Skip to main content
PMC home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1991 Jul;173(13):4032–4038. doi: 10.1128/jb.173.13.4032-4038.1991

Multiple effects of Fis on integration and the control of lysogeny in phage lambda.

C A Ball 1, R C Johnson 1
PMCID: PMC208051  PMID: 1829454

Abstract

Fis is a small, basic, site-specific DNA-binding protein present in Escherichia coli. A Fis-binding site (F) has been previously identified in the attP recombination site of phage lambda (J. F. Thompson, L. Moitoso de Vargas, C. Koch, R. Kahmann, and A. Landy, Cell 50:901-908, 1987). The present study demonstrates that in the absence of the phage-encoded Xis protein, the binding of Fis to F can stimulate integrative recombination and therefore increase the frequency of lambda lysogeny in vivo. Additionally, Fis exerts a stimulatory effect on both integration and lysogeny that is independent of binding to the attP F site. Maintenance of the lysogenic state also appears to be enhanced in the presence of Fis, as shown by the increased sensitivity of lambda prophages encoding temperature-sensitive repressors to partial thermoinduction in a fis mutant. In the presence of Xis, however, Fis binding to F interferes with integration by stimulating excision, the competing back-reaction. Since Fis stimulates both excision and integration, depending on the presence or absence of Xis, respectively, we conclude that Xis binding to X1 is the key determinant directing the formation of an excisive complex.

Full text

PDF
4038

Selected References

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

  1. Abremski K., Gottesman S. Purification of the bacteriophage lambda xis gene product required for lambda excisive recombination. J Biol Chem. 1982 Aug 25;257(16):9658–9662. [PubMed] [Google Scholar]
  2. Ball C. A., Johnson R. C. Efficient excision of phage lambda from the Escherichia coli chromosome requires the Fis protein. J Bacteriol. 1991 Jul;173(13):4027–4031. doi: 10.1128/jb.173.13.4027-4031.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Better M., Lu C., Williams R. C., Echols H. Site-specific DNA condensation and pairing mediated by the int protein of bacteriophage lambda. Proc Natl Acad Sci U S A. 1982 Oct;79(19):5837–5841. doi: 10.1073/pnas.79.19.5837. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bliska J. B., Cozzarelli N. R. Use of site-specific recombination as a probe of DNA structure and metabolism in vivo. J Mol Biol. 1987 Mar 20;194(2):205–218. doi: 10.1016/0022-2836(87)90369-x. [DOI] [PubMed] [Google Scholar]
  5. Bétermier M., Lefrère V., Koch C., Alazard R., Chandler M. The Escherichia coli protein, Fis: specific binding to the ends of phage Mu DNA and modulation of phage growth. Mol Microbiol. 1989 Apr;3(4):459–468. doi: 10.1111/j.1365-2958.1989.tb00192.x. [DOI] [PubMed] [Google Scholar]
  6. Enquist L. W., Weisberg R. A. The red plaque test: a rapid method for identification of excision defective variants of bacteriophage lambda. Virology. 1976 Jul 1;72(1):147–153. doi: 10.1016/0042-6822(76)90319-6. [DOI] [PubMed] [Google Scholar]
  7. Friedman D. I., Olson E. R., Georgopoulos C., Tilly K., Herskowitz I., Banuett F. Interactions of bacteriophage and host macromolecules in the growth of bacteriophage lambda. Microbiol Rev. 1984 Dec;48(4):299–325. doi: 10.1128/mr.48.4.299-325.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Gardner J. F., Nash H. A. Role of Escherichia coli IHF protein in lambda site-specific recombination. A mutational analysis of binding sites. J Mol Biol. 1986 Sep 20;191(2):181–189. doi: 10.1016/0022-2836(86)90255-x. [DOI] [PubMed] [Google Scholar]
  9. Gellert M., Mizuuchi K., O'Dea M. H., Nash H. A. DNA gyrase: an enzyme that introduces superhelical turns into DNA. Proc Natl Acad Sci U S A. 1976 Nov;73(11):3872–3876. doi: 10.1073/pnas.73.11.3872. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Giladi H., Gottesman M., Oppenheim A. B. Integration host factor stimulates the phage lambda pL promoter. J Mol Biol. 1990 May 5;213(1):109–121. doi: 10.1016/S0022-2836(05)80124-X. [DOI] [PubMed] [Google Scholar]
  11. Goodman S. D., Nash H. A. Functional replacement of a protein-induced bend in a DNA recombination site. Nature. 1989 Sep 21;341(6239):251–254. doi: 10.1038/341251a0. [DOI] [PubMed] [Google Scholar]
  12. Gottesman S., Abremski K. The role of HimA and Xis in lambda site-specific recombination. J Mol Biol. 1980 Apr 15;138(3):503–512. doi: 10.1016/s0022-2836(80)80015-5. [DOI] [PubMed] [Google Scholar]
  13. Hoess R. H., Foeller C., Bidwell K., Landy A. Site-specific recombination functions of bacteriophage lambda: DNA sequence of regulatory regions and overlapping structural genes for Int and Xis. Proc Natl Acad Sci U S A. 1980 May;77(5):2482–2486. doi: 10.1073/pnas.77.5.2482. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hoyt M. A., Knight D. M., Das A., Miller H. I., Echols H. Control of phage lambda development by stability and synthesis of cII protein: role of the viral cIII and host hflA, himA and himD genes. Cell. 1982 Dec;31(3 Pt 2):565–573. doi: 10.1016/0092-8674(82)90312-9. [DOI] [PubMed] [Google Scholar]
  15. Johnson R. C., Ball C. A., Pfeffer D., Simon M. I. Isolation of the gene encoding the Hin recombinational enhancer binding protein. Proc Natl Acad Sci U S A. 1988 May;85(10):3484–3488. doi: 10.1073/pnas.85.10.3484. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Landy A. Dynamic, structural, and regulatory aspects of lambda site-specific recombination. Annu Rev Biochem. 1989;58:913–949. doi: 10.1146/annurev.bi.58.070189.004405. [DOI] [PubMed] [Google Scholar]
  17. Mandal N. C., Lieb M. Heat-sensitive DNA-binding activity of the cI product of bacteriophage lambda. Mol Gen Genet. 1976 Aug 2;146(3):299–302. doi: 10.1007/BF00701254. [DOI] [PubMed] [Google Scholar]
  18. Mizuuchi K., Mizuuchi M. Integrative recombination of bacteriophage lambda: in vitro study of the intermolecular reaction. Cold Spring Harb Symp Quant Biol. 1979;43(Pt 2):1111–1114. doi: 10.1101/sqb.1979.043.01.123. [DOI] [PubMed] [Google Scholar]
  19. Nilsson L., Vanet A., Vijgenboom E., Bosch L. The role of FIS in trans activation of stable RNA operons of E. coli. EMBO J. 1990 Mar;9(3):727–734. doi: 10.1002/j.1460-2075.1990.tb08166.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Richet E., Abcarian P., Nash H. A. The interaction of recombination proteins with supercoiled DNA: defining the role of supercoiling in lambda integrative recombination. Cell. 1986 Sep 26;46(7):1011–1021. doi: 10.1016/0092-8674(86)90700-2. [DOI] [PubMed] [Google Scholar]
  21. Ross W., Thompson J. F., Newlands J. T., Gourse R. L. E.coli Fis protein activates ribosomal RNA transcription in vitro and in vivo. EMBO J. 1990 Nov;9(11):3733–3742. doi: 10.1002/j.1460-2075.1990.tb07586.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Sinden R. R., Broyles S. S., Pettijohn D. E. Perfect palindromic lac operator DNA sequence exists as a stable cruciform structure in supercoiled DNA in vitro but not in vivo. Proc Natl Acad Sci U S A. 1983 Apr;80(7):1797–1801. doi: 10.1073/pnas.80.7.1797. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Surette M. G., Chaconas G. A protein factor which reduces the negative supercoiling requirement in the Mu DNA strand transfer reaction is Escherichia coli integration host factor. J Biol Chem. 1989 Feb 15;264(5):3028–3034. [PubMed] [Google Scholar]
  24. Thompson J. F., Moitoso de Vargas L., Koch C., Kahmann R., Landy A. Cellular factors couple recombination with growth phase: characterization of a new component in the lambda site-specific recombination pathway. Cell. 1987 Sep 11;50(6):901–908. doi: 10.1016/0092-8674(87)90516-2. [DOI] [PubMed] [Google Scholar]
  25. Yin S., Bushman W., Landy A. Interaction of the lambda site-specific recombination protein Xis with attachment site DNA. Proc Natl Acad Sci U S A. 1985 Feb;82(4):1040–1044. doi: 10.1073/pnas.82.4.1040. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES