Skip to main content
NCBI home page
Journal of Virology logoLink to Journal of Virology
. 1981 Dec;40(3):912–919. doi: 10.1128/jvi.40.3.912-919.1981

Mechanism of coliphage M13 contraction: intermediate structures trapped at low temperatures.

M Manning, S Chrysogelos, J Griffith
PMCID: PMC256702  PMID: 7321105

Abstract

The filamentous coliphage M13 can be transformed into a spherical particle (termed spheroid) by exposure to an interface of water and slightly polar but hydrophobic solvent such as chloroform-water at 24 degrees C. We report here that exposure of M13 filaments to a chloroform-water interface at 2 degrees C trapped the phage particles in forms morphologically intermediate to filaments and spheroids. These structures were rods 250 nm long and 15 nm wide, and each had a closed, slightly pointed end, an open flaired end, and a hollow central channel. The final contraction of these intermediates (termed I-forms) into spheroids was dependent upon both temperature and the presence of the solvent-water interface but was apparently independent of both the minor phage coat proteins and the virion DNA. Although stable in an aqueous environment, I-forms, in contrast to filaments, were readily disrupted by detergents, suggesting that the phage structure had been altered to a form more easily solubilized by membrane lipids. These solvent-induced changes might be related to the initial steps of phage penetration in vivo.

Full text

PDF
912

Images in this article

913Image
on p.913
914Image
on p.914
916Image
on p.916
917Image
on p.917
917Image
on p.917
918Image
on p.918

Selected References

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

  1. Amako K., Yasunaka K. Ether induced morphological alteration of Pf-1 filamentous phage. Nature. 1977 Jun 30;267(5614):862–863. doi: 10.1038/267862a0. [DOI] [PubMed] [Google Scholar]
  2. Boeke J. D., Vovis G. F., Zinder N. D. Insertion mutant of bacteriophage f1 sensitive to EcoRI. Proc Natl Acad Sci U S A. 1979 Jun;76(6):2699–2702. doi: 10.1073/pnas.76.6.2699. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Day L. A. Protein conformation in fd bacteriophage as investigated by optical rotatory dispersion. J Mol Biol. 1966 Jan;15(1):395–398. doi: 10.1016/s0022-2836(66)80239-5. [DOI] [PubMed] [Google Scholar]
  4. Goldsmith M. E., Konigsberg W. H. Adsorption protein of the bacteriophage fd: isolation, molecular properties, and location in the virus. Biochemistry. 1977 Jun 14;16(12):2686–2694. doi: 10.1021/bi00631a016. [DOI] [PubMed] [Google Scholar]
  5. Grant R. A., Lin T. C., Konigsberg W., Webster R. E. Structure of the filamentous bacteriophage fl. Location of the A, C, and D minor coat proteins. J Biol Chem. 1981 Jan 10;256(1):539–546. [PubMed] [Google Scholar]
  6. Gray C. W., Brown R. S., Marvin D. A. Adsorption complex of filamentous fd virus. J Mol Biol. 1981 Mar 15;146(4):621–627. doi: 10.1016/0022-2836(81)90050-4. [DOI] [PubMed] [Google Scholar]
  7. Griffith J. D., Christiansen G. Electron microscope visualization of chromatin and other DNA-protein complexes. Annu Rev Biophys Bioeng. 1978;7:19–35. doi: 10.1146/annurev.bb.07.060178.000315. [DOI] [PubMed] [Google Scholar]
  8. Griffith J., Kornberg A. Mini M13 bacteriophage: circular fragments of M13 DNA are replicated and packaged during normal infections. Virology. 1974 May;59(1):139–152. doi: 10.1016/0042-6822(74)90211-6. [DOI] [PubMed] [Google Scholar]
  9. Griffith J., Manning M., Dunn K. Filamentous bacteriophage contract into hollow spherical particles upon exposure to a chloroform-water interface. Cell. 1981 Mar;23(3):747–753. doi: 10.1016/0092-8674(81)90438-4. [DOI] [PubMed] [Google Scholar]
  10. Lin T. C., Webster R. E., Konigsberg W. Isolation and characterization of the C and D proteins coded by gene IX and gene VI in the filamentous bacteriophage fl and fd. J Biol Chem. 1980 Nov 10;255(21):10331–10337. [PubMed] [Google Scholar]
  11. Makowski L., Caspar D. L., Marvin D. A. Filamentous bacteriophage Pf1 structure determined at 7A resolution by refinement of models for the alpha-helical subunit. J Mol Biol. 1980 Jun 25;140(2):149–181. doi: 10.1016/0022-2836(80)90101-1. [DOI] [PubMed] [Google Scholar]
  12. Marco R., Jazwinski S. M., Kornberg A. Binding, eclipse, and penetration of the filamentous bacteriophage M13 in intact and disrupted cells. Virology. 1974 Nov;62(1):209–223. doi: 10.1016/0042-6822(74)90316-x. [DOI] [PubMed] [Google Scholar]
  13. Marvin D. A., Pigram W. J., Wiseman R. L., Wachtel E. J., Marvin F. J. Filamentous bacterial viruses. XIL. Molecular architecture of the class I (fd, If1, IKe) virion. J Mol Biol. 1974 Sep 25;88(3):581–598. doi: 10.1016/0022-2836(74)90409-4. [DOI] [PubMed] [Google Scholar]
  14. Nakashima Y., Wiseman R. L., Konigsberg W., Marvin D. A. Primary structure and sidechain interactions of PFL filamentous bacterial virus coat protein. Nature. 1975 Jan 3;253(5486):68–71. doi: 10.1038/253068a0. [DOI] [PubMed] [Google Scholar]
  15. Newman J., Swinney H. L., Day L. A. Hydrodynamic properties and structure of fd virus. J Mol Biol. 1977 Nov 5;116(3):593–603. doi: 10.1016/0022-2836(77)90086-9. [DOI] [PubMed] [Google Scholar]
  16. Nozaki Y., Chamberlain B. K., Webster R. E., Tanford C. Evidence for a major conformational change of coat protein in assembly of fl bacteriophage. Nature. 1976 Jan 29;259(5541):335–337. doi: 10.1038/259335a0. [DOI] [PubMed] [Google Scholar]
  17. Sigal N., Delius H., Kornberg T., Gefter M. L., Alberts B. A DNA-unwinding protein isolated from Escherichia coli: its interaction with DNA and with DNA polymerases. Proc Natl Acad Sci U S A. 1972 Dec;69(12):3537–3541. doi: 10.1073/pnas.69.12.3537. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Smilowitz H. Bacteriophage f1 infection: fate of the parental major coat protein. J Virol. 1974 Jan;13(1):94–99. doi: 10.1128/jvi.13.1.94-99.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. TZAGOLOFF H., PRATT D. THE INITIAL STEPS IN INFECTION WITH COLIPHAGE M13. Virology. 1964 Nov;24:372–380. doi: 10.1016/0042-6822(64)90174-6. [DOI] [PubMed] [Google Scholar]
  20. Trenkner E., Bonhoeffer F., Gierer A. The fate of the protein component of bacteriophage fd during infection. Biochem Biophys Res Commun. 1967 Sep 27;28(6):932–939. doi: 10.1016/0006-291x(67)90069-1. [DOI] [PubMed] [Google Scholar]
  21. Williams R. W., Dunker A. K. Circular dichroism studies of fd coat protein in membrane vesicles. J Biol Chem. 1977 Sep 25;252(18):6253–6255. [PubMed] [Google Scholar]
  22. Woolford J. L., Jr, Steinman H. M., Webster R. E. Adsorption protein of bacteriophage fl: solubilization in deoxycholate and localization in the fl virion. Biochemistry. 1977 Jun 14;16(12):2694–2700. doi: 10.1021/bi00631a017. [DOI] [PubMed] [Google Scholar]

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

RESOURCES