Skip to main content
Journal of Virology logoLink to Journal of Virology
. 1971 May;7(5):673–678. doi: 10.1128/jvi.7.5.673-678.1971

Growth Inhibition and Appearance of the Membranous Structure in Escherichia coli Infected with Bacteriophage fd

Yoshinari Ohnishi a,1, Michihiko Kuwano a
PMCID: PMC356178  PMID: 4104255

Abstract

Thirty-six mutants of fd, a virus that infects but does not kill Escherichia coli, were isolated; 35 mutants were categorized into six complementation groups. Abortive infection with mutants in genes 1, 3, 4, 5, and 6, but not in gene 2, produced a cessation of host cell growth, generally linked to low burst size and to the formation of aberrant intracytoplasmic membranous structures. The membranous structure was studied during infection with various phage and hosts. Appearance of the membranous structure was linked specifically to incomplete phage maturation at the cell membrane, rather than solely to the inhibition of host cell growth or to infection with mutant phage, since (i) in one host, cell growth was inhibited, but no membranous structure developed; and (ii) when antibody against virus was added to cells infected with wild-type phage, phage extrusion was inhibited, cell growth stopped, and the membranous structure once again developed.

Full text

PDF
673

Images in this article

Selected References

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

  1. ANAND N., DAVIS B. D. Damage by streptomycin to the cell membrane of Escherichia coli. Nature. 1960 Jan 2;185:22–23. doi: 10.1038/185022a0. [DOI] [PubMed] [Google Scholar]
  2. Bradley D. E., Dewar C. A. Intracellular changes in cells of Escherichia coli infected with a filamentous bacteriophage. J Gen Virol. 1967 Apr;1(2):179–188. doi: 10.1099/0022-1317-1-2-179. [DOI] [PubMed] [Google Scholar]
  3. Brown L. R., Dowell C. E. Replication of coliphage M-13. I. Effects on host cells after synchronized infection. J Virol. 1968 Nov;2(11):1290–1295. doi: 10.1128/jvi.2.11.1290-1295.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. DUBIN D. T., DAVIS B. D. The effect of streptomycin on potassium flux in Escherichia coli. Biochim Biophys Acta. 1961 Sep 16;52:400–402. doi: 10.1016/0006-3002(61)90697-7. [DOI] [PubMed] [Google Scholar]
  5. DUBIN D. T., HANCOCK R., DAVIS B. D. THE SEQUENCE OF SOME EFFECTS OF STREPTOMYCIN IN ESCHERICHIA COLI. Biochim Biophys Acta. 1963 Aug 13;74:476–489. doi: 10.1016/0006-3002(63)91390-8. [DOI] [PubMed] [Google Scholar]
  6. FLAKS J. G., COX E. C., WHITE J. R. Inhibition of polypeptide synthesis by streptomycin. Biochem Biophys Res Commun. 1962 May 11;7:385–389. doi: 10.1016/0006-291x(62)90320-0. [DOI] [PubMed] [Google Scholar]
  7. FREESE E., BAUTZ E., FREESE E. B. The chemical and mutagenic specificity of hydroxylamine. Proc Natl Acad Sci U S A. 1961 Jun 15;47:845–855. doi: 10.1073/pnas.47.6.845. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. HOFFMANN BERLING H., MAZE R. RELEASE OF MALE-SPECIFIC BACTERIOPHAGES FROM SURVIVING HOST BACTERIA. Virology. 1964 Mar;22:305–313. doi: 10.1016/0042-6822(64)90021-2. [DOI] [PubMed] [Google Scholar]
  9. HOFFMANN-BERLING H., DUERWALD H., BEULKE I. EIN FAEDIGER DNS-PHAGE (FD) UND EIN SPHAERISCHER RNS-PHAGE (FR) WIRTSSPEZIFISCH FUER MAENNLICHE STAEMME VON E. COLI. III. BIOLOGISCHES VERHALTEN VON FD UND FR. Z Naturforsch B. 1963 Nov;18:893–898. [PubMed] [Google Scholar]
  10. HOFSCHNEIDER P. H., PREUSS A. M 13 BACTERIOPHAGE LIBERATION FROM INTACT BACTERIA AS REVEALED BY ELECTRON MICROSCOPY. J Mol Biol. 1963 Oct;7:450–451. doi: 10.1016/s0022-2836(63)80038-8. [DOI] [PubMed] [Google Scholar]
  11. Hsu Y. C. Propagation or elimination of viral infection in carrier cells. Bacteriol Rev. 1968 Dec;32(4 Pt 1):387–399. [PMC free article] [PubMed] [Google Scholar]
  12. JACOB F., SIMINOVITCH L., WOLLMAN E. Sur la biosynthèse d'une colicine et sur son mode d'action. Ann Inst Pasteur (Paris) 1952 Sep;83(3):295–315. [PubMed] [Google Scholar]
  13. KELLENBERGER E., RYTER A., SECHAUD J. Electron microscope study of DNA-containing plasms. II. Vegetative and mature phage DNA as compared with normal bacterial nucleoids in different physiological states. J Biophys Biochem Cytol. 1958 Nov 25;4(6):671–678. doi: 10.1083/jcb.4.6.671. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. LUFT J. H. Improvements in epoxy resin embedding methods. J Biophys Biochem Cytol. 1961 Feb;9:409–414. doi: 10.1083/jcb.9.2.409. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Marvin D. A., Hohn B. Filamentous bacterial viruses. Bacteriol Rev. 1969 Jun;33(2):172–209. doi: 10.1128/br.33.2.172-209.1969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Meynell G. G., Lawn A. M. Filamentous phages specific for the I sex factor. Nature. 1968 Mar 23;217(5134):1184–1186. doi: 10.1038/2171184a0. [DOI] [PubMed] [Google Scholar]
  17. Minamishima Y., Takeya K., Ohnishi Y., Amako K. Physicochemical and biological properties of fibrous Pseudomonas bacteriophages. J Virol. 1968 Mar;2(3):208–213. doi: 10.1128/jvi.2.3.208-213.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Pratt D., Erdahl W. S. Genetic control of bacteriophage M13 DNA synthesis. J Mol Biol. 1968 Oct 14;37(1):181–200. doi: 10.1016/0022-2836(68)90082-x. [DOI] [PubMed] [Google Scholar]
  19. Pratt D., Tzagoloff H., Beaudoin J. Conditional lethal mutants of the small filamentous coliphage M13. II. Two genes for coat proteins. Virology. 1969 Sep;39(1):42–53. doi: 10.1016/0042-6822(69)90346-8. [DOI] [PubMed] [Google Scholar]
  20. Pratt D., Tzagoloff H., Erdahl W. S. Conditional lethal mutants of the small filamentous coliphage M13. I. Isolation, complementation, cell killing, time of cistron action. Virology. 1966 Nov;30(3):397–410. doi: 10.1016/0042-6822(66)90118-8. [DOI] [PubMed] [Google Scholar]
  21. SALIVAR W. O., TZAGOLOFF H., PRATT D. SOME PHYSICAL-CHEMICAL AND BIOLOGICAL PROPERTIES OF THE ROD-SHAPED COLIPHAGE M13. Virology. 1964 Nov;24:359–371. doi: 10.1016/0042-6822(64)90173-4. [DOI] [PubMed] [Google Scholar]
  22. SPEYER J. F., LENGYEL P., BASILIO C. Ribosomal localization of streptomycin sensitivity. Proc Natl Acad Sci U S A. 1962 Apr 15;48:684–686. doi: 10.1073/pnas.48.4.684. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. SPOTTS C. R., STANIER R. Y. Mechanism of streptomycin action on bacteria: a unitary hypothesis. Nature. 1961 Nov 18;192:633–637. doi: 10.1038/192633a0. [DOI] [PubMed] [Google Scholar]
  24. Schwartz F. M., Zinder N. D. Morphological changes in Escherichia coli infected with the DNA bacteriophage fl. Virology. 1968 Feb;34(2):352–355. doi: 10.1016/0042-6822(68)90246-8. [DOI] [PubMed] [Google Scholar]
  25. Sinsheimer R. L., Knippers R., Komano T. Stages in the replication of bacteriophage phi X174 DNA in vivo. Cold Spring Harb Symp Quant Biol. 1968;33:443–447. doi: 10.1101/sqb.1968.033.01.051. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Virology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES