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Molecular and General Genetics MGG

, Volume 217, Issue 2–3, pp 269–277 | Cite as

Nucleotide sequences from the colicin E5, E6 and E9 operons: Presence of a degenerate transposon-like structure in the ColE9-J plasmid

  • Peter C. K. Lau
  • Janet A. Condie
Article

Summary

The nucleotide sequences of 1288 bp of plasmid ColE5-099, 1609 bp of ColE6-CT14 and 2099 bp of ColE9-J were determined. These sequences encompass the structural genes for the C-terminal receptor-binding and nuclease domains of colicins E5, E6 and E9, theircis- ortrans-acting immunity proteins and four lysis proteins including an atypical one of non-lipoprotein nature (Lys*) present in the ColE9-J plasmid. The ColE6 gene organisation, in the ordercol-imm-E8imm-lys, is identical to that found in the previously described double-immunity gene system of ColE3-CA38 (an RNase producer). The corresponding genes in the two plasmids are 87%–94% homologous. In ColE9-J, the genes are organised ascol-imm-lys *-E5imm-lys. The E9col-imm gene pair is homologous to the colicin E2-P9 type (a DNase producer). Downstream from E9imm is an E5imm (designated E5imm[E9]) which istrans-acting. Neither the predicted structures of E5Imm[E9] nor thecis-acting Imm resident in the ColE5-099 plasmid which differs by a single amino acid shows any resemblance to other immunity structures which have been sequenced. Furthermore, the E5col sequences differ from those predicted previously for other colicins except for the conservedbtuB-specified receptor-binding domain. A novel 205 nucleotide long insertion sequence is found in the ColE9-J plasmid. This insertion sequence, which we named ISE9, has features reminiscent of the degenerate transposon IS101 previously found in plasmid pSC101. One effect of ISE9 is the presence of the atypical lysis gene,lys *. The presence of a transposon-like element in the ColE9 plasmid exemplifies a new phenomenon relevant to the evolution of colicin E plasmids.

Key words

Endonuclease Immunity Lipoprotein signal peptide Lysis IS elements 

Abbreviations and symbols

[]

indicates the plasmid carrier strain

ORF

open reading frame

bp

base pairs

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References

  1. Bowman CM, Dahlerg JE, Ikemura T, Konisky J, Nomura M (1971) Specific inactivation of 16S ribosomal RNA induced by colicin E3in vitro. Proc Natl Acad Sci USA 68:964–968PubMedCrossRefGoogle Scholar
  2. Cavard D, Baty D, Howard SP, Verheij HM, Lazdunski C (1987) Lipoprotein nature of the colicin A lysis protein: Effect of amino acid substitutions at the site of modification and processing. J Bacteriol 169:2187–2194PubMedGoogle Scholar
  3. Chak K-F, James R (1984) Localisation and characterisation of a gene on the ColE3-CA38 plasmid that confers immunity to colicin E8. J Gen Microbiol 130:701–710PubMedGoogle Scholar
  4. Chak K-F, James R (1986) Characterisation of the ColE9-J plasmid and analysis of its genetic organisation. J Gen Microbiol 132:61–71PubMedGoogle Scholar
  5. Chen EY, Seeburg PH (1985) Supercoil sequencing: A fast and simple method for sequencing plasmid DNA. DNA 4:165–170PubMedCrossRefGoogle Scholar
  6. Cole ST, Saint-Joanis B, Pugsley AP (1985) Molecular characterisation of the colicin E2 operon and identification of its products. Mol Gen Genet 198:465–472PubMedCrossRefGoogle Scholar
  7. Cooper PC, James R (1984) Two new E colicins, E8 and E9, produced by a strain ofEscherichia coli. J Gen Microbiol 130:209–215PubMedGoogle Scholar
  8. Cooper PC, Hawkins FKL, James R (1986) Incompatibility between E colicin plasmids. J Gen Microbiol 132:1859–1862PubMedGoogle Scholar
  9. de Graaf FK, Oudega B (1986) Production and release of cloacin DF13 and related colicins. Curr Top Microbiol Immunol 125:183–205PubMedGoogle Scholar
  10. DiMasi RD, White J, Schnaitman CA, Bradbeer C (1973) Transport of vitamin B12 inE. coli: common receptor sites for vitamin B12 and the E colicins on the outer membrane of the cell envelope. J Bacteriol 115:506–573Google Scholar
  11. Fischhoff DA, Vovis GF, Zinder ND (1980) Organisation of chimeras between filamentous bacteriophage f1 and plasmid pSC101. J Mol Biol 144:247–265PubMedCrossRefGoogle Scholar
  12. Gaastra W, Oudega B, de Graaf FK (1978) The use of mutants in the study of structure-function relationships in cloacin DF13. Biochim Biophys Acta 540:301–312PubMedGoogle Scholar
  13. Grindley NDF, Lauth MR, Wells RG, Wityk RJ, Salvo JJ, Reed RR (1982) Transposon-mediated site-specific recombination: Identification of three binding sites for resolvase at theres sites of γσ and Tn3. Cell 30:19–27PubMedCrossRefGoogle Scholar
  14. Heffron F (1983) Tn3 and its relatives. In: Shapiro JA (ed) Mobile genetic elements. Academic Press, New York, pp 223–260Google Scholar
  15. Jakes KS (1982) The mechanism of action of colicin E2, colicin E3 and cloacin DF13. In: Cohen P, van Heyningen S (eds) Molecular action of toxins and viruses, vol. 2. Elsevier, Amsterdam, pp 131–167Google Scholar
  16. James R, Jarvis M, Barker DF (1987) Nucleotide sequence of the immunity and lysis regions of the ColE9-J plasmid. J Gen Microbiol 133:1553–1562PubMedGoogle Scholar
  17. Kleckner N (1981) Transposable elements in prokaryotes. Annu Rev Genetics 15:341–404CrossRefGoogle Scholar
  18. Klein P, Somorjai RL, Lau PCK (1988) Distinctive properties of signal sequences from bacterial lipoproteins. Protein Eng 2:15–20PubMedGoogle Scholar
  19. Konisky J (1982) Colicins and other bacteriocins with established modes of action. Annu Rev Microbiol 36:125–144PubMedCrossRefGoogle Scholar
  20. Kool AJ, Pols C, Nijkamp HJJ (1975) Bacteriocinogenic CloDF13 minicells ofEscherichia coli synthesize a protein that accounts for immunity to bacteriocin CloDF13: purification and characterization of the immunity protein. Antimicrob Agents Chemother 8:67–75PubMedGoogle Scholar
  21. Lau PCK, Rowsome RW, Watson RJ, Visentin LP (1984a) The immunity genes of colicins E2 and E8 are closely related. Biosci Rep 4:565–572PubMedCrossRefGoogle Scholar
  22. Lau PCK, Rowsome RW, Zuker M, Visentin LP (1984b) Comparative nucleotide sequences encoding the immunity proteins and the carboxyl-terminal peptides of colicins E2 and E3. Nucleic Acids Res 12:8733–8745PubMedGoogle Scholar
  23. Males BM, Stocker BAD (1982) Colicins E4, E5, E6 and A and properties ofbtuB+ colicinogenic transconjugants. J Gen Microbiol 128:95–106PubMedGoogle Scholar
  24. Masaki H, Ohta T (1982) A plasmid region encoding the active fragment and the inhibitor protein of colicin E3-CA38. FEBS Lett 149:129–132PubMedCrossRefGoogle Scholar
  25. Masaki H, Ohta T (1985) Colicin E3 and its immunity genes. J Mol Biol 182:217–227PubMedCrossRefGoogle Scholar
  26. Mochitate K, Suzuki K, Imahori K (1981) Amino acid sequence of immunity protein (B subunit) of colicin E3. J Biochem 89:1609–1618PubMedGoogle Scholar
  27. Mock M, Pugsley AP (1982) The BtuB group Col plasmids and homology between the colicins they encode. J Bacteriol 150:1069–1076PubMedGoogle Scholar
  28. Ohno S, Imahori K (1978) Colicin E3 is an endonuclease. J Biochem 84:1637–1640PubMedGoogle Scholar
  29. Ohno S, Saito K, Suzuki K, Imahori K (1980) The effects of carboxypeptidase digestion on the function of colicin E3. J Biochem 87:989–992PubMedGoogle Scholar
  30. Ohno-Iwashita Y, Imahori K (1980) Assignment of the functional loci in colicin E2 and E3 molecules by the characterisation of their proteolytic fragments. Biochemistry 19:652–659PubMedCrossRefGoogle Scholar
  31. Perlman D, Halvorson HO (1983) A putative signal peptidase recognition site and sequence in eukaryotic and prokaryotic signal peptides. J Mol Biol 167:391–409PubMedGoogle Scholar
  32. Pugsley AP (1988) The immunity and lysis genes of ColN plasmid pCHAP4. Mol Gen Genet 211:335–341PubMedCrossRefGoogle Scholar
  33. Pugsley AP, Cole ST (1987) An unmodified form of the ColE2 lysis protein, an envelope lipoprotein, retains reduced ability to promote colicin E2 release and lysis of producing cells. J Gen Microbiol 133:2411–2420PubMedGoogle Scholar
  34. Ravetch JV, Ohsumi M, Model P, Vovis GF, Fischhoff D, Zinder ND (1979) Organization of a hybrid between phage f1 and plasmid pSC101. Proc Natl Acad Sci USA 76:2195–2198PubMedCrossRefGoogle Scholar
  35. Schaller K, Nomura M (1976) Colicin E2 is a DNA endonuclease. Proc Natl Acad Sci USA 73:3989–3993PubMedCrossRefGoogle Scholar
  36. Terwilliger TC, Eisenberg D (1982) The structure of mellitin I. Structure determination and partial refinement. J Biol Chem 257:6010–6015PubMedGoogle Scholar
  37. Toba M, Masaki H, Ohta T (1986) Primary structures of the ColE2-P9 and ColE3-CA38 lysis genes. J Biochem 99:591–596PubMedGoogle Scholar
  38. Toba M, Masaki H, Ohta T (1988) Colicin E8, a DNase which indicates an evolutionary relationship between colicins E2 and E3. J Bacteriol 170:3237–2342PubMedGoogle Scholar
  39. Uchimura T, Lau PCK (1987) Nucleotides sequences from the colicin E8 operon: Homology with plasmid ColE2-P9. Mol Gen Genet 209:489–493PubMedCrossRefGoogle Scholar
  40. van den Elzen PJM, Gaastra W, Spelt CE, De Graaf FK, Veltkamp E, Nijkamp HJJ (1980) Molecular structure of the immunity gene and immunity protein of the bacteriocinogenic plasmid CloDF13. Nucleic Acids Res 8:4349–4363PubMedGoogle Scholar
  41. van den Elzen PJM, Walters HHB, Veltkamp E, Nijkamp HJJ (1983) Molecular structure and function of the bacteriocin gene and bacteriocin protein of plasmid CloDF13. Nucleic Acids Res 11:2465–2477PubMedGoogle Scholar
  42. Watson RJ, Lau PCK, Vernet T, Visentin LP (1984) Characterisation and nucleotide sequence of a colicin-release gene in thehic region of plasmid ColE3-CA38. Gene 29:175–184 (Corrigendum 42:351–353, 1986)PubMedCrossRefGoogle Scholar
  43. Watson RJ, Vernet T, Visentin LP (1985) Relationships of the Col plasmids E2, E3, E4, E5, E6 and E7: restriction mapping and colicin gene fusions. Plasmid 13:205–210PubMedCrossRefGoogle Scholar
  44. Yanisch-Perron C, Vieira J, Messing J (1985) Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33:103–119PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 1989

Authors and Affiliations

  • Peter C. K. Lau
    • 1
  • Janet A. Condie
    • 1
  1. 1.Genetic Engineering Section, Biotechnology Research InstituteNational Research Council of CanadaMontréalCanada

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