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. 1971 Dec;8(6):869–886. doi: 10.1128/jvi.8.6.869-886.1971

Breakdown and Exclusion of Superinfecting T-Even Bacteriophage in Escherichia coli

Carl W Anderson 1,1, Joseph Eigner 1
PMCID: PMC376278  PMID: 4950690

Abstract

In bacterial strains containing the deoxyribonuclease endonuclease I (endonuclease I+ strains), 70 to 80% of the injected superinfecting T-even phage deoxyribonucleic acid (DNA) is rapidly degraded to oligonucleotides having an average chain length of 8, the same value as that obtained by endonuclease I digestion of purified T-even phage DNA in vitro. In endonuclease I− strains, less than 5% of the injected superinfecting T-even phage DNA is degraded to acid-soluble components. The superinfecting phage DNA is, however, fragmented into a large segment having a molecular weight of about 90 × 106 and 30 or more small acid-insoluble segments having molecular weights of less than 106. In both endonuclease I+ and endonuclease I− strains, over 80% of the DNA from adsorbed primary T2 or T4 phage, but only 50% of the DNA from adsorbed superinfecting T2 or T4 phage, is injected. Superinfecting T4 are genetically excluded as efficiently from endonuclease I− strains as they are from endonuclease I+ strains. The excluded phage cannot complement defects in either early or late gene functions carried by the primary phage. The induction of both superinfection breakdown and superinfection exclusion requires a period of protein synthesis between primary infection and addition of the superinfecting phage. These observations seem best explained by failure of superinfecting DNA to enter the host cell cytoplasm, presumably as a result of changes in the cell envelope induced by the primary phage.

