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. 1990 Nov 25;18(22):6503–6508. doi: 10.1093/nar/18.22.6503

A novel repeated DNA sequence located in the intergenic regions of bacterial chromosomes.

G J Sharples 1, R G Lloyd 1
PMCID: PMC332602  PMID: 2251112

Abstract

We report the discovery of a novel group of highly conserved DNA sequences located within the intergenic regions of the chromosomes of Escherichia coli, Salmonella typhimurium and other bacteria. These intergenic repeat units (IRUs) are 124-127 nucleotides long and have the potential to form stable stem-loop structures. The location of these sequences within the intergenic regions is variable with respect to known or putative signals for transcription and translation of the flanking genes. Some of the IRU sequences are transcribed, others are probably not. The structure and possible functions of these sequences are discussed in relation to palindromic units and other repeated DNA sequences in bacteria.

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Selected References

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

  1. Alefounder P. R., Perham R. N. Identification, molecular cloning and sequence analysis of a gene cluster encoding the class II fructose 1,6-bisphosphate aldolase, 3-phosphoglycerate kinase and a putative second glyceraldehyde 3-phosphate dehydrogenase of Escherichia coli. Mol Microbiol. 1989 Jun;3(6):723–732. doi: 10.1111/j.1365-2958.1989.tb00221.x. [DOI] [PubMed] [Google Scholar]
  2. Alm R. A., Stroeher U. H., Manning P. A. Extracellular proteins of Vibrio cholerae: nucleotide sequence of the structural gene (hlyA) for the haemolysin of the haemolytic El Tor strain 017 and characterization of the hlyA mutation in the non-haemolytic classical strain 569B. Mol Microbiol. 1988 Jul;2(4):481–488. doi: 10.1111/j.1365-2958.1988.tb00054.x. [DOI] [PubMed] [Google Scholar]
  3. An G., Bendiak D. S., Mamelak L. A., Friesen J. D. Organization and nucleotide sequence of a new ribosomal operon in Escherichia coli containing the genes for ribosomal protein S2 and elongation factor Ts. Nucleic Acids Res. 1981 Aug 25;9(16):4163–4172. doi: 10.1093/nar/9.16.4163. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Arndt E., Weigel C. Nucleotide sequence of the genes encoding the L11, L1, L10 and L12 equivalent ribosomal proteins from the archaebacterium Halobacterium marismortui. Nucleic Acids Res. 1990 Mar 11;18(5):1285–1285. doi: 10.1093/nar/18.5.1285. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Burton Z. F., Gross C. A., Watanabe K. K., Burgess R. R. The operon that encodes the sigma subunit of RNA polymerase also encodes ribosomal protein S21 and DNA primase in E. coli K12. Cell. 1983 Feb;32(2):335–349. doi: 10.1016/0092-8674(83)90453-1. [DOI] [PubMed] [Google Scholar]
  6. Christensen T., Johnsen M., Fiil N. P., Friesen J. D. RNA secondary structure and translation inhibition: analysis of mutants in the rplJ leader. EMBO J. 1984 Jul;3(7):1609–1612. doi: 10.1002/j.1460-2075.1984.tb02018.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Clément J. M., Hofnung M. Gene sequence of the lambda receptor, an outer membrane protein of E. coli K12. Cell. 1981 Dec;27(3 Pt 2):507–514. doi: 10.1016/0092-8674(81)90392-5. [DOI] [PubMed] [Google Scholar]
  8. Erickson B. D., Burton Z. F., Watanabe K. K., Burgess R. R. Nucleotide sequence of the rpsU-dnaG-rpoD operon from Salmonella typhimurium and a comparison of this sequence with the homologous operon of Escherichia coli. Gene. 1985;40(1):67–78. doi: 10.1016/0378-1119(85)90025-3. [DOI] [PubMed] [Google Scholar]
  9. Gilson E., Clément J. M., Brutlag D., Hofnung M. A family of dispersed repetitive extragenic palindromic DNA sequences in E. coli. EMBO J. 1984 Jun;3(6):1417–1421. doi: 10.1002/j.1460-2075.1984.tb01986.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Gilson E., Perrin D., Clement J. M., Szmelcman S., Dassa E., Hofnung M. Palindromic units from E. coli as binding sites for a chromoid-associated protein. FEBS Lett. 1986 Oct 6;206(2):323–328. doi: 10.1016/0014-5793(86)81005-5. [DOI] [PubMed] [Google Scholar]
  11. Gilson E., Perrin D., Hofnung M. DNA polymerase I and a protein complex bind specifically to E. coli palindromic unit highly repetitive DNA: implications for bacterial chromosome organization. Nucleic Acids Res. 1990 Jul 11;18(13):3941–3952. doi: 10.1093/nar/18.13.3941. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hanau R., Koduri R. K., Ho N., Brenchley J. E. Nucleotide sequence of the control regions for the glnA and glnL genes of Salmonella typhimurium. J Bacteriol. 1983 Jul;155(1):82–89. doi: 10.1128/jb.155.1.82-89.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Higgins C. F., Ames G. F., Barnes W. M., Clement J. M., Hofnung M. A novel intercistronic regulatory element of prokaryotic operons. Nature. 1982 Aug 19;298(5876):760–762. doi: 10.1038/298760a0. [DOI] [PubMed] [Google Scholar]
  14. Higgins C. F., McLaren R. S., Newbury S. F. Repetitive extragenic palindromic sequences, mRNA stability and gene expression: evolution by gene conversion? A review. Gene. 1988 Dec 10;72(1-2):3–14. doi: 10.1016/0378-1119(88)90122-9. [DOI] [PubMed] [Google Scholar]
  15. Isberg R. R., Voorhis D. L., Falkow S. Identification of invasin: a protein that allows enteric bacteria to penetrate cultured mammalian cells. Cell. 1987 Aug 28;50(5):769–778. doi: 10.1016/0092-8674(87)90335-7. [DOI] [PubMed] [Google Scholar]
  16. Komine Y., Adachi T., Inokuchi H., Ozeki H. Genomic organization and physical mapping of the transfer RNA genes in Escherichia coli K12. J Mol Biol. 1990 Apr 20;212(4):579–598. doi: 10.1016/0022-2836(90)90224-A. [DOI] [PubMed] [Google Scholar]
  17. Kröger M., Wahl R., Rice P. Compilation of DNA sequences of Escherichia coli (update 1990). Nucleic Acids Res. 1990 Apr 25;18 (Suppl):2549–2587. doi: 10.1093/nar/18.suppl.2549. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Li S. F., DeMoss J. A. Promoter region of the nar operon of Escherichia coli: nucleotide sequence and transcription initiation signals. J Bacteriol. 1987 Oct;169(10):4614–4620. doi: 10.1128/jb.169.10.4614-4620.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Loenen W. A., Daniel A. S., Braymer H. D., Murray N. E. Organization and sequence of the hsd genes of Escherichia coli K-12. J Mol Biol. 1987 Nov 20;198(2):159–170. doi: 10.1016/0022-2836(87)90303-2. [DOI] [PubMed] [Google Scholar]
  20. MacFarlane S. A., Merrick M. The nucleotide sequence of the nitrogen regulation gene ntrB and the glnA-ntrBC intergenic region of Klebsiella pneumoniae. Nucleic Acids Res. 1985 Nov 11;13(21):7591–7606. doi: 10.1093/nar/13.21.7591. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Manulis S., Kobayashi D. Y., Keen N. T. Molecular cloning and sequencing of a pectate lyase gene from Yersinia pseudotuberculosis. J Bacteriol. 1988 Apr;170(4):1825–1830. doi: 10.1128/jb.170.4.1825-1830.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Maxon M. E., Redfield B., Cai X. Y., Shoeman R., Fujita K., Fisher W., Stauffer G., Weissbach H., Brot N. Regulation of methionine synthesis in Escherichia coli: effect of the MetR protein on the expression of the metE and metR genes. Proc Natl Acad Sci U S A. 1989 Jan;86(1):85–89. doi: 10.1073/pnas.86.1.85. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. McConnell D. J. Control sites in the sequence at the beginning of T7 gene 1. Nucleic Acids Res. 1979 Aug 10;6(11):3491–3503. doi: 10.1093/nar/6.11.3491. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Merino E., Becerril B., Valle F., Bolivar F. Deletion of a repetitive extragenic palindromic (REP) sequence downstream from the structural gene of Escherichia coli glutamate dehydrogenase affects the stability of its mRNA. Gene. 1987;58(2-3):305–309. doi: 10.1016/0378-1119(87)90386-6. [DOI] [PubMed] [Google Scholar]
  25. Miranda-Ríos J., Sánchez-Pescador R., Urdea M., Covarrubias A. A. The complete nucleotide sequence of the glnALG operon of Escherichia coli K12. Nucleic Acids Res. 1987 Mar 25;15(6):2757–2770. doi: 10.1093/nar/15.6.2757. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Newbury S. F., Smith N. H., Higgins C. F. Differential mRNA stability controls relative gene expression within a polycistronic operon. Cell. 1987 Dec 24;51(6):1131–1143. doi: 10.1016/0092-8674(87)90599-x. [DOI] [PubMed] [Google Scholar]
  27. Newbury S. F., Smith N. H., Robinson E. C., Hiles I. D., Higgins C. F. Stabilization of translationally active mRNA by prokaryotic REP sequences. Cell. 1987 Jan 30;48(2):297–310. doi: 10.1016/0092-8674(87)90433-8. [DOI] [PubMed] [Google Scholar]
  28. Nonet M. L., Marvel C. C., Tolan D. R. The hisT-purF region of the Escherichia coli K-12 chromosome. Identification of additional genes of the hisT and purF operons. J Biol Chem. 1987 Sep 5;262(25):12209–12217. [PubMed] [Google Scholar]
  29. Nussinov R., Tinoco I., Jr, Jacobson A. B. Small changes in free energy assignments for unpaired bases do not affect predicted secondary structures in single stranded RNA. Nucleic Acids Res. 1982 Jan 11;10(1):341–349. doi: 10.1093/nar/10.1.341. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Ostrowski J., Jagura-Burdzy G., Kredich N. M. DNA sequences of the cysB regions of Salmonella typhimurium and Escherichia coli. J Biol Chem. 1987 May 5;262(13):5999–6005. [PubMed] [Google Scholar]
  31. Ostrowski J., Kredich N. M. Molecular characterization of the cysJIH promoters of Salmonella typhimurium and Escherichia coli: regulation by cysB protein and N-acetyl-L-serine. J Bacteriol. 1989 Jan;171(1):130–140. doi: 10.1128/jb.171.1.130-140.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Papanicolaou C., Gouy M., Ninio J. An energy model that predicts the correct folding of both the tRNA and the 5S RNA molecules. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):31–44. doi: 10.1093/nar/12.1part1.31. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Plamann L. S., Stauffer G. V. Nucleotide sequence of the Salmonella typhimurium metR gene and the metR-metE control region. J Bacteriol. 1987 Sep;169(9):3932–3937. doi: 10.1128/jb.169.9.3932-3937.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Post L. E., Strycharz G. D., Nomura M., Lewis H., Dennis P. P. Nucleotide sequence of the ribosomal protein gene cluster adjacent to the gene for RNA polymerase subunit beta in Escherichia coli. Proc Natl Acad Sci U S A. 1979 Apr;76(4):1697–1701. doi: 10.1073/pnas.76.4.1697. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Sor F., Nomura M. Cloning and DNA sequence determination of the L11 ribosomal protein operon of Serratia marcescens and Proteus vulgaris: translational feedback regulation of the Escherichia coli L11 operon by heterologous L1 proteins. Mol Gen Genet. 1987 Nov;210(1):52–59. doi: 10.1007/BF00337758. [DOI] [PubMed] [Google Scholar]
  36. Stephens P. E., Lewis H. M., Darlison M. G., Guest J. R. Nucleotide sequence of the lipoamide dehydrogenase gene of Escherichia coli K12. Eur J Biochem. 1983 Oct 3;135(3):519–527. doi: 10.1111/j.1432-1033.1983.tb07683.x. [DOI] [PubMed] [Google Scholar]
  37. Stern M. J., Ames G. F., Smith N. H., Robinson E. C., Higgins C. F. Repetitive extragenic palindromic sequences: a major component of the bacterial genome. Cell. 1984 Jul;37(3):1015–1026. doi: 10.1016/0092-8674(84)90436-7. [DOI] [PubMed] [Google Scholar]
  38. Stormo G. D., Schneider T. D., Gold L. M. Characterization of translational initiation sites in E. coli. Nucleic Acids Res. 1982 May 11;10(9):2971–2996. doi: 10.1093/nar/10.9.2971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Tinoco I., Jr, Borer P. N., Dengler B., Levin M. D., Uhlenbeck O. C., Crothers D. M., Bralla J. Improved estimation of secondary structure in ribonucleic acids. Nat New Biol. 1973 Nov 14;246(150):40–41. doi: 10.1038/newbio246040a0. [DOI] [PubMed] [Google Scholar]
  40. Umeda M., Ohtsubo E. Mapping of insertion element IS30 in the Escherichia coli K12 chromosome. Mol Gen Genet. 1990 Jul;222(2-3):317–322. doi: 10.1007/BF00633835. [DOI] [PubMed] [Google Scholar]
  41. Umeda M., Ohtsubo E. Mapping of insertion element IS5 in the Escherichia coli K-12 chromosome. Chromosomal rearrangements mediated by IS5. J Mol Biol. 1990 May 20;213(2):229–237. doi: 10.1016/S0022-2836(05)80186-X. [DOI] [PubMed] [Google Scholar]
  42. Umeda M., Ohtsubo E. Mapping of insertion elements IS1, IS2 and IS3 on the Escherichia coli K-12 chromosome. Role of the insertion elements in formation of Hfrs and F' factors and in rearrangement of bacterial chromosomes. J Mol Biol. 1989 Aug 20;208(4):601–614. doi: 10.1016/0022-2836(89)90151-4. [DOI] [PubMed] [Google Scholar]
  43. Yang Y., Ames G. F. DNA gyrase binds to the family of prokaryotic repetitive extragenic palindromic sequences. Proc Natl Acad Sci U S A. 1988 Dec;85(23):8850–8854. doi: 10.1073/pnas.85.23.8850. [DOI] [PMC free article] [PubMed] [Google Scholar]

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