Skip to main content
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1984 Aug;159(2):618–623. doi: 10.1128/jb.159.2.618-623.1984

Location and analysis of nucleotide sequences at one end of a putative lac transposon in the Escherichia coli chromosome.

W E Buvinger, K A Lampel, R J Bojanowski, M Riley
PMCID: PMC215688  PMID: 6086580

Abstract

A segment of Escherichia coli DNA that contained a discontinuity of homology with Salmonella typhimurium DNA was isolated. The segment, 1,430 base pairs long, was derived from one end of the lac "loop," a region of about 12 kilobase pairs of E. coli DNA, including the lac operon which has no detectable homology with S. typhimurium DNA (K. Lampel and M. Riley, Mol. Gen. Genet. 186:82-86, 1982). The nucleotide sequence of the 1,430-base-pair segment of DNA was determined. The location of the junction of discontinuity of homology within the segment was established by hybridization experiments. Nucleotide sequences at or near the junction were determined to be similar to sequences that are involved in site-specific inversion in S. typhimurium, E. coli, phage P1, and phage Mu. Similar sequences are also present within the terminal inverted repeat sequences of transposon Tn5 and at the V-D-J joining sequences of eucaryotic immunoglobulin genes. Therefore, the lac operon, together with flanking DNA, may have been inserted into the E. coli chromosome at one time via a site-specific recombination event. Rearrangement events of this kind undoubtedly have played a significant role in the evolutionary divergence of chromosomal DNAs.