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Selected References

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

  1. Anderson C. W., Williamson J. R., Eigner J. Localization of parental deoxyribonucleic acid from superinfecting T4 bacteriophage in Escherichia coli. J Virol. 1971 Dec;8(6):887–893. doi: 10.1128/jvi.8.6.887-893.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Anderson E. H. Growth Requirements of Virus-Resistant Mutants of Escherichia Coli Strain "B". Proc Natl Acad Sci U S A. 1946 May;32(5):120–128. doi: 10.1073/pnas.32.5.120. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. BURGI E., HERSHEY A. D. Sedimentation rate as a measure of molecular weight of DNA. Biophys J. 1963 Jul;3:309–321. doi: 10.1016/s0006-3495(63)86823-x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bose S. K., Warren R. J. Bacteriophage-induced inhibition of host functions. II. Evidence for multiple, sequential bacteriophage-induced deoxyribonucleases responsible for degradation of cellular deoxyribonucleic acid. J Virol. 1969 Jun;3(6):549–556. doi: 10.1128/jvi.3.6.549-556.1969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bremer H., Yuan D. Chain growth rate of messenger RNA in Escherichia coli infected with bacteriophage T4. J Mol Biol. 1968 Jun 28;34(3):527–540. doi: 10.1016/0022-2836(68)90178-2. [DOI] [PubMed] [Google Scholar]
  6. Cordonnier C., Bernardi G. Localization of E. coli endonuclease I. Biochem Biophys Res Commun. 1965 Sep 8;20(5):555–559. doi: 10.1016/0006-291x(65)90434-1. [DOI] [PubMed] [Google Scholar]
  7. Cronan J. E., Jr, Wulff D. L. A role for phospholipid hydrolysis in the lysis of Escherichia coli infected with bacteriophage T4. Virology. 1969 Jun;38(2):241–246. doi: 10.1016/0042-6822(69)90365-1. [DOI] [PubMed] [Google Scholar]
  8. DULBECCO R. Mutual exclusion between related phages. J Bacteriol. 1952 Feb;63(2):209–217. doi: 10.1128/jb.63.2.209-217.1952. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Duckworth D. H. Biological activity of bacteriophage ghosts and "take-over" of host functions by bacteriophage. Bacteriol Rev. 1970 Sep;34(3):344–363. doi: 10.1128/br.34.3.344-363.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. EDGAR R. S., STEINBERG C. M. On the origin of high negative interference over short segments of the genetic structure of bacteriophage T4. Virology. 1958 Aug;6(1):115–128. doi: 10.1016/0042-6822(58)90063-1. [DOI] [PubMed] [Google Scholar]
  11. Earhart C. F. The association of host and phage DNA with the membrane of Escherichia coli. Virology. 1970 Oct;42(2):420–436. [PubMed] [Google Scholar]
  12. Eigner J., Block S. Host-controlled restriction of T-even bacteriophages: relation of four bacterial deoxyribonucleases to restriction. J Virol. 1968 Apr;2(4):320–326. doi: 10.1128/jvi.2.4.320-326.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Emrich J. Lysis of T4-infected bacteria in the absence of lysozyme. Virology. 1968 May;35(1):158–165. doi: 10.1016/0042-6822(68)90315-2. [DOI] [PubMed] [Google Scholar]
  14. Fielding P. E., Lunt M. R. The relation between breakdown of superinfecting virus deoxyribonucleic acid and temporal exclusion induced by T4 and T5 bacteriophages. J Gen Virol. 1970 Mar;6(3):333–342. doi: 10.1099/0022-1317-6-3-333. [DOI] [PubMed] [Google Scholar]
  15. Frankel F. R., Majumdar C., Weintraub S., Frankel D. M. DNA polymerase and the cell membrane after T4 infection. Cold Spring Harb Symp Quant Biol. 1968;33:495–500. doi: 10.1101/sqb.1968.033.01.057. [DOI] [PubMed] [Google Scholar]
  16. Frankel F. R. The absence of mature phage DNA molecules from the replicating pool of T-even-infected Escherichia coli. J Mol Biol. 1966 Jun;18(1):109–126. doi: 10.1016/s0022-2836(66)80080-3. [DOI] [PubMed] [Google Scholar]
  17. GRAHAM A. F. The fate of the infecting phage particle. Ann Inst Pasteur (Paris) 1953 Jan;84(1):90–98. [PubMed] [Google Scholar]
  18. HERSHEY A. D., CHASE M. Independent functions of viral protein and nucleic acid in growth of bacteriophage. J Gen Physiol. 1952 May;36(1):39–56. doi: 10.1085/jgp.36.1.39. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hattman S., Revel H. R., Luria S. E. Enzyme synthesis directed by nonglucosylated T-even bacteriophages in restrictive hosts. Virology. 1966 Nov;30(3):427–438. doi: 10.1016/0042-6822(66)90120-6. [DOI] [PubMed] [Google Scholar]
  20. Israeli M., Artman M. Leakage of beta-galactosidase from phage-infected Escherichia coli: a re-evaluation. J Gen Virol. 1970;7(2):137–142. doi: 10.1099/0022-1317-7-2-137. [DOI] [PubMed] [Google Scholar]
  21. KOZINSKI A. W., SZYBALSKI W. Dispersive transfer of the parental DNA molecule to the progeny of phage phiX-174. Virology. 1959 Oct;9:260–274. doi: 10.1016/0042-6822(59)90119-9. [DOI] [PubMed] [Google Scholar]
  22. KOZLOFF L. M. Origin and fate of bacteriophage material. Cold Spring Harb Symp Quant Biol. 1953;18:209–220. doi: 10.1101/sqb.1953.018.01.032. [DOI] [PubMed] [Google Scholar]
  23. KUNKEE R. E., PARDEE A. B. Studies on the role of deoxyribonuclease in T2 bacteriophage development. Biochim Biophys Acta. 1956 Feb;19(2):236–246. doi: 10.1016/0006-3002(56)90424-3. [DOI] [PubMed] [Google Scholar]
  24. Kozinski A. W. Molecular recombination in the ligase negative T4 amber mutant. Cold Spring Harb Symp Quant Biol. 1968;33:375–391. doi: 10.1101/sqb.1968.033.01.044. [DOI] [PubMed] [Google Scholar]
  25. LEHMAN I. R., ROUSSOS G. G., PRATT E. A. The deoxyribonucleases of Escherichia coli. II. Purification and properties of a ribonucleic acid-inhibitable endonuclease. J Biol Chem. 1962 Mar;237:819–828. [PubMed] [Google Scholar]
  26. LESLEY S. M., FRENCH R. C., GRAHAM A. F. Breakdown of infecting coliphage by the host cell. Arch Biochem. 1950 Aug;28(1):149–150. [PubMed] [Google Scholar]
  27. LESLEY S. M., FRENCH R. C., GRAHAM A. F., van ROOYEN C. E. Studies on the relationship between virus and host cell. II. The breakdown of T2r+ bacteriophage upon infection of its host Escherichia coli. Can J Med Sci. 1951 Jun;29(3):128–143. doi: 10.1139/cjms51-017. [DOI] [PubMed] [Google Scholar]
  28. Miller R. C., Jr, Kozinski A. W. Early intracellular events in the replication of bacteriophage T4 deoxyribonucleic acid. V. Further studies on the T4 protein-deoxyribonucleic acid complex. J Virol. 1970 Apr;5(4):490–501. doi: 10.1128/jvi.5.4.490-501.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Nossal N. G., Heppel L. A. The release of enzymes by osmotic shock from Escherichia coli in exponential phase. J Biol Chem. 1966 Jul 10;241(13):3055–3062. [PubMed] [Google Scholar]
  30. PUCK T. T., LEE H. H. Mechanism of cell wall penetration by viruses. II. Demonstration of cyclic permeability change accompanying virus infection of Escherichia coli B cells. J Exp Med. 1955 Feb 1;101(2):151–175. doi: 10.1084/jem.101.2.151. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. STONE A. B., BURTON K. Studies on the deoxyribonucleases of bacteriophage-infected Escherichia coli. Biochem J. 1962 Dec;85:600–606. doi: 10.1042/bj0850600. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Sauri C. J., Earhart C. F. Superinfection with bacteriophage T4: inverse relationship between genetic exclusion and membrane association of deoxyribonucleic acid of secondary bacteriophage. J Virol. 1971 Dec;8(6):856–859. doi: 10.1128/jvi.8.6.856-859.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Silver S. Acridine sensitivity of bacteriophage T2: a virus gene affecting cell permeability. J Mol Biol. 1967 Oct 14;29(1):191–202. doi: 10.1016/0022-2836(67)90190-8. [DOI] [PubMed] [Google Scholar]
  34. Snustad D. P. Limited genome expression in bacteriophage T4-infected Escherichia coli. I. Demonstration of the effect. Genetics. 1966 Oct;54(4):923–935. doi: 10.1093/genetics/54.4.923. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Snustad D. P. Site- and gene-specific limited heterocatalytic expression in bacteriophage T4-infected Escherichia coli. J Virol. 1969 May;3(5):533–535. doi: 10.1128/jvi.3.5.533-535.1969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Visconti N., Garen A. Unity of the Vegetative Pool in Phage-Infected Bacteria. Proc Natl Acad Sci U S A. 1953 Jul;39(7):620–627. doi: 10.1073/pnas.39.7.620. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. WATSON J. D. The properties of x-ray inactivated bacteriophage. I. Inactivation by direct effect. J Bacteriol. 1950 Dec;60(6):697–718. doi: 10.1128/jb.60.6.697-718.1950. [DOI] [PMC free article] [PubMed] [Google Scholar]

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