• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of geneticsGeneticsCurrent IssueInformation for AuthorsEditorial BoardSubscribeSubmit a Manuscript
Genetics. Mar 1997; 145(3): 551–562.
PMCID: PMC1207841

Bacterial Interspersed Mosaic Elements (Bimes) Are a Major Source of Sequence Polymorphism in Escherichia Coli Intergenic Regions Including Specific Associations with a New Insertion Sequence

Abstract

A significant fraction of Escherichia coli intergenic DNA sequences is composed of two families of repeated bacterial interspersed mosaic elements (BIME-1 and BIME-2). In this study, we determined the sequence organization of six intergenic regions in 51 E. coli and Shigella natural isolates. Each region contains a BIME in E. coli K-12. We found that multiple sequence variations are located within or near these BIMEs in the different bacteria. Events included excisions of a whole BIME-1, expansion/deletion within a BIME-2 and insertions of non-BIME sequences like the boxC repeat or a new IS element, named IS1397. Remarkably, 14 out of 14 IS1397 integration sites correspond to a BIME sequence, strongly suggesting that this IS element is specifically associated with BIMEs, and thus inserts only in extragenic regions. Unlike BIMEs, IS1397 is not detected in all E. coli isolates. Possible relationships between the presence of this IS element and the evolution of BIMEs are discussed.

Full Text

The Full Text of this article is available as a PDF (3.9M).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Bachellier S, Perrin D, Hofnung M, Gilson E. Bacterial interspersed mosaic elements (BIMEs) are present in the genome of Klebsiella. Mol Microbiol. 1993 Feb;7(4):537–544. [PubMed]
  • Bachellier S, Saurin W, Perrin D, Hofnung M, Gilson E. Structural and functional diversity among bacterial interspersed mosaic elements (BIMEs). Mol Microbiol. 1994 Apr;12(1):61–70. [PubMed]
  • Birkenbihl RP, Vielmetter W. Complete maps of IS1, IS2, IS3, IS4, IS5, IS30 and IS150 locations in Escherichia coli K12. Mol Gen Genet. 1989 Dec;220(1):147–153. [PubMed]
  • Boccard F, Prentki P. Specific interaction of IHF with RIBs, a class of bacterial repetitive DNA elements located at the 3' end of transcription units. EMBO J. 1993 Dec 15;12(13):5019–5027. [PMC free article] [PubMed]
  • Chandler M, Fayet O. Translational frameshifting in the control of transposition in bacteria. Mol Microbiol. 1993 Feb;7(4):497–503. [PubMed]
  • Dahl MK, Francoz E, Saurin W, Boos W, Manson MD, Hofnung M. Comparison of sequences from the malB regions of Salmonella typhimurium and Enterobacter aerogenes with Escherichia coli K12: a potential new regulatory site in the interoperonic region. Mol Gen Genet. 1989 Aug;218(2):199–207. [PubMed]
  • Dimri GP, Rudd KE, Morgan MK, Bayat H, Ames GF. Physical mapping of repetitive extragenic palindromic sequences in Escherichia coli and phylogenetic distribution among Escherichia coli strains and other enteric bacteria. J Bacteriol. 1992 Jul;174(14):4583–4593. [PMC free article] [PubMed]
  • Dodd IB, Egan JB. Improved detection of helix-turn-helix DNA-binding motifs in protein sequences. Nucleic Acids Res. 1990 Sep 11;18(17):5019–5026. [PMC free article] [PubMed]
  • Gilson E, Rousset JP, Clément JM, Hofnung M. A subfamily of E. coli palindromic units implicated in transcription termination? Ann Inst Pasteur Microbiol. 1986 Nov-Dec;137B(3):259–270. [PubMed]
  • 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. [PMC free article] [PubMed]
  • Gilson E, Saurin W, Perrin D, Bachellier S, Hofnung M. Palindromic units are part of a new bacterial interspersed mosaic element (BIME). Nucleic Acids Res. 1991 Apr 11;19(7):1375–1383. [PMC free article] [PubMed]
  • Gilson E, Saurin W, Perrin D, Bachellier S, Hofnung M. The BIME family of bacterial highly repetitive sequences. Res Microbiol. 1991 Feb-Apr;142(2-3):217–222. [PubMed]
  • Gustafson CE, Chu S, Trust TJ. Mutagenesis of the paracrystalline surface protein array of Aeromonas salmonicida by endogenous insertion elements. J Mol Biol. 1994 Apr 8;237(4):452–463. [PubMed]
  • Herzer PJ, Inouye S, Inouye M, Whittam TS. Phylogenetic distribution of branched RNA-linked multicopy single-stranded DNA among natural isolates of Escherichia coli. J Bacteriol. 1990 Nov;172(11):6175–6181. [PMC free article] [PubMed]
  • Higgins CF, Ames GF, Barnes WM, Clement JM, Hofnung M. A novel intercistronic regulatory element of prokaryotic operons. Nature. 1982 Aug 19;298(5876):760–762. [PubMed]
  • Higgins DG, Bleasby AJ, Fuchs R. CLUSTAL V: improved software for multiple sequence alignment. Comput Appl Biosci. 1992 Apr;8(2):189–191. [PubMed]
  • Hill CW, Sandt CH, Vlazny DA. Rhs elements of Escherichia coli: a family of genetic composites each encoding a large mosaic protein. Mol Microbiol. 1994 Jun;12(6):865–871. [PubMed]
  • Hill CW, Feulner G, Brody MS, Zhao S, Sadosky AB, Sandt CH. Correlation of Rhs elements with Escherichia coli population structure. Genetics. 1995 Sep;141(1):15–24. [PMC free article] [PubMed]
  • Hsiao K. A fast and simple procedure for sequencing double stranded DNA with sequenase. Nucleic Acids Res. 1991 May 25;19(10):2787–2787. [PMC free article] [PubMed]
  • Kulkosky J, Jones KS, Katz RA, Mack JP, Skalka AM. Residues critical for retroviral integrative recombination in a region that is highly conserved among retroviral/retrotransposon integrases and bacterial insertion sequence transposases. Mol Cell Biol. 1992 May;12(5):2331–2338. [PMC free article] [PubMed]
  • Landschulz WH, Johnson PF, McKnight SL. The leucine zipper: a hypothetical structure common to a new class of DNA binding proteins. Science. 1988 Jun 24;240(4860):1759–1764. [PubMed]
  • Lim D, Gomes TA, Maas WK. Distribution of msDNAs among serotypes of enteropathogenic Escherichia coli strains. Mol Microbiol. 1990 Oct;4(10):1711–1714. [PubMed]
  • Lin HC, Lei SP, Studnicka G, Wilcox G. The araBAD operon of Salmonella typhimurium LT2. III. Nucleotide sequence of araD and its flanking regions, and primary structure of its product, L-ribulose-5-phosphate 4-epimerase. Gene. 1985;34(1):129–134. [PubMed]
  • McAdam RA, Hermans PW, van Soolingen D, Zainuddin ZF, Catty D, van Embden JD, Dale JW. Characterization of a Mycobacterium tuberculosis insertion sequence belonging to the IS3 family. Mol Microbiol. 1990 Sep;4(9):1607–1613. [PubMed]
  • Mueller PR, Wold B. In vivo footprinting of a muscle specific enhancer by ligation mediated PCR. Science. 1989 Nov 10;246(4931):780–786. [PubMed]
  • Newbury SF, Smith NH, Higgins CF. Differential mRNA stability controls relative gene expression within a polycistronic operon. Cell. 1987 Dec 24;51(6):1131–1143. [PubMed]
  • Newbury SF, Smith NH, Robinson EC, Hiles ID, Higgins CF. Stabilization of translationally active mRNA by prokaryotic REP sequences. Cell. 1987 Jan 30;48(2):297–310. [PubMed]
  • Ochman H, Selander RK. Standard reference strains of Escherichia coli from natural populations. J Bacteriol. 1984 Feb;157(2):690–693. [PMC free article] [PubMed]
  • Oppenheim AB, Rudd KE, Mendelson I, Teff D. Integration host factor binds to a unique class of complex repetitive extragenic DNA sequences in Escherichia coli. Mol Microbiol. 1993 Oct;10(1):113–122. [PubMed]
  • Polard P, Chandler M. Bacterial transposases and retroviral integrases. Mol Microbiol. 1995 Jan;15(1):13–23. [PubMed]
  • Polard P, Prère MF, Chandler M, Fayet O. Programmed translational frameshifting and initiation at an AUU codon in gene expression of bacterial insertion sequence IS911. J Mol Biol. 1991 Dec 5;222(3):465–477. [PubMed]
  • Prère MF, Chandler M, Fayet O. Transposition in Shigella dysenteriae: isolation and analysis of IS911, a new member of the IS3 group of insertion sequences. J Bacteriol. 1990 Jul;172(7):4090–4099. [PMC free article] [PubMed]
  • Sadosky AB, Davidson A, Lin RJ, Hill CW. rhs gene family of Escherichia coli K-12. J Bacteriol. 1989 Feb;171(2):636–642. [PMC free article] [PubMed]
  • Sansonetti PJ, Arondel J. Construction and evaluation of a double mutant of Shigella flexneri as a candidate for oral vaccination against shigellosis. Vaccine. 1989 Oct;7(5):443–450. [PubMed]
  • Sawyer SA, Dykhuizen DE, DuBose RF, Green L, Mutangadura-Mhlanga T, Wolczyk DF, Hartl DL. Distribution and abundance of insertion sequences among natural isolates of Escherichia coli. Genetics. 1987 Jan;115(1):51–63. [PMC free article] [PubMed]
  • Sekine Y, Eisaki N, Ohtsubo E. Translational control in production of transposase and in transposition of insertion sequence IS3. J Mol Biol. 1994 Feb 4;235(5):1406–1420. [PubMed]
  • Shyamala V, Schneider E, Ames GF. Tandem chromosomal duplications: role of REP sequences in the recombination event at the join-point. EMBO J. 1990 Mar;9(3):939–946. [PMC free article] [PubMed]
  • Skaugen M, Nes IF. Transposition in Lactobacillus sake and its abolition of lactocin S production by insertion of IS1163, a new member of the IS3 family. Appl Environ Microbiol. 1994 Aug;60(8):2818–2825. [PMC free article] [PubMed]
  • Stern MJ, Ames GF, Smith NH, Robinson EC, Higgins CF. Repetitive extragenic palindromic sequences: a major component of the bacterial genome. Cell. 1984 Jul;37(3):1015–1026. [PubMed]
  • Stern MJ, Prossnitz E, Ames GF. Role of the intercistronic region in post-transcriptional control of gene expression in the histidine transport operon of Salmonella typhimurium: involvement of REP sequences. Mol Microbiol. 1988 Jan;2(1):141–152. [PubMed]
  • Vögele K, Schwartz E, Welz C, Schiltz E, Rak B. High-level ribosomal frameshifting directs the synthesis of IS150 gene products. Nucleic Acids Res. 1991 Aug 25;19(16):4377–4385. [PMC free article] [PubMed]
  • Walker JE, Saraste M, Runswick MJ, Gay NJ. Distantly related sequences in the alpha- and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J. 1982;1(8):945–951. [PMC free article] [PubMed]
  • Yang Y, Ames GF. 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. [PMC free article] [PubMed]
  • Zhao S, Hill CW. Reshuffling of Rhs components to create a new element. J Bacteriol. 1995 Mar;177(5):1393–1398. [PMC free article] [PubMed]
  • Zhao S, Sandt CH, Feulner G, Vlazny DA, Gray JA, Hill CW. Rhs elements of Escherichia coli K-12: complex composites of shared and unique components that have different evolutionary histories. J Bacteriol. 1993 May;175(10):2799–2808. [PMC free article] [PubMed]
  • Zou S, Ke N, Kim JM, Voytas DF. The Saccharomyces retrotransposon Ty5 integrates preferentially into regions of silent chromatin at the telomeres and mating loci. Genes Dev. 1996 Mar 1;10(5):634–645. [PubMed]

Articles from Genetics are provided here courtesy of Genetics Society of America

Formats:

Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...

Links

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...