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Journal of General Virology header logo Journal of General Virology

Volume 94, Issue 4

Proteomic profiles and kinetics of development of bacteriophage T4 and its and mutants in slowly growing No Access

Abstract

Bacteriophage T4 survival in its natural environment requires adjustment of phage development to the slow bacterial growth rate or the initiation of mechanisms of pseudolysogeny or lysis inhibition (LIN). While phage-encoded RI and probably RIII proteins seem to be crucial players in pseudolysogeny and LIN phenomena, the identity of proteins involved in the regulation of T4 development in slowly growing bacteria has remained unknown. In this work, using a chemostat system, we studied the development of wild-type T4 (T4wt) and its (T4) and (T4) mutants in slowly growing bacteria, where T4 did not initiate LIN or pseudolysogeny. We determined eclipse periods, phage propagation times, latent periods and burst sizes of T4wt, T4 and T4. We also compared intracellular proteomes of slowly growing infected with either T4wt or the mutants. Using two-dimensional PAGE analyses we found 18 differentially expressed proteins from lysates of infected cells. Proteins whose amounts were different in cells harbouring T4wt and the mutants are involved in processes of replication, phage–host interactions or they constitute virion components. Our data indicate that functional RI and RIII proteins – apart from their already known roles in LIN and pseudolysogeny – are also necessary for the regulation of phage T4 development in slowly growing bacteria. This regulation may be more complicated than previously anticipated, with many factors influencing T4 development in its natural habitat.

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© 2013 SGM
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/content/journal/jgv/10.1099/vir.0.048686-0
2013-04-01
2025-04-23
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References

  1. Abedon S. T. 1994; Lysis and interaction between free phage and infected cells. In Molecular Biology of Bacteriophage T4 pp. 397–405 Edited by Karam J. D. Washington, DC: American Society for Microbiology;
     [Google Scholar]
  2. Abedon S. T., Herschler T. D., Stopar D. 2001; Bacteriophage latent-period evolution as a response to resource availability. Appl Environ Microbiol 67:4233–4241 [View Article][PubMed]
     [Google Scholar]
  3. Abedon S. T., Hyman P., Thomas C. 2003; Experimental examination of bacteriophage latent-period evolution as a response to bacterial availability. Appl Environ Microbiol 69:7499–7506 [View Article][PubMed]
     [Google Scholar]
  4. Bernhardt J., Büttner K., Scharf C., Hecker M. 1999; Dual channel imaging of two-dimensional electropherograms in Bacillus subtilis. Electrophoresis 20:2225–2240 [View Article][PubMed]
     [Google Scholar]
  5. Bode W. 1967; Lysis inhibition in Escherichia coli infected with bacteriophage T4. J Virol 1:948–955[PubMed]
     [Google Scholar]
  6. Burch L. H., Zhang L., Chao F. G., Xu H., Drake J. W. 2011; The bacteriophage T4 rapid-lysis genes and their mutational proclivities. J Bacteriol 193:3537–3545 [View Article][PubMed]
     [Google Scholar]
  7. Doermann A. H. 1948; Lysis and lysis inhibition with Escherichia coli bacteriophage. J Bacteriol 55:257–276[PubMed]
     [Google Scholar]
  8. Doermann A. H., Hill M. B. 1953; Genetic structure of bacteriophage T4 as described by recombination studies of factors influencing plaque morphology. Genetics 38:79–90[PubMed]
     [Google Scholar]
  9. Edgar R. S., Feynman R. P., Klein S., Lielausis I., Steinberg C. M. 1962; Mapping experiments with r mutants of bacteriophage T4D. Genetics 47:179–186[PubMed]
     [Google Scholar]
  10. Golec P. 2010 The role of RI and RIII proteins in regulation of developmental cycle of bacteriophage T4. PhD thesis. University of Gdansk
  11. Golec P., Wiczk A., Majchrzyk A., Łoś J. M., Węgrzyn G., Łoś M. 2010; A role for accessory genes rI.-1 and rI.1 in the regulation of lysis inhibition by bacteriophage T4. Virus Genes 41:459–468 [View Article][PubMed]
     [Google Scholar]
  12. Golec P., Wiczk A., Łoś J. M., Konopa G., Węgrzyn G., Łoś M. 2011; Persistence of bacteriophage T4 in a starved Escherichia coli culture: evidence for the presence of phage subpopulations. J Gen Virol 92:,997–1003 [View Article][PubMed]
     [Google Scholar]
  13. Görg A., Obermaier C., Boguth G., Weiss W. 1999; Recent developments in two-dimensional gel electrophoresis with immobilized pH gradients: wide pH gradients up to pH 12, longer separation distances and simplified procedures. Electrophoresis 20:712–717 [View Article][PubMed]
     [Google Scholar]
  14. Hadas H., Einav M., Fishov I., Zaritsky A. 1997; Bacteriophage T4 development depends on the physiology of its host Escherichia coli.. Microbiology 143:179–185 [View Article][PubMed]
     [Google Scholar]
  15. Hoskisson P. A., Hobbs G. 2005; Continuous culture – making a comeback?. Microbiology 151:3153–3159 [View Article][PubMed]
     [Google Scholar]
  16. Jensen K. F. 1993; The Escherichia coli K-12 “wild types” W3110 and MG1655 have an rph frameshift mutation that leads to pyrimidine starvation due to low pyrE expression levels. J Bacteriol 175:3401–3407[PubMed]
     [Google Scholar]
  17. Kang D., Gho Y. S., Suh M., Kang C. 2002; Highly sensitive and fast protein detection with Coomassie brilliant blue in sodium dodecyl sulfate–polyacrylamide gel electrophoresis. Bull Korean Chem Soc 23:1511–1512 [View Article]
     [Google Scholar]
  18. Koch A. L. 1971; The adaptive responses of Escherichia coli to a feast and famine existence. Adv Microb Physiol 6:147–217 [View Article][PubMed]
     [Google Scholar]
  19. Kutter E., Kellenberger E., Carlson K., Eddy S., Neitzel J., Messinger L., North J., Guttman B. 1994; Effects of bacterial growth conditions and physiology on T4 infection. In Molecular Biology of Bacteriophage T4 pp. 406–418 Edited by Karam J. D. Washington, DC: American Society for Microbiology;
     [Google Scholar]
  20. Łoś M., Węgrzyn G. 2012; Pseudolysogeny. Adv Virus Res 82:339–349 [View Article][PubMed]
     [Google Scholar]
  21. Łoś M., Węgrzyn G., Neubauer P. 2003; A role for bacteriophage T4 rI gene function in the control of phage development during pseudolysogeny and in slowly growing host cells. Res Microbiol 154:547–552 [View Article][PubMed]
     [Google Scholar]
  22. Miller E. S., Kutter E., Mosig G., Arisaka F., Kunisawa T., Rüger W. 2003; Bacteriophage T4 genome. Microbiol Mol Biol Rev 67:86–156 [View Article][PubMed]
     [Google Scholar]
  23. Paddison P., Abedon S. T., Dressman H. K., Gailbreath K., Tracy J., Mosser E., Neitzel J., Guttman B., Kutter E. 1998; The roles of the bacteriophage T4 r genes in lysis inhibition and fine-structure genetics: a new perspective. Genetics 148:1539–1550[PubMed]
     [Google Scholar]
  24. Rabinovitch A., Hadas H., Einav M., Melamed Z., Zaritsky A. 1999; Model for bacteriophage T4 development in Escherichia coli.. J Bacteriol 181:1677–1683[PubMed]
     [Google Scholar]
  25. Rabinovitch A., Fishov I., Hadas H., Einav M., Zaritsky A. 2002; Bacteriophage T4 development in Escherichia coli is growth rate dependent. J Theor Biol 216:1–4 [View Article][PubMed]
     [Google Scholar]
  26. Ramanculov E., Young R. 2001; Functional analysis of the phage T4 holin in a λ context. Mol Genet Genomics 265:345–353 [View Article][PubMed]
     [Google Scholar]
  27. Sambrook J., Fritsh E. F., Maniatis T. 1989 Molecular Cloning: a Laboratory Manual Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
     [Google Scholar]
  28. Teich A., Lin H. Y., Andersson L., Meyer S., Neubauer P. 1998; Amplification of ColE1 related plasmids in recombinant cultures of Escherichia coli after IPTG induction. J Biotechnol 64:197–210 [View Article][PubMed]
     [Google Scholar]
  29. Thürmer A., Voigt B., Angelov A., Albrecht D., Hecker M., Liebl W. 2011; Proteomic analysis of the extremely thermoacidophilic archaeon Picrophilus torridus at pH and temperature values close to its growth limit. Proteomics 11:4559–4568 [View Article][PubMed]
     [Google Scholar]
  30. Tran T. A., Struck D. K., Young R. 2005; Periplasmic domains define holin-antiholin interactions in T4 lysis inhibition. J Bacteriol 187:6631–6640 [View Article][PubMed]
     [Google Scholar]
  31. Tran T. A., Struck D. K., Young R. 2007; The T4 RI antiholin has an N-terminal signal anchor release domain that targets it for degradation by DegP. J Bacteriol 189:7618–7625 [View Article][PubMed]
     [Google Scholar]
/content/journal/jgv/10.1099/vir.0.048686-0
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Proteomic profiles and kinetics of development of bacteriophage T4 and its rI and rIII mutants in slowly growing Escherichia coli
J. Gen. Virol. 94, 896 (2013); https://doi.org/10.1099/vir.0.048686-0
/content/journal/jgv/10.1099/vir.0.048686-0
/content/journal/jgv/10.1099/vir.0.048686-0
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