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Dynamics of PhiX174 protein E-mediated lysis of Escherichia coli

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Abstract

Expression of cloned gene E of bacteriophage PhiX174 induces lysis by formation of a transmembrane tunnel structure in the cell envelope of Escherichia coli. Ultrastructural studies of the location of the lysis tunnel indicate that it is preferentially located at the septum or at polar regions of the cell. Furthermore, the diameter and shape of individual tunnel structures vary greatly indicating that its structure is not rigid. Apparently, the contours of individual lysis tunnels are determined by enlarged meshes in the peptidoglycan net and the force produced at its orifice, by the outflow of cytoplasmic content. Once the tunnel is formed the driving force for the lysis process is the osmotic pressure difference between cytoplasm and medium. During the lysis process areas of the cytoplasmic membrane which are not tightly attached to the envelope are extended inward by the negative pressure produced during lysis. After cell lysis external medium can diffuse through the lysis tunnel filling the inner cell space of the still rigid bacterial ghosts.

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References

  • Altman E, Young KD, Garret J, Altman R, Young R (1985) Subcellular location of lethal lysis proteins of bacteriophages lambda and PhiX174. J Virol 53: 1008–1011

    Google Scholar 

  • Barrel BG, Air GM, Hutchison III CA (1976) Overlapping genes in bacteriophage PhiX174. Nature 264: 34–41

    Google Scholar 

  • Bayer ME (1968) Areas of adhesion between wall and membrane of Escherichia coli. J Gen Microbiol 53: 395–404

    Google Scholar 

  • Bläsi U, Geisen R, Lubitz W, Henrich B, Plapp R (1983) Localization of the bacteriophage PhiX174 lysis gene product in the cell envelope of Escherichia coli. In: Hakenbeck R, Höltje JV, Labischinski H (eds) Target of penicillin. de Gruyter, Berlin New York, pp 205–210

    Google Scholar 

  • Bläsi U, Halfmann G, Lubitz W (1984) Induction of autolysis of Escherichia coli by PhiX174 gene E product. In: Nombela C (ed) Microbial cell wall synthesis and autolysis. Elsevier, Amsterdam New York, pp 213–218

    Google Scholar 

  • Bläsi U, Henrich B, Lubitz W (1985) Lysis of Escherichia coli by cloned PhiX174 gene E depends on its expression. J Gen Microbiol 131: 1007–1114

    Google Scholar 

  • Bläsi U, Young R, Lubitz W (1988) Evaluation of the interaction of PhiX174 gene products E and K in E-mediated lysis of Escherichia coli. J Virol 62: 4362–4364

    Google Scholar 

  • Bläsi U, Linke RP, Lubitz W (1989) Evidence for membrane-bound oligomerization of bacterophage PhiX174 lysis protein E. J Biol Chem 264: 4552–4558

    Google Scholar 

  • Cook WR, MacAlister TJ, Rothfield LI (1986) Compartimentalization of the periplasmic space at division sites in Gram-negative bacteria. J Bacteriol 168: 1430–1438

    Google Scholar 

  • Costerton JW, Ingram JM, Cheng KJ (1974) Structure and function of the cell envelope of Gram-negative bacteria. Bacteriol Rev 38: 87–110

    Google Scholar 

  • deBoer PAJ, Cook WR, Rothfield LI (1990) Bacterial cell division. Ann Rev Genet 24: 249–274

    Google Scholar 

  • Eigner J, Stouthamer AH, Van derSluys J, Cohen JA (1963) A study of the 70S component of bacteriophage PhiX174. J Mol Biol 6: 61–84

    Google Scholar 

  • Fillingme RH, Foster DL (1986) Purification of F1F0H+-ATPase from Escherichia coli. Methods Enzymol 126: 545–557

    Google Scholar 

  • Garrett J, Fusselman R, Hise J, Chio L, Smith-Grillo D, Schulz J, Young R (1981) Cell lysis by induction of cloned Lambda lysis genes. Mol Gen Genet 181: 326–331

    Google Scholar 

  • Halfmann G, Leduc M, Lubitz W (1984) Different sensitivity of autolytic deficient Escherichia coli mutants to the mode of induction. FEMS Microbiol Lett 24: 205–208

    Google Scholar 

  • Halfmann G, Lubitz W (1986) Different induction of Escherichia coli autolysis by penicillin and the bacteriophage PhiX174 gene E product. J Bacteriol 66: 683–685

    Google Scholar 

  • Henrich B, Lubitz W, Plapp R (1982) Lysis of Escherichia coli by induction of cloned PhiX174 genes. Mol Gen Genet 185: 493–497

    Google Scholar 

  • Hutchison III CA, Sinsheimer RL (1963) Kinetics of bacteriophage release by single cells of PhiX174-infected E. coli. J Mol Biol 7: 206–208

    Google Scholar 

  • Hutchison III CA, Sinsheimer RL (1966) The process of infection with bacteriophage PhiX174. Mutations in a PhiX174 lysis gene. J Mol Biol 18: 429–447

    Google Scholar 

  • Kellenberger E (1990) The ‘Bayer bridges’ confrontated with results from improved electron microscopy methods. Mol Microbiol 4: 697–705

    Google Scholar 

  • Lubitz W, Plapp R (1980) Murein degradation in Escherichia coli infected with bacteriophage PhiX174. Curr Microbiol 4: 301–304

    Google Scholar 

  • Lubitz W, Halfmann G, Plapp R (1984a) Lysis of Escherichia coli after infection with PhiX174 depends on the regulation of the cellular autolytic system. J Gen Microbiol 130: 1079–1087

    Google Scholar 

  • Lubitz W, Harkness RE, Ishiguro EE (1984b) Requirement for a functional host cell autolytic system for lysis of Escherichia coli by bacteriophage PhiX174. J Bacteriol 159: 385–387

    Google Scholar 

  • Lubitz W, Pugsley AP (1985) Changes in cell phospholipid composition of PhiX174 gene E product. FEMS Microbiol Lett 30: 171–175

    Google Scholar 

  • Lutkenhaus JF, Wolf-Watz H, Donachie WD (1980) Organization of genes in the ftsA-envA region of the Escherichia coli genetic map and identification of a new fts locus (ftsZ). J Bacteriol 142: 615–620

    Google Scholar 

  • Lutkenhaus J (1990) Regulation of cell division in E. coli. Trends Genet 6: 22–25

    Google Scholar 

  • MacAlister TJ, MacDonald B, Rothfield LI (1983) The periseptal annulus: an organelle associated with cell division in Gramnegative bateria. Proc Natl Acad Sci USA 80: (1372–1376)

    Google Scholar 

  • MacAlister TJ, Coo WR, Weigand R, Rothfield LI (1987) Membrane-murein attachment at the leading edge of the division septum: a second membrane-murein structure associated with morphogenesis of the Gram-negative bacterial division septum. J Bacteriol 169: 3945–3951

    Google Scholar 

  • Markert A, Zillig W (1965) Studies on the lysis of Escherichia coli by bacteriophage PhiX174. Virology 25: 88–97

    Google Scholar 

  • Müller M, Blobel G (1984) In vitro translocation of bacterial proteins across the plasma membrane of Escherichia coli. Proc Natl Acad Sci USA 81: 7421–7425

    Google Scholar 

  • Osborn MJ, Munson R (1974) Separation of the inner (cytoplasmic) and outer membranes of gram negative bacteria. Methods Enzymol 31A: 642–653

    Google Scholar 

  • Remaut E, Tsao H, Fiers W (1983) Improved plasmid vectors with a thermoinducible expression and temperature regulated runaway replication. Gene 22: 103–113

    Google Scholar 

  • Robin A, Joseleau-Petit D, D'Ari R (1990) Transcription of the ftsZ gene and cell division in Escherichia coli. J Bacteriol 172: 1392–1399

    Google Scholar 

  • Rottenberg H (1979) The measurement of membrane potential and pH in cells, organells and vesicles. Methods Enzymol LV: 547–569

    Google Scholar 

  • Szostak M, Wanner G, Lubitz W (1990) Recombinant bacterial ghosts as vaccines. Res Microbiol 141: 1005–1007

    Google Scholar 

  • Witte A (1990) Untersuchungen zur Wirkung von PhiX174 Protein E sowie davon abgeleiteter chimärer Proteine auf den Zellwandkomplex von Escherichia coli. PhD-Thesis, University of Munich, Faculty of Science

  • Witte A, Lubitz W, Bakker EP (1987) Proton-motive-force-dependent step in the pathway of lysis of Escherichia coli induced by bacteriophage PhiX174 gene E product. J Bacteriol 169: 1750–1752

    Google Scholar 

  • Witte A, Lubitz W (1989) Biochemical characterization of PhiX174-protein-E-mediated lysis of Escherichia coli. Eur J Biochem 180: 393–398

    Google Scholar 

  • Witte A, Wanner G, Bläsi U, Halfmann G, Szostak M, Lubitz W (1990a) Endogenous transmembrane tunnel formation mediated by PhiX174 protein E. J Bacteriol 172: 4109–4114

    Google Scholar 

  • Witte A, Bläsi U, Halfmann G, Szostak M, Wanner G, Lubitz W (1990b) PhiX174 protein E-mediated lysis of Escherichia coli. Biochimie 72: 191–200

    Google Scholar 

  • Young KD, Young R (1982) Lytic action of cloned PhiX174 gene E. J Virol 44: 993–1002

    Google Scholar 

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Witte, A., Wanner, G., Sulzner, M. et al. Dynamics of PhiX174 protein E-mediated lysis of Escherichia coli . Arch. Microbiol. 157, 381–388 (1992). https://doi.org/10.1007/BF00248685

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