1887

Microbiology Society logo

Volume 147, Issue 3

Regulation of the switch from early to late bacteriophage λ DNA replication Free

Abstract

There are two modes of bacteriophage λ DNA replication following infection of its host, . Early after infection, replication occurs according to the theta (θ or circle-to-circle) mode, and is later switched to the sigma (σ or rolling-circle) mode. It is not known how this switch, occurring at a specific time in the infection cycle, is regulated. Here it is demonstrated that in wild-type cells the replication starting from λ proceeds both bidirectionally and unidirectionally, whereas in bacteria devoid of a functional DnaA protein, replication from λ is predominantly unidirectional. The regulation of directionality of replication from λ is mediated by positive control of λ promoter activity by DnaA, since the mode of replication of an artificial λ replicon bearing the promoter instead of was found to be independent of DnaA function. These findings and results of density-shift experiments suggest that in mutants infected with λ, phage DNA replication proceeds predominantly according to the unidirectional θ mechanism and is switched early after infection to the σ mode. It is proposed that in wild-type cells infected with λ, phage DNA replication proceeds according to a bidirectional θ mechanism early after infection due to efficient transcriptional activation of λ, stimulated by the host DnaA protein. After a few rounds of this type of replication, the resulting increased copy number of λ genomic DNA may cause a depletion of free DnaA protein because of its interaction with the multiple DnaA-binding sites in λ DNA. It is proposed that this may lead to inefficient transcriptional activation of λ resulting in unidirectional θ replication followed by σ type replication.

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
Keyword(s): bacteriophage λ development , Escherichia coli DnaA protein , rolling-circle DNA replication , theta DNA replication and transcriptional activation of origin
© Microbiology Society
Loading

Article metrics loading...

/content/journal/micro/10.1099/00221287-147-3-535
2001-03-01
2024-04-25
Loading full text...

Full text loading...

/deliver/fulltext/micro/147/3/1470535a.html?itemId=/content/journal/micro/10.1099/00221287-147-3-535&mimeType=html&fmt=ahah

References

  1. Alfano C., McMacken R. 1989a; Ordered assembly of nucleoprotein structures at the bacteriophage λ replication origin during the initiation of DNA replication. J Biol Chem 264:10699–10708
     [Google Scholar]
  2. Alfano C., McMacken R. 1989b; Heat shock protein-mediated disassembly of nucleoprotein structures is required for the initiation of bacteriophage λ DNA replication. J Biol Chem 264:10709–10718
     [Google Scholar]
  3. Better M., Freifelder D. 1983; Studies on the replication of Escherichia coli phage λ DNA. Virology 126:168–182 [CrossRef]
     [Google Scholar]
  4. Burkardt H., Lurz R. 1984; Electron microscopy. In Advanced Molecular Genetics pp 281–313 Edited by Puhler A., Timmis K. N. Berlin and Heidelberg: Springer;
     [Google Scholar]
  5. Dodson M., Echols H., Wickner S., Alfano C., Mensa-Wilmot K., Gomes B., LeBowitz J., Roberts J. D., McMacken R. 1986; Specialized nucleoprotein structures at the origin of replication of bacteriophage λ: localized unwinding of duplex DNA by a six protein reaction. Proc Natl Acad Sci USA 83:7638–7642 [CrossRef]
     [Google Scholar]
  6. Dove W. F., Hargrove E., Ohashi M., Haugli F., Guha A. 1969; Replicator activation in lambda. Jpn J Genet 44 (Suppl. 1):11–22 [CrossRef]
     [Google Scholar]
  7. Gabig M., Obuchowski M., Węgrzyn A., Szalewska-Pałasz A., Thomas M. S., Węgrzyn G. 1998; Excess production of phage λ delayed early proteins under conditions supporting high Escherichia coli growth rates. Microbiology 144:2217–2224 [CrossRef]
     [Google Scholar]
  8. Glinkowska M., Węgrzyn A., Węgrzyn G. 1999; Replication of bacteriophage λ in the Escherichia coli dnaA Δ rac hosts. Genetics 151:1633–1635
     [Google Scholar]
  9. Gottesman M. 1999; Bacteriophage λ: the untold story. J Mol Biol 293:177–180 [CrossRef]
     [Google Scholar]
  10. Herman-Antosiewicz A., Taylor K, Śrutkowska S., Węgrzyn G. 1998a; Replication and maintenance of λ plasmids devoid of the Cro repressor autoregulatory loop in Escherichia coli . Plasmid 40:113–125 [CrossRef]
     [Google Scholar]
  11. Herman-Antosiewicz A., Taylor K, Węgrzyn A., Węgrzyn G. 1998b; DnaA-mediated regulation of phage λ-derived replicons in the absence of p R and Cro function. Virology 249:98–107 [CrossRef]
     [Google Scholar]
  12. Ingmer H., Atlung T. 1992; Expression and regulation of a dnaA homologue isolated from Pseudomonas putida . Mol Gen Genet 232:431–439
     [Google Scholar]
  13. Jensen K. F. 1993; The Escherichia coli ‘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
     [Google Scholar]
  14. Konopa G., Barańska S., Węgrzyn A., Węgrzyn G. 2000; Bacteriophage and host mutants causing the rolling-circle λ DNA replication early after infection. FEBS Lett 472:217–220 [CrossRef]
     [Google Scholar]
  15. Kornberg A., Baker T. A. 1992 DNA Replication New York: W. H. Freeman;
     [Google Scholar]
  16. Kur J., Taylor K, Górska I. 1987; Escherichia coli dnaA initiation function is required for replication of plasmids derived from coliphage lambda. J Mol Biol 198:203–210 [CrossRef]
     [Google Scholar]
  17. Learn B., Karzai A. W., McMacken R. 1993; Transcription stimulates the establishment of bidirectional λ DNA replication in vitro . Cold Spring Harbor Symp Quant Biol 58:389–402 [CrossRef]
     [Google Scholar]
  18. Mensa-Wilmot K., Seaby R., Alfano C., Wold M. S., Gomes B., McMacken R. 1989; Reconstitution of a nine-protein system that initiates bacteriophage λ DNA replication. J Biol Chem 264:2853–2861
     [Google Scholar]
  19. Nijkamp H. J. J., Szybalski W., Ohashi M., Dove W. F. 1971; Gene expression by constitutive mutants of coliphage lambda. Mol Gen Genet 114:80–88
     [Google Scholar]
  20. Schnos M., Inman R. B. 1970; Position of branch point in replicating λ DNA. J Mol Biol 51:61–73 [CrossRef]
     [Google Scholar]
  21. Singer M., Baker T. A., Schnitzler G. 7 other authors 1989; A collection of strains containing genetically linked alternating antibiotic resistance elements for genetic mapping of Escherichia coli. Microbiol Rev 53:1–24
     [Google Scholar]
  22. Śrutkowska S. Konopa G., Węgrzyn G. 1998; A method for isolation of plasmid DNA replication intermediates from unsynchronized bacterial cultures for electron microscopy analysis. Acta Biochim Pol 45:233–240
     [Google Scholar]
  23. Śrutkowska S. Caspi R., Gabig M., Węgrzyn G. 1999; Detection of DNA replication intermediates after two-dimensional agarose gel electrophoresis using a fluorescein-labeled probe. Anal Biochem 269:221–222 [CrossRef]
     [Google Scholar]
  24. Stillman B. 1994; Initiation of chromosomal DNA replication in eukaryotes: lessons from lambda. J Biol Chem 269:7047–7050
     [Google Scholar]
  25. Subak-Sharpe J. H., Dargan D. J. 1998; HSV molecular biology: general aspects of Herpes Simplex Virus molecular biology. Virus Genes 16:239–251 [CrossRef]
     [Google Scholar]
  26. Sutton M. D., Kaguni J. M. 1997; Novel alleles of the Escherichia coli dnaA gene. J Mol Biol 271:693–703 [CrossRef]
     [Google Scholar]
  27. Szalewska-Pałasz A., Węgrzyn A., Błaszczak A., Taylor K., Węgrzyn G. 1998a; DnaA-stimulated transcriptional activation of ori λ: Escherichia coli RNA polymerase β subunit as a transcriptional activator contact site. Proc Natl Acad Sci USA 95:4241–4246 [CrossRef]
     [Google Scholar]
  28. Szalewska-Pałasz A., Lemieszek E., Pankiewicz A., Helinski D. R, Węgrzyn A., Węgrzyn G. 1998b; Escherichia coli dnaA gene function and bacteriophage λ replication. FEMS Microbiol Lett 167:27–32
     [Google Scholar]
  29. Szalewska-Pałasz A., Weigel C., Speck C. 7 other authors 1998c; Interaction of the Escherichia coli DnaA protein with bacteriophage λ DNA. Mol Gen Genet 259:679–688 [CrossRef]
     [Google Scholar]
  30. Taylor K., Węgrzyn G. 1995; Replication of coliphage lambda DNA. FEMS Microbiol Rev 17:109–119 [CrossRef]
     [Google Scholar]
  31. Taylor K., Węgrzyn G. 1998; Regulation of bacteriophage λ replication. In Molecular Microbiology pp 81–97 Edited by Busby S. J. W., Thomas C. M., Brown N. L. Berlin and Heidelberg: Springer;
     [Google Scholar]
  32. Thomas R. 1993; Bacteriophage λ: transactivation, positive control and other odd findings. BioEssays 15:285–289 [CrossRef]
     [Google Scholar]
  33. Viguera E., Hernandez P., Krimer D. B., Boistov A. S., Lurz R., Alonso J. C., Schvartzman J. B. 1996; The ColE1 unidirectional origin acts as a polar replication fork pausing site. J Biol Chem 271:22414–22421 [CrossRef]
     [Google Scholar]
  34. Viguera E., Rodrı́guez A., Krimer D. B., Trelles O., Schvartzman J. B, Hernández P. 1998; A computer model for the analysis of DNA replication intermediates by two-dimensional (2D) agarose gel electrophoresis. Gene 217:41–49 [CrossRef]
     [Google Scholar]
  35. Węgrzyn A., Węgrzyn G. Taylor K. 1995a; Protection of coliphage λO initiator protein from proteolysis in the assembly of the replication complex in vivo . Virology 207:179–184 [CrossRef]
     [Google Scholar]
  36. Węgrzyn A., Węgrzyn G. Taylor K. 1995b; Plasmid and host functions required for λ plasmid replication carried out by the inherited replication complex. Mol Gen Genet 247:501–508 [CrossRef]
     [Google Scholar]
  37. Węgrzyn A., Czyż A. Gabig M., Węgrzyn G. 2000; ClpP/ClpX-mediated degradation of the bacteriophage λ O protein and regulation of λ phage and λ plasmid replication. Arch Microbiol 174:89–96 [CrossRef]
     [Google Scholar]
  38. Węgrzyn G., Kwásnik E. Taylor K. 1991; Replication of λ plasmid in amino acid-starved strains of Escherichia coli . Acta Biochim Pol 38:181–186
     [Google Scholar]
  39. Węgrzyn G., Szalewska-Pałasz A., Obuchowski M., Taylor K, Węgrzyn A. 1995a; Transcriptional activation of the origin of coliphage λ DNA replication is regulated by the host DnaA initiator function. Gene 154:47–50 [CrossRef]
     [Google Scholar]
  40. Węgrzyn G., Węgrzyn A. Konieczny I., Bielawski K., Konopa G., Obuchowski M., Helinski D. R., Taylor K. 1995b; Involvement of the host initiator function dnaA in the replication of coliphage λ. Genetics 139:1469–1481
     [Google Scholar]
  41. Węgrzyn G., Węgrzyn A., Pankiewicz A. Taylor K. 1996; Allele specificity of the Escherichia coli dnaA gene function in the replication of plasmids derived from phage λ. Mol Gen Genet 252:580–586
     [Google Scholar]
  42. Żylicz M. Ang D., Liberek K., Georgopoulos C. 1989; Initiation of λ DNA replication with purified host- and bacteriophage-encoded proteins: the role of the DnaK, DnaJ and GrpE heat shock proteins. EMBO J 8:1601–1608
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/00221287-147-3-535
Loading
Regulation of the switch from early to late bacteriophage λ DNA replication
Microbiology 147, 535 (2001); https://doi.org/10.1099/00221287-147-3-535
/content/journal/micro/10.1099/00221287-147-3-535
/content/journal/micro/10.1099/00221287-147-3-535
Loading

Data & Media loading...

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error