Full text

PDF
618

Images in this article

Selected References

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

  1. Alwine J. C., Kemp D. J., Parker B. A., Reiser J., Renart J., Stark G. R., Wahl G. M. Detection of specific RNAs or specific fragments of DNA by fractionation in gels and transfer to diazobenzyloxymethyl paper. Methods Enzymol. 1979;68:220–242. doi: 10.1016/0076-6879(79)68017-5. [DOI] [PubMed] [Google Scholar]
  2. Anilionis A., Riley M. Conservation and variation of nucleotide sequences within related bacterial genomes: Escherichia coli strains. J Bacteriol. 1980 Jul;143(1):355–365. doi: 10.1128/jb.143.1.355-365.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bachmann B. J. Linkage map of Escherichia coli K-12, edition 7. Microbiol Rev. 1983 Jun;47(2):180–230. doi: 10.1128/mr.47.2.180-230.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bolivar F., Rodriguez R. L., Greene P. J., Betlach M. C., Heyneker H. L., Boyer H. W., Crosa J. H., Falkow S. Construction and characterization of new cloning vehicles. II. A multipurpose cloning system. Gene. 1977;2(2):95–113. [PubMed] [Google Scholar]
  5. Chaconas G., de Bruijn F. J., Casadaban M. J., Lupski J. R., Kwoh T. J., Harshey R. M., DuBow M. S., Bukhari A. I. In vitro and in vivo manipulations of bacteriophage Mu DNA: cloning of Mu ends and construction of mini-Mu's carrying selectable markers. Gene. 1981 Jan-Feb;13(1):37–46. doi: 10.1016/0378-1119(81)90041-x. [DOI] [PubMed] [Google Scholar]
  6. Cornelis G., Ghosal D., Saedler H. Tn951: a new transposon carrying a lactose operon. Mol Gen Genet. 1978 Apr 6;160(2):215–224. doi: 10.1007/BF00267484. [DOI] [PubMed] [Google Scholar]
  7. Cornelis G. Sequence relationships between plasmids carrying genes for lactose utilization. J Gen Microbiol. 1981 May;124(1):91–97. doi: 10.1099/00221287-124-1-91. [DOI] [PubMed] [Google Scholar]
  8. Fultz P. N., Kwoh D. Y., Kemper J. Salmonella typhimurium newD and Escherichia coli leuC genes code for a functional isopropylmalate isomerase in Salmonella typhimurium-Escherichia coli hybrids. J Bacteriol. 1979 Mar;137(3):1253–1262. doi: 10.1128/jb.137.3.1253-1262.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Guiso N., Ullmann A. Expression and regulation of lactose genes carried by plasmids. J Bacteriol. 1976 Aug;127(2):691–697. doi: 10.1128/jb.127.2.691-697.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Hiestand-Nauer R., Iida S. Sequence of the site-specific recombinase gene cin and of its substrates serving in the inversion of the C segment of bacteriophage P1. EMBO J. 1983;2(10):1733–1740. doi: 10.1002/j.1460-2075.1983.tb01650.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hong G. F. A systemic DNA sequencing strategy. J Mol Biol. 1982 Jul 5;158(3):539–549. doi: 10.1016/0022-2836(82)90213-3. [DOI] [PubMed] [Google Scholar]
  12. Kamp D., Chow L. T., Broker T. R., Kwoh D., Zipser D., Kahmann R. Site-specific recombination in phage mu. Cold Spring Harb Symp Quant Biol. 1979;43(Pt 2):1159–1167. doi: 10.1101/sqb.1979.043.01.131. [DOI] [PubMed] [Google Scholar]
  13. Kennedy K. E., Iida S., Meyer J., Stålhammar-Carlemalm M., Hiestand-Nauer R., Arber W. Genome fusion mediated by the site specific DNA inversion system of bacteriophage P1. Mol Gen Genet. 1983;189(3):413–421. doi: 10.1007/BF00325903. [DOI] [PubMed] [Google Scholar]
  14. Lampel K. A., Riley M. Discontinuity of homology of Escherichia coli and Salmonella typhimurium DNA in the lac region. Mol Gen Genet. 1982;186(1):82–86. doi: 10.1007/BF00422916. [DOI] [PubMed] [Google Scholar]
  15. Le Minor L., Coynault C., Pessoa G. Déterminisme plasmidique du caractère atypique "lactose positif" de souches de S. typhi-murium et de S. oranienburg isolées au Brésil lors d'épidémies de 1971 à 1973. Ann Microbiol (Paris) 1974 Apr;125A(3):261–285. [PubMed] [Google Scholar]
  16. Messing J., Vieira J. A new pair of M13 vectors for selecting either DNA strand of double-digest restriction fragments. Gene. 1982 Oct;19(3):269–276. doi: 10.1016/0378-1119(82)90016-6. [DOI] [PubMed] [Google Scholar]
  17. Plasterk R. H., Brinkman A., van de Putte P. DNA inversions in the chromosome of Escherichia coli and in bacteriophage Mu: relationship to other site-specific recombination systems. Proc Natl Acad Sci U S A. 1983 Sep;80(17):5355–5358. doi: 10.1073/pnas.80.17.5355. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Reeve E. C., Braithwaite J. A. The lactose system in Klebsiella aerogenes V9A. 4. A comparison of the lac operons of Klebsiella and Escherichia coli. Genet Res. 1974 Dec;24(3):323–331. doi: 10.1017/s0016672300015329. [DOI] [PubMed] [Google Scholar]
  19. Rigby P. W., Dieckmann M., Rhodes C., Berg P. Labeling deoxyribonucleic acid to high specific activity in vitro by nick translation with DNA polymerase I. J Mol Biol. 1977 Jun 15;113(1):237–251. doi: 10.1016/0022-2836(77)90052-3. [DOI] [PubMed] [Google Scholar]
  20. Riley M., Anilionis A. Conservation and variation of nucleotide sequences within related bacterial genomes: enterobacteria. J Bacteriol. 1980 Jul;143(1):366–376. doi: 10.1128/jb.143.1.366-376.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Riley M., Anilionis A. Evolution of the bacterial genome. Annu Rev Microbiol. 1978;32:519–560. doi: 10.1146/annurev.mi.32.100178.002511. [DOI] [PubMed] [Google Scholar]
  22. Riley M., O'Reilly C., McConnell D. Physical map of Salmonella typhimurium LT2 DNA in the vicinity of the proA gene. J Bacteriol. 1984 Feb;157(2):655–657. doi: 10.1128/jb.157.2.655-657.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Rothstein S. J., Reznikoff W. S. The functional differences in the inverted repeats of Tn5 are caused by a single base pair nonhomology. Cell. 1981 Jan;23(1):191–199. doi: 10.1016/0092-8674(81)90284-1. [DOI] [PubMed] [Google Scholar]
  24. Sanderson K. E., Roth J. R. Linkage map of Salmonella typhimurium, Edition VI. Microbiol Rev. 1983 Sep;47(3):410–453. doi: 10.1128/mr.47.3.410-453.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Sasakawa C., Carle G. F., Berg D. E. Sequences essential for transposition at the termini of IS50. Proc Natl Acad Sci U S A. 1983 Dec;80(23):7293–7297. doi: 10.1073/pnas.80.23.7293. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Schlesinger M. J., Olsen R. Expression and localization of Escherichia coli alkaline phosphatase synthesized in Salmonella typhimurium cytoplasm. J Bacteriol. 1968 Nov;96(5):1601–1605. doi: 10.1128/jb.96.5.1601-1605.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Scott T. N., Simon M. I. Genetic analysis of the mechanism of the Salmonella phase variation site specific recombination system. Mol Gen Genet. 1982;188(2):313–321. doi: 10.1007/BF00332694. [DOI] [PubMed] [Google Scholar]
  29. Simon M., Zieg J., Silverman M., Mandel G., Doolittle R. Phase variation: evolution of a controlling element. Science. 1980 Sep 19;209(4463):1370–1374. doi: 10.1126/science.6251543. [DOI] [PubMed] [Google Scholar]
  30. Southern E. M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. doi: 10.1016/s0022-2836(75)80083-0. [DOI] [PubMed] [Google Scholar]
  31. Szekely E., Simon M. DNA sequence adjacent to flagellar genes and evolution of flagellar-phase variation. J Bacteriol. 1983 Jul;155(1):74–81. doi: 10.1128/jb.155.1.74-81.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Tonegawa S. Somatic generation of antibody diversity. Nature. 1983 Apr 14;302(5909):575–581. doi: 10.1038/302575a0. [DOI] [PubMed] [Google Scholar]
  33. York M. K., Stodolsky M. Characterization of P1argF derivatives from Escherichia coli K12 transduction. I. IS1 elements flank the argF gene segment. Mol Gen Genet. 1981;181(2):230–240. doi: 10.1007/BF00268431. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES