-9 PMID: 378405
  29. 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 PMID: 389624
  30. Chloramphenicol acetyltransferase from chloramphenicol-resistant bacteria.
    Methods Enzymol. 1975;43:737-55 PMID: 1094240
  31. Structural analysis of the Escherichia coli K-12 hisT operon by using a kanamycin resistance cassette.
    J Bacteriol. 1987 Mar;169(3):1061-70 PMID: 3029016
  32. Hin-mediated site-specific recombination requires two 26 bp recombination sites and a 60 bp recombinational enhancer.
    Cell. 1985 Jul;41(3):781-91 PMID: 2988787
  33. Purification and properties of the Escherichia coli host factor required for inversion of the G segment in bacteriophage Mu.
    J Biol Chem. 1986 Nov 25;261(33):15673-8 PMID: 3536909
  34. Structurally distinct, stage-specific ribosomes occur in Plasmodium.
    Science. 1987 Nov 13;238(4829):933-7 PMID: 3672135
  35. Transcriptional control of the S10 ribosomal protein operon of Escherichia coli after a shift to higher temperature.
    J Bacteriol. 1985 Jul;163(1):140-7 PMID: 3891722
  36. Nonchromosomal antibiotic resistance in bacteria: genetic transformation of Escherichia coli by R-factor DNA.
    Proc Natl Acad Sci U S A. 1972 Aug;69(8):2110-4 PMID: 4559594
  37. Antitermination of E. coli rRNA transcription is caused by a control region segment containing lambda nut-like sequences.
    Cell. 1984 Oct;38(3):851-60 PMID: 6091902
  38. Deletion of a ribosomal ribonucleic acid operon in Escherichia coli.
    J Bacteriol. 1980 Aug;143(2):1077-80 PMID: 6162835
  39. 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):1337-46 PMID: 6188537
  40. Positive selection for loss of tetracycline resistance.
    J Bacteriol. 1980 Aug;143(2):926-33 PMID: 6259126
  41. Nucleotide sequence of the rrnG ribosomal RNA promoter region of Escherichia coli.
    Nucleic Acids Res. 1982 May 25;10(10):3303-13 PMID: 6285294
  42. Detection of specific sequences among DNA fragments separated by gel electrophoresis.
    J Mol Biol. 1975 Nov 5;98(3):503-17 PMID: 1195397
  43. Factor-independent activation of Escherichia coli rRNA transcription. I. Kinetic analysis of the roles of the upstream activator region and supercoiling on transcription of the rrnB P1 promoter in vitro.
    J Mol Biol. 1991 Aug 5;220(3):555-68 PMID: 1870123
  44. Sequences upstream of the-35 hexamer of rrnB P1 affect promoter strength and upstream activation.
    Biochim Biophys Acta. 1990 Aug 27;1050(1-3):307-11 PMID: 2119814
  45. Potential binding sites of the trans-activator FIS are present upstream of all rRNA operons and of many but not all tRNA operons.
    Biochim Biophys Acta. 1990 Aug 27;1050(1-3):302-6 PMID: 2207159
  46. Nucleotide sequence between the fadB gene and the rrnA operon from Escherichia coli.
    Nucleic Acids Res. 1990 Nov 11;18(21):6439 PMID: 2243799
  47. A simple method for the preparation of plasmid and chromosomal E. coli DNA.
    Nucleic Acids Res. 1989 Nov 11;17(21):8893 PMID: 2587246
  48. Effect of variation of charged and uncharged tRNA(Trp) levels on ppGpp synthesis in Escherichia coli.
    J Bacteriol. 1989 Dec;171(12):6493-502 PMID: 2687238
  49. Nucleotide sequence analysis of genes purH and purD involved in the de novo purine nucleotide biosynthesis of Escherichia coli.
    J Biol Chem. 1989 Dec 15;264(35):21239-46 PMID: 2687276
  50. Isolation of the gene encoding the Hin recombinational enhancer binding protein.
    Proc Natl Acad Sci U S A. 1988 May;85(10):3484-8 PMID: 2835774
  51. Plasmid vectors for the selection of promoters.
    Gene. 1984 Feb;27(2):151-60 PMID: 6327464
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
1992-11-00
Pages
4175-85
Language
English
Region
England
NLM ID
8208664
PMCID
PMC556928
Subset
IM
Grants
NIGMS NIH HHS · GM24751 · United States
Databases
GENBANK
X66364, X66365, X67217, X67682, X67872, X67873, Z14319, Z14320, Z14954, Z14955
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com