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. 1985 Sep;163(3):832–836. doi: 10.1128/jb.163.3.832-836.1985

Presence of DNA, encoding parts of bacteriophage tail fiber genes, in the chromosome of Escherichia coli K-12.

I Riede, M L Eschbach, U Henning
PMCID: PMC219206  PMID: 2993246

Abstract

The classical T-even bacteriophages recognize host cells with their long tail fibers. Gene products 35, 36, and 37 constitute the distal moiety of these fibers. The free ends of the tail fibers, which are formed by the CO2H terminus of gene product 37, possess the host range determinants. It was found that 4 out of 10 different strains of Escherichia coli K-12 contained regions of chromosomal DNA which hybridized with a probe consisting of genes 35, 36, and 37 of the T-even phage K3. From one strain this homologous DNA, which was associated with an EcoRI fragment of about 5 kilobases, was cloned into plasmid pUC8. Two independently recovered hybrid plasmids had undergone a peculiar rearrangement which resulted in the loss of about 3 kilobases of cloned DNA and a duplication of both the vector and the remaining chromosomal DNA. The mechanisms causing this duplication-deletion may be related to that of transposases. The cloned DNA was capable of recombination with phage T4 gene 36 and a phage T2 gene 37 amber mutant. DNA sequencing revealed the existence of regions of identity between the cloned DNA and genes 36 and 37 of phage T2. In addition, after growth of a derivative of phage K3 on a strain harboring T2 DNA, it was found that this phage contained the same parts of the T2 tail fiber genes which had been recovered from the bacterial chromosome. There appears to be little doubt that the phage had picked up this DNA from the host. The possibility is considered that a repertoire of parts of genes 36 and 37 of various T-even-type phages is present in their hosts, allowing the former to change their host ranges.

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Selected References

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  1. Beckendorf S. K., Kim J. S., Lielausis I. Structure of bacteriophage T4 genes 37 and 38. J Mol Biol. 1973 Jan;73(1):17–35. doi: 10.1016/0022-2836(73)90156-3. [DOI] [PubMed] [Google Scholar]
  2. Beckendorf S. K. Structure of the distal half of the bacteriophage T4 tail fiber. J Mol Biol. 1973 Jan;73(1):37–53. doi: 10.1016/0022-2836(73)90157-5. [DOI] [PubMed] [Google Scholar]
  3. Boyer H. W., Roulland-Dussoix D. A complementation analysis of the restriction and modification of DNA in Escherichia coli. J Mol Biol. 1969 May 14;41(3):459–472. doi: 10.1016/0022-2836(69)90288-5. [DOI] [PubMed] [Google Scholar]
  4. Bremer E., Cole S. T., Hindennach I., Henning U., Beck E., Kurz C., Schaller H. Export of a protein into the outer membrane of Escherichia coli K12. Stable incorporation of the OmpA protein requires less than 193 amino-terminal amino-acid residues. Eur J Biochem. 1982 Feb;122(1):223–231. doi: 10.1111/j.1432-1033.1982.tb05870.x. [DOI] [PubMed] [Google Scholar]
  5. George D. G., Yeh L. S., Barker W. C. Unexpected relationships between bacteriophage lambda hypothetical proteins and bacteriophage T4 tail-fiber proteins. Biochem Biophys Res Commun. 1983 Sep 30;115(3):1061–1068. doi: 10.1016/s0006-291x(83)80043-6. [DOI] [PubMed] [Google Scholar]
  6. Hanahan D., Meselson M. Plasmid screening at high colony density. Gene. 1980 Jun;10(1):63–67. doi: 10.1016/0378-1119(80)90144-4. [DOI] [PubMed] [Google Scholar]
  7. Hantke K. Major outer membrane proteins of E. coli K12 serve as receptors for the phages T2 (protein Ia) and 434 (protein Ib). Mol Gen Genet. 1978 Aug 17;164(2):131–135. doi: 10.1007/BF00267377. [DOI] [PubMed] [Google Scholar]
  8. Kim J. S., Davidson N. Electron microscope heteroduplex study of sequence relations of T2, T4, and T6 bacteriophage DNAs. Virology. 1974 Jan;57(1):93–111. doi: 10.1016/0042-6822(74)90111-1. [DOI] [PubMed] [Google Scholar]
  9. Low B. Formation of merodiploids in matings with a class of Rec- recipient strains of Escherichia coli K12. Proc Natl Acad Sci U S A. 1968 May;60(1):160–167. doi: 10.1073/pnas.60.1.160. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Meselson M., Yuan R. DNA restriction enzyme from E. coli. Nature. 1968 Mar 23;217(5134):1110–1114. doi: 10.1038/2171110a0. [DOI] [PubMed] [Google Scholar]
  11. Messing J., Crea R., Seeburg P. H. A system for shotgun DNA sequencing. Nucleic Acids Res. 1981 Jan 24;9(2):309–321. doi: 10.1093/nar/9.2.309. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. 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]
  13. Morona R., Klose M., Henning U. Escherichia coli K-12 outer membrane protein (OmpA) as a bacteriophage receptor: analysis of mutant genes expressing altered proteins. J Bacteriol. 1984 Aug;159(2):570–578. doi: 10.1128/jb.159.2.570-578.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Nakamura K., Pirtle R. M., Inouye M. Homology of the gene coding for outer membrane lipoprotein within various Gram-negative bacteria. J Bacteriol. 1979 Jan;137(1):595–604. doi: 10.1128/jb.137.1.595-604.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Oliver D. B., Crowther R. A. DNA sequence of the tail fibre genes 36 and 37 of bacteriophage T4. J Mol Biol. 1981 Dec 15;153(3):545–568. doi: 10.1016/0022-2836(81)90407-1. [DOI] [PubMed] [Google Scholar]
  16. Revel H. R. Molecular cloning of the T4 genome: organization and expression of the tail fiber gene cluster 34--38. Mol Gen Genet. 1981;182(3):445–455. doi: 10.1007/BF00293934. [DOI] [PubMed] [Google Scholar]
  17. Riede I., Drexler K., Eschbach M. L. The nucleotide sequences of the tail fiber gene 36 of bacteriophage T2 and of genes 36 of the T-even type Escherichia coli phages K3 and Ox2. Nucleic Acids Res. 1985 Jan 25;13(2):605–616. doi: 10.1093/nar/13.2.605. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Riede I., Eschbach M. L., Henning U. DNA sequence heterogeneity in the genes of T-even type Escherichia coli phages encoding the receptor recognizing protein of the long tail fibers. Mol Gen Genet. 1984;195(1-2):144–152. doi: 10.1007/BF00332737. [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. Russell R. L. Comparative genetics of the T-even bacteriophages. Genetics. 1974 Dec;78(4):967–988. doi: 10.1093/genetics/78.4.967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Russell R. L., Huskey R. J. Partial exclusion between T-even bacteriophages: an incipient genetic isolation mechanism. Genetics. 1974 Dec;78(4):989–1014. doi: 10.1093/genetics/78.4.989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Rüther U., Koenen M., Otto K., Müller-Hill B. pUR222, a vector for cloning and rapid chemical sequencing of DNA. Nucleic Acids Res. 1981 Aug 25;9(16):4087–4098. doi: 10.1093/nar/9.16.4087. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. 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]
  24. Schwarz H., Riede I., Sonntag I., Henning U. Degrees of relatedness of T-even type E. coli phages using different or the same receptors and topology of serologically cross-reacting sites. EMBO J. 1983;2(3):375–380. doi: 10.1002/j.1460-2075.1983.tb01433.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Simon L. D., Anderson T. F. The infection of Escherichia coli by T2 and T4 bacteriophages as seen in the electron microscope. I. Attachment and penetration. Virology. 1967 Jun;32(2):279–297. doi: 10.1016/0042-6822(67)90277-2. [DOI] [PubMed] [Google Scholar]
  26. Singh L., Jones K. W. The use of heparin as a simple cost-effective means of controlling background in nucleic acid hybridization procedures. Nucleic Acids Res. 1984 Jul 25;12(14):5627–5638. doi: 10.1093/nar/12.14.5627. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Skurray R. A., Hancock R. E., Reeves P. Con--mutants: class of mutants in Escherichia coli K-12 lacking a major cell wall protein and defective in conjugation and adsorption of a bacteriophage. J Bacteriol. 1974 Sep;119(3):726–735. doi: 10.1128/jb.119.3.726-735.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. 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]
  29. Timmis K. N., Andrés I., Achtman M. Fertility repression of F-like conjugative plasmids: physical mapping of the R6--5 finO and finP cistrons and identification of the finO protein. Proc Natl Acad Sci U S A. 1978 Dec;75(12):5836–5840. doi: 10.1073/pnas.75.12.5836. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Vieira J., Messing J. The pUC plasmids, an M13mp7-derived system for insertion mutagenesis and sequencing with synthetic universal primers. Gene. 1982 Oct;19(3):259–268. doi: 10.1016/0378-1119(82)90015-4. [DOI] [PubMed] [Google Scholar]
  31. Wahl G. M., Stern M., Stark G. R. Efficient transfer of large DNA fragments from agarose gels to diazobenzyloxymethyl-paper and rapid hybridization by using dextran sulfate. Proc Natl Acad Sci U S A. 1979 Aug;76(8):3683–3687. doi: 10.1073/pnas.76.8.3683. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Wilson J. H., Luftig R. B., Wood W. B. Interaction of bacteriophage T4 tail fiber components with a lipopolysaccharide fraction from Escherichia coli. J Mol Biol. 1970 Jul 28;51(2):423–434. doi: 10.1016/0022-2836(70)90152-x. [DOI] [PubMed] [Google Scholar]
  33. Wood W. B., Revel H. R. The genome of bacteriophage T4. Bacteriol Rev. 1976 Dec;40(4):847–868. doi: 10.1128/br.40.4.847-868.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]

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