Skip to main content
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1989 Sep;171(9):4938–4944. doi: 10.1128/jb.171.9.4938-4944.1989

Translesion synthesis is the main component of SOS repair in bacteriophage lambda DNA.

M Defais 1, C Lesca 1, B Monsarrat 1, P Hanawalt 1
PMCID: PMC210300  PMID: 2527845

Abstract

Agents that interfere with DNA replication in Escherichia coli induce physiological adaptations that increase the probability of survival after DNA damage and the frequency of mutants among the survivors (the SOS response). Such agents also increase the survival rate and mutation frequency of irradiated bacteriophage after infection of treated bacteria, a phenomenon known as Weigle reactivation. In UV-irradiated single-stranded DNA phage, Weigle reactivation is thought to occur via induced, error-prone replication through template lesions (translesion synthesis [P. Caillet-Fauquet, M: Defais, and M. Radman, J. Mol. Biol. 117:95-112, 1977]). Weigle reactivation occurs with higher efficiency in double-stranded DNA phages such as lambda, and we therefore asked if another process, recombination between partially replicated daughter molecules, plays a major role in this case. To distinguish between translesion synthesis and recombinational repair, we studied the early replication of UV-irradiated bacteriophage lambda in SOS-induced and uninduced bacteria. To avoid complications arising from excision of UV lesions, we used bacterial uvrA mutants, in which such excision does not occur. Our evidence suggests that translesion synthesis is the primary component of Weigle reactivation of lambda phage in the absence of excision repair. The greater efficiency in Weigle reactivation of double-stranded DNA phage could thus be attributed to some inducible excision repair unable to occur on single-stranded DNA. In addition, after irradiation, lambda phage replication seems to switch prematurely from the theta mode to the rolling circle mode.

Full text

PDF
4938

Images in this article

Selected References

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

  1. Boyle J. M., Setlow R. B. Correlations between host-cell reactivation, ultraviolet reactivation and pyrimidine dimer excision in the DNA of bacteriophage lambda. J Mol Biol. 1970 Jul 14;51(1):131–144. doi: 10.1016/0022-2836(70)90275-5. [DOI] [PubMed] [Google Scholar]
  2. Bridges B. A., Woodgate R. Mutagenic repair in Escherichia coli. X. The umuC gene product may be required for replication past pyrimidine dimers but not for the coding error in UV-mutagenesis. Mol Gen Genet. 1984;196(2):364–366. doi: 10.1007/BF00328073. [DOI] [PubMed] [Google Scholar]
  3. Burckhardt S. E., Woodgate R., Scheuermann R. H., Echols H. UmuD mutagenesis protein of Escherichia coli: overproduction, purification, and cleavage by RecA. Proc Natl Acad Sci U S A. 1988 Mar;85(6):1811–1815. doi: 10.1073/pnas.85.6.1811. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Cadet J., Voituriez L., Hahn B. S., Wang S. Y. Separation of cyclobutyl dimers of thymine and thymidine by high-performance liquid chromatography and thin-layer chromatography. J Chromatogr. 1980 Jul 4;195(1):139–145. doi: 10.1016/s0021-9673(00)81552-6. [DOI] [PubMed] [Google Scholar]
  5. Caillet-Fauquet P., Defais M., Radman M. Molecular mechanisms of induced mutagenesis. Replication in vivo of bacteriophage phiX174 single-stranded, ultraviolet light-irradiated DNA in intact and irradiated host cells. J Mol Biol. 1977 Nov 25;117(1):95–110. doi: 10.1016/0022-2836(77)90025-0. [DOI] [PubMed] [Google Scholar]
  6. Caillet-Fauquet P., Defais M. UV reactivation of phage lambda in a polA mutant of E. coli. Mutat Res. 1972 Jul;15(3):353–355. doi: 10.1016/0027-5107(72)90081-4. [DOI] [PubMed] [Google Scholar]
  7. Casaregola S., D'Ari R., Huisman O. Role of DNA replication in the induction and turn-off of the SOS response in Escherichia coli. Mol Gen Genet. 1982;185(3):440–444. doi: 10.1007/BF00334136. [DOI] [PubMed] [Google Scholar]
  8. Cooper P. K. Characterization of long patch excision repair of DNA in ultraviolet-irradiated Escherichia coli: an inducible function under rec-lex control. Mol Gen Genet. 1982;185(2):189–197. doi: 10.1007/BF00330785. [DOI] [PubMed] [Google Scholar]
  9. D'Ari R., Huisman O. DNA replication and indirect induction of the SOS response in Escherichia coli. Biochimie. 1982 Aug-Sep;64(8-9):623–627. doi: 10.1016/s0300-9084(82)80100-4. [DOI] [PubMed] [Google Scholar]
  10. Defais M., Fauquet P., Radman M., Errera M. Ultraviolet reactivation and ultraviolet mutagenesis of lambda in different genetic systems. Virology. 1971 Feb;43(2):495–503. doi: 10.1016/0042-6822(71)90321-7. [DOI] [PubMed] [Google Scholar]
  11. Defais M. Role of the E. coli umuC gene product in the repair of single-stranded DNA phage. Mol Gen Genet. 1983;192(3):509–511. doi: 10.1007/BF00392198. [DOI] [PubMed] [Google Scholar]
  12. Edlund T., Gustafsson P., Wolf-Watz H. Effect of thymine concentration on the mode of chromosomal replication in Escherichia coli K-12. J Mol Biol. 1976 Dec;108(2):295–303. doi: 10.1016/s0022-2836(76)80122-2. [DOI] [PubMed] [Google Scholar]
  13. Fersht A. R., Knill-Jones J. W. Contribution of 3' leads to 5' exonuclease activity of DNA polymerase III holoenzyme from Escherichia coli to specificity. J Mol Biol. 1983 Apr 25;165(4):669–682. doi: 10.1016/s0022-2836(83)80273-3. [DOI] [PubMed] [Google Scholar]
  14. Ganesan A. K. Persistence of pyrimidine dimers during post-replication repair in ultraviolet light-irradiated Escherichia coli K12. J Mol Biol. 1974 Jul 25;87(1):103–119. doi: 10.1016/0022-2836(74)90563-4. [DOI] [PubMed] [Google Scholar]
  15. George J., Devoret R., Radman M. Indirect ultraviolet-reactivation of phage lambda. Proc Natl Acad Sci U S A. 1974 Jan;71(1):144–147. doi: 10.1073/pnas.71.1.144. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kato T., Shinoura Y. Isolation and characterization of mutants of Escherichia coli deficient in induction of mutations by ultraviolet light. Mol Gen Genet. 1977 Nov 14;156(2):121–131. doi: 10.1007/BF00283484. [DOI] [PubMed] [Google Scholar]
  17. Koffel-Schwartz N., Maenhaut-Michel G., Fuchs R. P. Specific strand loss in N-2-acetylaminofluorene-modified DNA. J Mol Biol. 1987 Feb 20;193(4):651–659. doi: 10.1016/0022-2836(87)90348-2. [DOI] [PubMed] [Google Scholar]
  18. Lackey D., Krauss S. W., Linn S. Characterization of DNA polymerase I*, a form of DNA polymerase I found in Escherichia coli expressing SOS functions. J Biol Chem. 1985 Mar 10;260(5):3178–3184. [PubMed] [Google Scholar]
  19. Lackey D., Krauss S. W., Linn S. Isolation of an altered form of DNA polymerase I from Escherichia coli cells induced for recA/lexA functions. Proc Natl Acad Sci U S A. 1982 Jan;79(2):330–334. doi: 10.1073/pnas.79.2.330. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Livneh Z. Mechanism of replication of ultraviolet-irradiated single-stranded DNA by DNA polymerase III holoenzyme of Escherichia coli. Implications for SOS mutagenesis. J Biol Chem. 1986 Jul 15;261(20):9526–9533. [PubMed] [Google Scholar]
  21. Livneh Z. Replication of UV-irradiated single-stranded DNA by DNA polymerase III holoenzyme of Escherichia coli: evidence for bypass of pyrimidine photodimers. Proc Natl Acad Sci U S A. 1986 Jul;83(13):4599–4603. doi: 10.1073/pnas.83.13.4599. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Love J. D., Friedberg E. C. Use of high-performance liquid chromatography to quantitate thymine-containing pyrimidine dimers in DNA. J Chromatogr. 1982 May 21;240(2):475–487. doi: 10.1016/s0021-9673(00)99626-2. [DOI] [PubMed] [Google Scholar]
  23. Lu C., Scheuermann R. H., Echols H. Capacity of RecA protein to bind preferentially to UV lesions and inhibit the editing subunit (epsilon) of DNA polymerase III: a possible mechanism for SOS-induced targeted mutagenesis. Proc Natl Acad Sci U S A. 1986 Feb;83(3):619–623. doi: 10.1073/pnas.83.3.619. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Monk M., Gross J. Induction of prophage lambda in a mutant of E. coli K12 defective in initiation of DNA replication at high temperature. Mol Gen Genet. 1971;110(4):299–306. doi: 10.1007/BF00438272. [DOI] [PubMed] [Google Scholar]
  25. Nohmi T., Battista J. R., Dodson L. A., Walker G. C. RecA-mediated cleavage activates UmuD for mutagenesis: mechanistic relationship between transcriptional derepression and posttranslational activation. Proc Natl Acad Sci U S A. 1988 Mar;85(6):1816–1820. doi: 10.1073/pnas.85.6.1816. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Rupp W. D., Wilde C. E., 3rd, Reno D. L., Howard-Flanders P. Exchanges between DNA strands in ultraviolet-irradiated Escherichia coli. J Mol Biol. 1971 Oct 14;61(1):25–44. doi: 10.1016/0022-2836(71)90204-x. [DOI] [PubMed] [Google Scholar]
  27. Schendel P. F., Defais M. The role of umuC gene product in mutagenesis by simple alkylating agents. Mol Gen Genet. 1980;177(4):661–665. doi: 10.1007/BF00272677. [DOI] [PubMed] [Google Scholar]
  28. Sedliaková M., Brozmanová J., Masek F., Kleibl K. Evidence that dimers remaining in preinduced Escherichia coli B/r Hcr+ become insensitive after DNA replication to the extract from Micrococcus luteus. Biophys J. 1981 Nov;36(2):429–441. doi: 10.1016/S0006-3495(81)84742-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Shinagawa H., Iwasaki H., Kato T., Nakata A. RecA protein-dependent cleavage of UmuD protein and SOS mutagenesis. Proc Natl Acad Sci U S A. 1988 Mar;85(6):1806–1810. doi: 10.1073/pnas.85.6.1806. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Shwartz H., Livneh Z. Dynamics of termination during in vitro replication of ultraviolet-irradiated DNA with DNA polymerase III holoenzyme of Escherichia coli. J Biol Chem. 1987 Aug 5;262(22):10518–10523. [PubMed] [Google Scholar]
  31. Valenzuela M. S., Inman R. B. Direction of bacteriophage lambda DNA replication in a thymine requiring Escherichia coli K-12 strain. Effect of thymidine concentration. Nucleic Acids Res. 1981 Dec 21;9(24):6975–6984. doi: 10.1093/nar/9.24.6975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Villani G., Boiteux S., Radman M. Mechanism of ultraviolet-induced mutagenesis: extent and fidelity of in vitro DNA synthesis on irradiated templates. Proc Natl Acad Sci U S A. 1978 Jul;75(7):3037–3041. doi: 10.1073/pnas.75.7.3037. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Wahl G. M., Stern M., Stark G. R. Efficient transfer of large DNA fragments from agarose gels to diazobenzyloxymethyl-paper and rapid hybridization by using dextran sulfate. Proc Natl Acad Sci U S A. 1979 Aug;76(8):3683–3687. doi: 10.1073/pnas.76.8.3683. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Walker G. C. Mutagenesis and inducible responses to deoxyribonucleic acid damage in Escherichia coli. Microbiol Rev. 1984 Mar;48(1):60–93. doi: 10.1128/mr.48.1.60-93.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Weigle J. J. Induction of Mutations in a Bacterial Virus. Proc Natl Acad Sci U S A. 1953 Jul;39(7):628–636. doi: 10.1073/pnas.39.7.628. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Witkin E. M. Ultraviolet mutagenesis and inducible DNA repair in Escherichia coli. Bacteriol Rev. 1976 Dec;40(4):869–907. doi: 10.1128/br.40.4.869-907.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Witkin E. M. Ultraviolet mutagenesis in strains of E. coli deficient in DNA polymerase. Nat New Biol. 1971 Jan 20;229(3):81–82. doi: 10.1038/newbio229081a0. [DOI] [PubMed] [Google Scholar]

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

RESOURCES