Skip to main content
NCBI home page
Genetics logoLink to Genetics
. 1994 Jul;137(3):613–625. doi: 10.1093/genetics/137.3.613

A Late Exclusion of Bacteriophage T4 Can Be Suppressed by Escherichia Coli Groel or Rho

C H Linder 1, K Carlson 1, F Albertioni 1, J Soderstrom 1, C Pahlson 1
PMCID: PMC1206021  PMID: 7916307

Abstract

A litCon mutation in Escherichia coli TU6 results in exclusion of bacteriophage T4 during the late, morphogenetic stage of its development at low temperatures. DNA was synthesized continuously in the infected cells, but less than 10% of the DNA made by 90 min after infection was packaged into DNAase-resistant particles, few viable phage were formed, and the cells lysed poorly. The exclusion could be relieved by conditions leading to elevated levels, determined immunologically, of the E. coli Rho protein (believed to be involved in regulation of T4 transcription), or chromosomally encoded E. coli GroEL (a chaperone known to be involved in phage assembly), or by supplying GroEL in trans from a plasmid. The two suppressing proteins appeared to act independently of each other. GroEL-suppression restored packaging to normal levels, perhaps by preventing GP23 from activating the host Lit protein; in addition DNA synthesis was delayed and reduced and cell lysis enhanced, demonstrating involvement of GroEL in both these processes. Rho suppression was less efficient. Since both transcription-termination-proficient and transcription-termination-deficient Rho suppressed, the results raise the possibility that Rho has a role during T4 development not directly involving transcription regulation.

Full Text

The Full Text of this article is available as a PDF (2.3 MB).

Selected References

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

  1. Bachmann B. J. Linkage map of Escherichia coli K-12, edition 8. Microbiol Rev. 1990 Jun;54(2):130–197. doi: 10.1128/mr.54.2.130-197.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Baumberg S., Lovett M. G. Reduced recovery of plasmid transconjugants in crosses with Escherichia coli rho mutant recipients. Plasmid. 1977 Nov;1(1):118–122. doi: 10.1016/0147-619x(77)90014-2. [DOI] [PubMed] [Google Scholar]
  3. Beckmann J. S., Tichauer Y., Daniel V., Littauer U. Z. Binding of the termination factor rho to DNA. Biochem Biophys Res Commun. 1971 May 21;43(4):806–813. doi: 10.1016/0006-291x(71)90688-7. [DOI] [PubMed] [Google Scholar]
  4. Bergsland K. J., Kao C., Yu Y. T., Gulati R., Snyder L. A site in the T4 bacteriophage major head protein gene that can promote the inhibition of all translation in Escherichia coli. J Mol Biol. 1990 Jun 5;213(3):477–494. doi: 10.1016/S0022-2836(05)80209-8. [DOI] [PubMed] [Google Scholar]
  5. Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. doi: 10.1016/0003-2697(76)90527-3. [DOI] [PubMed] [Google Scholar]
  6. Brennan C. A., Dombroski A. J., Platt T. Transcription termination factor rho is an RNA-DNA helicase. Cell. 1987 Mar 27;48(6):945–952. doi: 10.1016/0092-8674(87)90703-3. [DOI] [PubMed] [Google Scholar]
  7. Cardillo T. S., Landry E. F., Wiberg J. S. regA protein of bacteriophage T4D: identification, schedule of synthesis, and autogenous regulation. J Virol. 1979 Dec;32(3):905–916. doi: 10.1128/jvi.32.3.905-916.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Carlson K., Wiberg J. S. In vivo cleavage of cytosine-containing bacteriophage T4 DNA to genetically distinct, discretely sized fragments. J Virol. 1983 Oct;48(1):18–30. doi: 10.1128/jvi.48.1.18-30.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Cooley W., Sirotkin K., Green R., Synder L. A new gene of Escherichia coli K-12 whose product participates in T4 bacteriophage late gene expression: interaction of lit with the T4-induced polynucleotide 5'-kinase 3'-phosphatase. J Bacteriol. 1979 Oct;140(1):83–91. doi: 10.1128/jb.140.1.83-91.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Daegelen P., D'Aubenton-Carafa Y., Brody E. The role of rho in bacteriophage T4 development. I. Control of growth and polarity. Virology. 1982 Feb;117(1):105–120. doi: 10.1016/0042-6822(82)90511-6. [DOI] [PubMed] [Google Scholar]
  11. Daegelen P., D'Aubenton-Carafa Y., Brody E. The role of rho in bacteriophage T4 development. II. mot-dependent (middle mode) RNA synthesis. Virology. 1982 Feb;117(1):121–134. doi: 10.1016/0042-6822(82)90512-8. [DOI] [PubMed] [Google Scholar]
  12. Daniels D. L., Plunkett G., 3rd, Burland V., Blattner F. R. Analysis of the Escherichia coli genome: DNA sequence of the region from 84.5 to 86.5 minutes. Science. 1992 Aug 7;257(5071):771–778. doi: 10.1126/science.1379743. [DOI] [PubMed] [Google Scholar]
  13. Das A., Merril C., Adhya S. Interaction of RNA polymerase and rho in transcription termination: coupled ATPase. Proc Natl Acad Sci U S A. 1978 Oct;75(10):4828–4832. doi: 10.1073/pnas.75.10.4828. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Datta A. R., Rosner J. L. Reduced transposition in rho mutants of Escherichia coli K-12. J Bacteriol. 1987 Feb;169(2):888–890. doi: 10.1128/jb.169.2.888-890.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Dokland T., Isaksen M. L., Fuller S. D., Lindqvist B. H. Capsid localization of the bacteriophage P4 Psu protein. Virology. 1993 Jun;194(2):682–687. doi: 10.1006/viro.1993.1308. [DOI] [PubMed] [Google Scholar]
  16. FRASER D., JERREL E. A. The amino acid composition of T3 bacteriophage. J Biol Chem. 1953 Nov;205(1):291–295. [PubMed] [Google Scholar]
  17. Georgopoulos C. P., Hendrix R. W., Kaiser A. D., Wood W. B. Role of the host cell in bacteriophage morphogenesis: effects of a bacterial mutation on T4 head assembly. Nat New Biol. 1972 Sep 13;239(89):38–41. doi: 10.1038/newbio239038a0. [DOI] [PubMed] [Google Scholar]
  18. Gray J. E., Patin D. W., Calhoun D. H. Identification of the protein products of the rrnC, ilv, rho region of the Escherichia coli K-12 chromosome. Mol Gen Genet. 1981;183(3):428–436. doi: 10.1007/BF00268761. [DOI] [PubMed] [Google Scholar]
  19. Gulletta E., Das A., Adhya S. The pleiotropic ts15 mutation of E. coli is an IS1 insertion in the rho structural gene. Genetics. 1983 Oct;105(2):265–280. doi: 10.1093/genetics/105.2.265. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Guterman S. K., Howitt C. L. Rho and ribosome mutation interaction: lethality of rho-15 in rpsL or rpsE strains, and rho-15 methionine auxotrophy in rps+ strains of Escherichia coli. Genetics. 1979 Oct;93(2):353–360. doi: 10.1093/genetics/93.2.353. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Herendeen S. L., VanBogelen R. A., Neidhardt F. C. Levels of major proteins of Escherichia coli during growth at different temperatures. J Bacteriol. 1979 Jul;139(1):185–194. doi: 10.1128/jb.139.1.185-194.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Hill C. W., Gray J. A., Brody H. Use of the isocitrate dehydrogenase structural gene for attachment of e14 in Escherichia coli K-12. J Bacteriol. 1989 Jul;171(7):4083–4084. doi: 10.1128/jb.171.7.4083-4084.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Hinton D. M. Altered expression of the bacteriophage T4 gene 41 (primase-helicase) in an Escherichia coli rho mutant. J Biol Chem. 1989 Aug 25;264(24):14440–14446. [PubMed] [Google Scholar]
  24. Holmdahl R., Moran T., Andersson M. A rapid and efficient immunization protocol for production of monoclonal antibodies reactive with autoantigens. J Immunol Methods. 1985 Nov 7;83(2):379–384. doi: 10.1016/0022-1759(85)90260-1. [DOI] [PubMed] [Google Scholar]
  25. Horwich A. L., Neupert W., Hartl F. U. Protein-catalysed protein folding. Trends Biotechnol. 1990 May;8(5):126–131. doi: 10.1016/0167-7799(90)90153-o. [DOI] [PubMed] [Google Scholar]
  26. Isaksen M. L., Rishovd S. T., Calendar R., Lindqvist B. H. The polarity suppression factor of bacteriophage P4 is also a decoration protein of the P4 capsid. Virology. 1992 Jun;188(2):831–839. doi: 10.1016/0042-6822(92)90538-z. [DOI] [PubMed] [Google Scholar]
  27. Jayaraman R. Transcription of bacteriophage T4 DNA by Escherichia coli RNA polymerase in vitro: identification of some immediate-early and delayed-early genes. J Mol Biol. 1972 Sep 28;70(2):253–263. doi: 10.1016/0022-2836(72)90537-2. [DOI] [PubMed] [Google Scholar]
  28. Josslin R. Physiological studies on the t gene defect in T4-infected Escherichia coli. Virology. 1971 Apr;44(1):101–107. doi: 10.1016/0042-6822(71)90157-7. [DOI] [PubMed] [Google Scholar]
  29. Josslin R. The lysis mechanism of phage T4: mutants affecting lysis. Virology. 1970 Mar;40(3):719–726. doi: 10.1016/0042-6822(70)90216-3. [DOI] [PubMed] [Google Scholar]
  30. Kass L. R. The antibacterial activity of 3-decynoyl-n-acetylcysteamine. Inhibition in vivo of beta-hydroxydecanoyl thioester dehydrase. J Biol Chem. 1968 Jun 25;243(12):3223–3228. [PubMed] [Google Scholar]
  31. Korn L. J., Yanofsky C. Polarity suppressors increase expression of the wild-type tryptophan operon of Escherichia coli. J Mol Biol. 1976 May 15;103(2):395–409. doi: 10.1016/0022-2836(76)90319-3. [DOI] [PubMed] [Google Scholar]
  32. Kumamoto C. A. Molecular chaperones and protein translocation across the Escherichia coli inner membrane. Mol Microbiol. 1991 Jan;5(1):19–22. doi: 10.1111/j.1365-2958.1991.tb01821.x. [DOI] [PubMed] [Google Scholar]
  33. Kusukawa N., Yura T. Heat shock protein GroE of Escherichia coli: key protective roles against thermal stress. Genes Dev. 1988 Jul;2(7):874–882. doi: 10.1101/gad.2.7.874. [DOI] [PubMed] [Google Scholar]
  34. Köhler G., Milstein C. Continuous cultures of fused cells secreting antibody of predefined specificity. Nature. 1975 Aug 7;256(5517):495–497. doi: 10.1038/256495a0. [DOI] [PubMed] [Google Scholar]
  35. Linder C. H., Sköld O. Control of early gene expression of bacteriophage T4: involvement of the host rho factor and the mot gene of the bacteriophage. J Virol. 1980 Feb;33(2):724–732. doi: 10.1128/jvi.33.2.724-732.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Linderoth N. A., Calendar R. L. The Psu protein of bacteriophage P4 is an antitermination factor for rho-dependent transcription termination. J Bacteriol. 1991 Nov;173(21):6722–6731. doi: 10.1128/jb.173.21.6722-6731.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Raleigh E. A., Trimarchi R., Revel H. Genetic and physical mapping of the mcrA (rglA) and mcrB (rglB) loci of Escherichia coli K-12. Genetics. 1989 Jun;122(2):279–296. doi: 10.1093/genetics/122.2.279. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Richardson J. P. Activation of rho protein ATPase requires simultaneous interaction at two kinds of nucleic acid-binding sites. J Biol Chem. 1982 May 25;257(10):5760–5766. [PubMed] [Google Scholar]
  39. Russel M., Model P. Characterization of the cloned fip gene and its product. J Bacteriol. 1984 Feb;157(2):526–532. doi: 10.1128/jb.157.2.526-532.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Shigesada K., Tsurushita N., Matsumoto Y., Imai M. Overproduction of transcription termination factor Rho in Escherichia coli. Gene. 1984 Jul-Aug;29(1-2):199–209. doi: 10.1016/0378-1119(84)90180-x. [DOI] [PubMed] [Google Scholar]
  41. Simons R. W., Egan P. A., Chute H. T., Nunn W. D. Regulation of fatty acid degradation in Escherichia coli: isolation and characterization of strains bearing insertion and temperature-sensitive mutations in gene fadR. J Bacteriol. 1980 May;142(2):621–632. doi: 10.1128/jb.142.2.621-632.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Sinensky M. Temperature control of phospholipid biosynthesis in Escherichia coli. J Bacteriol. 1971 May;106(2):449–455. doi: 10.1128/jb.106.2.449-455.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Singer M., Baker T. A., Schnitzler G., Deischel S. M., Goel M., Dove W., Jaacks K. J., Grossman A. D., Erickson J. W., Gross C. A. A collection of strains containing genetically linked alternating antibiotic resistance elements for genetic mapping of Escherichia coli. Microbiol Rev. 1989 Mar;53(1):1–24. doi: 10.1128/mr.53.1.1-24.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Stitt B. L., Revel H. R., Lielausis I., Wood W. B. Role of the host cell in bacteriophage T4 development. II. Characterization of host mutants that have pleiotropic effects on T4 growth. J Virol. 1980 Sep;35(3):775–789. doi: 10.1128/jvi.35.3.775-789.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Wiberg J. S., Mowrey-McKee M. F., Stevens E. J. Induction of the heat shock regulon of Escherichia coli markedly increases production of bacterial viruses at high temperatures. J Virol. 1988 Jan;62(1):234–245. doi: 10.1128/jvi.62.1.234-245.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Wilson G. G., Young K. Y., Edlin G. J., Konigsberg W. High-frequency generalised transduction by bacteriophage T4. Nature. 1979 Jul 5;280(5717):80–82. doi: 10.1038/280080a0. [DOI] [PubMed] [Google Scholar]
  47. 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]
  48. Yung B. Y., Kornberg A. Membrane attachment activates dnaA protein, the initiation protein of chromosome replication in Escherichia coli. Proc Natl Acad Sci U S A. 1988 Oct;85(19):7202–7205. doi: 10.1073/pnas.85.19.7202. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Zhou Y. N., Kusukawa N., Erickson J. W., Gross C. A., Yura T. Isolation and characterization of Escherichia coli mutants that lack the heat shock sigma factor sigma 32. J Bacteriol. 1988 Aug;170(8):3640–3649. doi: 10.1128/jb.170.8.3640-3649.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Zograff Y. N., Gintsburg A. L. Transcription termination factor rho and T-even phage development. Mol Gen Genet. 1980;177(4):699–705. doi: 10.1007/BF00272682. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES