Skip to main content
Genetics logoLink to Genetics
. 1993 Jan;133(1):17–28. doi: 10.1093/genetics/133.1.17

Lethal Transposition of Mud Phages in Rec(-) Strains of Salmonella Typhimurium

R V Sonti 1, D H Keating 1, J R Roth 1
PMCID: PMC1205294  PMID: 8417985

Abstract

Under several circumstances, the frequency with which Mud prophages form lysogens is apparently reduced in rec strains of Salmonella typhimurium. Lysogen formation by a MudI genome (37 kb) injected by a Mu virion is unaffected by a host rec mutation. However when the same MudI phage is injected by a phage P22 virion, lysogeny is reduced in a recA or recB mutant host. A host rec mutation reduces the lysogenization of mini-Mu phages injected by either Mu or P22 virions. When lysogen frequency is reduced by a host rec mutation, the surviving lysogens show an increased probability of carrying a deletion adjacent to the Mud insertion site. We propose that the rec effects seen are due to a failure of conservative Mu transposition. Replicative Mud transposition from a linear fragment causes a break in the host chromosome with a Mu prophage at both broken ends. These breaks are lethal unless repaired; repair can be achieved by Rec functions acting on the repeated Mu sequences or by secondary transposition events. In a normal Mu infection, the initial transposition from the injected fragment is conservative and does not break the chromosome. To account for the conditions under which rec effects are seen, we propose that conservative transposition of Mu depends on a protein that must be injected with the DNA. This protein can be injected by Mu but not by P22 virions. Injection or function of the protein may depend on its association with a particular Mu DNA sequence that is present and properly positioned in Mu capsids containing full-sized Mu or MudI genomes; this sequence may be lacking or abnormally positioned in the mini-Mud phages tested.

Full Text

The Full Text of this article is available as a PDF (1.8 MB).

Selected References

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

  1. Alper M. D., Ames B. N. Positive selection of mutants with deletions of the gal-chl region of the Salmonella chromosome as a screening procedure for mutagens that cause deletions. J Bacteriol. 1975 Jan;121(1):259–266. doi: 10.1128/jb.121.1.259-266.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Berkowitz D., Hushon J. M., Whitfield H. J., Jr, Roth J., Ames B. N. Procedure for identifying nonsense mutations. J Bacteriol. 1968 Jul;96(1):215–220. doi: 10.1128/jb.96.1.215-220.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Breepoel H., Hoogendorp J., Mellema J. E., Wijffelman C. Linkage of the variable end of the bacteriophage mu DNA to the tail. Virology. 1976 Oct 15;74(2):279–286. doi: 10.1016/0042-6822(76)90335-4. [DOI] [PubMed] [Google Scholar]
  4. Cabezón T., Gijsegem F. V., Toussaint A., Faelen M., Bollen A. Phage Mu-1 mediated transposition: a tool to study the organization of ribosomal protein genes in Escherichia coli. Mol Gen Genet. 1978 May 31;161(3):291–296. doi: 10.1007/BF00331003. [DOI] [PubMed] [Google Scholar]
  5. Casadaban M. J., Cohen S. N. Lactose genes fused to exogenous promoters in one step using a Mu-lac bacteriophage: in vivo probe for transcriptional control sequences. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4530–4533. doi: 10.1073/pnas.76.9.4530. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Castilho B. A., Olfson P., Casadaban M. J. Plasmid insertion mutagenesis and lac gene fusion with mini-mu bacteriophage transposons. J Bacteriol. 1984 May;158(2):488–495. doi: 10.1128/jb.158.2.488-495.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Chaconas G., Giddens E. B., Miller J. L., Gloor G. A truncated form of the bacteriophage Mu B protein promotes conservative integration, but not replicative transposition, of Mu DNA. Cell. 1985 Jul;41(3):857–865. doi: 10.1016/s0092-8674(85)80066-0. [DOI] [PubMed] [Google Scholar]
  8. Chaconas G., Gloor G., Miller J. L., Kennedy D. L., Giddens E. B., Nagainis C. R. Transposition of bacteriophage mu DNA: expression of the A and B proteins from lambda pL and analysis of infecting mu DNA. Cold Spring Harb Symp Quant Biol. 1984;49:279–284. doi: 10.1101/sqb.1984.049.01.033. [DOI] [PubMed] [Google Scholar]
  9. Chaconas G., de Bruijn F. J., Casadaban M. J., Lupski J. R., Kwoh T. J., Harshey R. M., DuBow M. S., Bukhari A. I. In vitro and in vivo manipulations of bacteriophage Mu DNA: cloning of Mu ends and construction of mini-Mu's carrying selectable markers. Gene. 1981 Jan-Feb;13(1):37–46. doi: 10.1016/0378-1119(81)90041-x. [DOI] [PubMed] [Google Scholar]
  10. Chan R. K., Botstein D., Watanabe T., Ogata Y. Specialized transduction of tetracycline resistance by phage P22 in Salmonella typhimurium. II. Properties of a high-frequency-transducing lysate. Virology. 1972 Dec;50(3):883–898. doi: 10.1016/0042-6822(72)90442-4. [DOI] [PubMed] [Google Scholar]
  11. Craigie R., Mizuuchi K. Mechanism of transposition of bacteriophage Mu: structure of a transposition intermediate. Cell. 1985 Jul;41(3):867–876. doi: 10.1016/s0092-8674(85)80067-2. [DOI] [PubMed] [Google Scholar]
  12. Faelen M., Huisman O., Toussaint A. Involvement of phage Mu-1 early functions in Mu-mediated chromosomal rearrangements. Nature. 1978 Feb 9;271(5645):580–582. doi: 10.1038/271580a0. [DOI] [PubMed] [Google Scholar]
  13. Faelen M., Mergeay M., Gerits J., Toussaint A., Lefèbvre N. Genetic mapping of a mutation conferring sensitivity to bacteriophage Mu in Salmonella typhimurium LT2. J Bacteriol. 1981 Jun;146(3):914–919. doi: 10.1128/jb.146.3.914-919.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Gloor G., Chaconas G. Sequence of bacteriophage Mu N and P genes. Nucleic Acids Res. 1988 Jun 10;16(11):5211–5212. doi: 10.1093/nar/16.11.5211. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Gloor G., Chaconas G. The bacteriophage Mu N gene encodes the 64-kDa virion protein which is injected with, and circularizes, infecting Mu DNA. J Biol Chem. 1986 Dec 15;261(35):16682–16688. [PubMed] [Google Scholar]
  16. Grundy F. J., Howe M. M. Involvement of the invertible G segment in bacteriophage mu tail fiber biosynthesis. Virology. 1984 Apr 30;134(2):296–317. doi: 10.1016/0042-6822(84)90299-x. [DOI] [PubMed] [Google Scholar]
  17. Harshey R. M., Bukhari A. I. Infecting bacteriophage mu DNA forms a circular DNA-protein complex. J Mol Biol. 1983 Jun 25;167(2):427–441. doi: 10.1016/s0022-2836(83)80343-x. [DOI] [PubMed] [Google Scholar]
  18. Howe M. M., Schumm J. W. Transposition of bacteriophage Mu: properties of lambda phages containing both ends of Mu. Cold Spring Harb Symp Quant Biol. 1981;45(Pt 1):337–346. doi: 10.1101/sqb.1981.045.01.047. [DOI] [PubMed] [Google Scholar]
  19. Hughes K. T., Olivera B. M., Roth J. R. Rec dependence of mu transposition from P22-transduced fragments. J Bacteriol. 1987 Jan;169(1):403–409. doi: 10.1128/jb.169.1.403-409.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Hughes K. T., Roth J. R. Transitory cis complementation: a method for providing transposition functions to defective transposons. Genetics. 1988 May;119(1):9–12. doi: 10.1093/genetics/119.1.9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Sanderson K. E., Roth J. R. Linkage map of Salmonella typhimurium, edition VII. Microbiol Rev. 1988 Dec;52(4):485–532. doi: 10.1128/mr.52.4.485-532.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Schmieger H. Phage P22-mutants with increased or decreased transduction abilities. Mol Gen Genet. 1972;119(1):75–88. doi: 10.1007/BF00270447. [DOI] [PubMed] [Google Scholar]
  23. Shapiro J. A. Molecular model for the transposition and replication of bacteriophage Mu and other transposable elements. Proc Natl Acad Sci U S A. 1979 Apr;76(4):1933–1937. doi: 10.1073/pnas.76.4.1933. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. TAYLOR A. L. BACTERIOPHAGE-INDUCED MUTATION IN ESCHERICHIA COLI. Proc Natl Acad Sci U S A. 1963 Dec;50:1043–1051. doi: 10.1073/pnas.50.6.1043. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. VOGEL H. J., BONNER D. M. Acetylornithinase of Escherichia coli: partial purification and some properties. J Biol Chem. 1956 Jan;218(1):97–106. [PubMed] [Google Scholar]
  26. Van Leerdam E., Karreman C., van de Putte P. Ner, a cro-like function of bacteriophage Mu. Virology. 1982 Nov;123(1):19–28. doi: 10.1016/0042-6822(82)90291-4. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES