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. 1987 Jul;169(7):2956–2961. doi: 10.1128/jb.169.7.2956-2961.1987

Lysis gene t of T-even bacteriophages: evidence that colicins and bacteriophage genes have common ancestors.

I Riede
PMCID: PMC212333  PMID: 3597316

Abstract

The lysis gene t of the T-even-like bacteriophage K3 has been cloned and sequenced. The gene codes for a protein with a predicted molecular weight of 25,200. Expression of the complete lysis protein was impossible, but peptides complementing T4 amber mutants in t are described. No known lysis protein of other phages is homologous to protein T. Also, the Escherichia coli phospholipase A is different from protein T. CelB, the lysis protein of the colicin E2 operon, shows a similarity to protein T. Sequences of colicins A, E1, and E2 are related to gene 38 sequences, the gene preceding t and coding for the phage adhesin. A common origin for colicin genes and phage genes is discussed, and a protein region in colicins that is responsible for receptor recognition is predicted.

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Selected References

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  1. Achtman M., Willetts N., Clark A. J. Beginning a genetic analysis of conjugational transfer determined by the F factor in Escherichia coli by isolation and characterization of transfer-deficient mutants. J Bacteriol. 1971 May;106(2):529–538. doi: 10.1128/jb.106.2.529-538.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Altman E., Young K., Garrett J., Altman R., Young R. Subcellular localization of lethal lysis proteins of bacteriophages lambda and phiX174. J Virol. 1985 Mar;53(3):1008–1011. doi: 10.1128/jvi.53.3.1008-1011.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Barrell B. G., Air G. M., Hutchison C. A., 3rd Overlapping genes in bacteriophage phiX174. Nature. 1976 Nov 4;264(5581):34–41. doi: 10.1038/264034a0. [DOI] [PubMed] [Google Scholar]
  4. Bienkowska-Szewczyk K., Lipinska B., Taylor A. The R gene product of bacteriophage lambda is the murein transglycosylase. Mol Gen Genet. 1981;184(1):111–114. doi: 10.1007/BF00271205. [DOI] [PubMed] [Google Scholar]
  5. Bradley D. E. Ultrastructure of bacteriophage and bacteriocins. Bacteriol Rev. 1967 Dec;31(4):230–314. doi: 10.1128/br.31.4.230-314.1967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Buckley K. J., Hayashi M. Lytic activity localized to membrane-spanning region of phi X174 E protein. Mol Gen Genet. 1986 Jul;204(1):120–125. doi: 10.1007/BF00330198. [DOI] [PubMed] [Google Scholar]
  7. Cole S. T., Saint-Joanis B., Pugsley A. P. Molecular characterisation of the colicin E2 operon and identification of its products. Mol Gen Genet. 1985;198(3):465–472. doi: 10.1007/BF00332940. [DOI] [PubMed] [Google Scholar]
  8. Cramer W. A., Dankert J. R., Uratani Y. The membrane channel-forming bacteriocidal protein, colicin El. Biochim Biophys Acta. 1983 Mar 21;737(1):173–193. doi: 10.1016/0304-4157(83)90016-3. [DOI] [PubMed] [Google Scholar]
  9. Dayhoff M. O., Barker W. C., Hunt L. T. Establishing homologies in protein sequences. Methods Enzymol. 1983;91:524–545. doi: 10.1016/s0076-6879(83)91049-2. [DOI] [PubMed] [Google Scholar]
  10. Deininger P. L. Random subcloning of sonicated DNA: application to shotgun DNA sequence analysis. Anal Biochem. 1983 Feb 15;129(1):216–223. doi: 10.1016/0003-2697(83)90072-6. [DOI] [PubMed] [Google Scholar]
  11. Devereux J., Haeberli P., Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. doi: 10.1093/nar/12.1part1.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Garrett J. M., Young R. Lethal action of bacteriophage lambda S gene. J Virol. 1982 Dec;44(3):886–892. doi: 10.1128/jvi.44.3.886-892.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Grunstein M., Hogness D. S. Colony hybridization: a method for the isolation of cloned DNAs that contain a specific gene. Proc Natl Acad Sci U S A. 1975 Oct;72(10):3961–3965. doi: 10.1073/pnas.72.10.3961. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hutchison C. A., 3rd, Sinsheimer R. L. The process of infection with bacteriophage phi-X174. X. Mutations in a phi-X Lysis gene. J Mol Biol. 1966 Jul;18(3):429–447. doi: 10.1016/s0022-2836(66)80035-9. [DOI] [PubMed] [Google Scholar]
  15. Ito S., Nishimune T., Abe M., Kimoto M., Hayashi R. Bacteriocinlike killing action of a temperate bacteriophage phiBA1 of Bacillus aneurinolyticus. J Virol. 1986 Jul;59(1):103–111. doi: 10.1128/jvi.59.1.103-111.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. 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]
  17. 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]
  18. Mock M., Pugsley A. P. The BtuB group col plasmids and homology between the colicins they encode. J Bacteriol. 1982 Jun;150(3):1069–1076. doi: 10.1128/jb.150.3.1069-1076.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Morlon J., Lloubès R., Varenne S., Chartier M., Lazdunski C. Complete nucleotide sequence of the structural gene for colicin A, a gene translated at non-uniform rate. J Mol Biol. 1983 Oct 25;170(2):271–285. doi: 10.1016/s0022-2836(83)80148-x. [DOI] [PubMed] [Google Scholar]
  20. Nelson E. T., Buller C. S. Phospholipase activity in bacteriophage-infected Escherichia coli. I. Demonstration of a T4 bacteriophage-associated phospholipase. J Virol. 1974 Sep;14(3):479–484. doi: 10.1128/jvi.14.3.479-484.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Ohno-Iwashita Y., Imahori K. Assignment of the functional loci in colicin E2 and E3 molecules by the characterization of their proteolytic fragments. Biochemistry. 1980 Feb 19;19(4):652–659. doi: 10.1021/bi00545a008. [DOI] [PubMed] [Google Scholar]
  22. Ohno-Iwashita Y., Imahori K. Assignment of the functional loci in the colicin E1 molecule by characterization of its proteolytic fragments. J Biol Chem. 1982 Jun 10;257(11):6446–6451. [PubMed] [Google Scholar]
  23. Owen J. E., Schultz D. W., Taylor A., Smith G. R. Nucleotide sequence of the lysozyme gene of bacteriophage T4. Analysis of mutations involving repeated sequences. J Mol Biol. 1983 Apr 5;165(2):229–248. doi: 10.1016/s0022-2836(83)80255-1. [DOI] [PubMed] [Google Scholar]
  24. Pugsley A. P., Rosenbusch J. P. Release of colicin E2 from Escherichia coli. J Bacteriol. 1981 Jul;147(1):186–192. doi: 10.1128/jb.147.1.186-192.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Pugsley A. P., Schwartz M. Colicin E2 release: lysis, leakage or secretion? Possible role of a phospholipase. EMBO J. 1984 Oct;3(10):2393–2397. doi: 10.1002/j.1460-2075.1984.tb02145.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Pugsley A. P. The ins and outs of colicins. Part I: Production, and translocation across membranes. Microbiol Sci. 1984 Oct;1(7):168–175. [PubMed] [Google Scholar]
  27. Rennell D., Poteete A. R. Phage P22 lysis genes: nucleotide sequences and functional relationships with T4 and lambda genes. Virology. 1985 May;143(1):280–289. doi: 10.1016/0042-6822(85)90115-1. [DOI] [PubMed] [Google Scholar]
  28. 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]
  29. Riede I., Drexler K., Eschbach M. L., Henning U. DNA sequence of genes 38 encoding a receptor-recognizing protein of bacteriophages T2, K3 and of K3 host range mutants. J Mol Biol. 1987 Mar 5;194(1):31–39. doi: 10.1016/0022-2836(87)90713-3. [DOI] [PubMed] [Google Scholar]
  30. Riede I., Drexler K., Schwarz H., Henning U. T-even-type bacteriophages use an adhesin for recognition of cellular receptors. J Mol Biol. 1987 Mar 5;194(1):23–30. doi: 10.1016/0022-2836(87)90712-1. [DOI] [PubMed] [Google Scholar]
  31. Riede I., Eschbach M. L. Evidence that TraT interacts with OmpA of Escherichia coli. FEBS Lett. 1986 Sep 15;205(2):241–245. doi: 10.1016/0014-5793(86)80905-x. [DOI] [PubMed] [Google Scholar]
  32. 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]
  33. 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]
  34. Sanger F., Coulson A. R., Hong G. F., Hill D. F., Petersen G. B. Nucleotide sequence of bacteriophage lambda DNA. J Mol Biol. 1982 Dec 25;162(4):729–773. doi: 10.1016/0022-2836(82)90546-0. [DOI] [PubMed] [Google Scholar]
  35. 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]
  36. Schaller K., Nomura M. Colicin E2 is DNA endonuclease. Proc Natl Acad Sci U S A. 1976 Nov;73(11):3989–3993. doi: 10.1073/pnas.73.11.3989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. 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]
  38. 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]
  39. 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]
  40. Waleh N. S., Johnson P. H. Structural and functional organization of the colicin E1 operon. Proc Natl Acad Sci U S A. 1985 Dec;82(24):8389–8393. doi: 10.1073/pnas.82.24.8389. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Yamada M., Ebina Y., Miyata T., Nakazawa T., Nakazawa A. Nucleotide sequence of the structural gene for colicin E1 and predicted structure of the protein. Proc Natl Acad Sci U S A. 1982 May;79(9):2827–2831. doi: 10.1073/pnas.79.9.2827. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Yanisch-Perron C., Vieira J., Messing J. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene. 1985;33(1):103–119. doi: 10.1016/0378-1119(85)90120-9. [DOI] [PubMed] [Google Scholar]
  43. Young K. D., Young R. Lytic action of cloned phi X174 gene E. J Virol. 1982 Dec;44(3):993–1002. doi: 10.1128/jvi.44.3.993-1002.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Young R., Way J., Way S., Yin J., Syvanen M. Transposition mutagenesis of bacteriophage lambda: a new gene affecting cell lysis. J Mol Biol. 1979 Aug 15;132(3):307–322. doi: 10.1016/0022-2836(79)90262-6. [DOI] [PubMed] [Google Scholar]
  45. de Geus P., Verheij H. M., Riegman N. H., Hoekstra W. P., de Haas G. H. The pro- and mature forms of the E. coli K-12 outer membrane phospholipase A are identical. EMBO J. 1984 Aug;3(8):1799–1802. doi: 10.1002/j.1460-2075.1984.tb02048.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

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