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. 1985 Feb;82(4):1180–1183. doi: 10.1073/pnas.82.4.1180

Mutagenic DNA repair in Streptomyces.

J Stonesifer, R H Baltz
PMCID: PMC397218  PMID: 3856255

Abstract

Streptomyces fradiae JS6 (mcr-6) is defective in the repair of potentially lethal damage to DNA induced by mitomycin C (MC), hydroxylamine (NH2OH), methyl methanesulfonate (MMS), 4-nitroquinoline 1-oxide (NQO), N-methyl-N'-nitro-N-nitrosoguanidine (MNNG), and ultraviolet light (UV), but it exhibits nearly normal sensitivity to ethyl methanesulfonate (EMS)-induced lethality. JS6 is substantially less mutable by MNNG, MMS, NQO, UV, NH2OH, and also EMS than is the parental strain. A spontaneous revertant of JS6 showed wild-type levels of resistance to all of these agents and wild-type levels of induced mutagenesis, indicating that a single mutation caused the multiple traits displayed by JS6. The mcr-6 gene product thus appears to control an error-prone (mutagenic) DNA repair system. Mediation of EMS mutagenesis by an error-prone repair pathway in S. fradiae, rather than by direct mispairing as in Escherichia coli, suggests that the streptomycetes have evolved more efficient error-avoidance mechanisms than those commonly observed in the single-celled eubacteria.

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Selected References

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

  1. Baltz R. H. Genetic recombination in Streptomyces fradiae by protoplast fusion and cell regeneration. J Gen Microbiol. 1978 Jul;107(1):93–102. doi: 10.1099/00221287-107-1-93. [DOI] [PubMed] [Google Scholar]
  2. Baltz R. H., Seno E. T. Properties of Streptomyces fradiae mutants blocked in biosynthesis of the macrolide antibiotic tylosin. Antimicrob Agents Chemother. 1981 Aug;20(2):214–225. doi: 10.1128/aac.20.2.214. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Baltz R. H., Seno E. T., Stonesifer J., Wild G. M. Biosynthesis of the macrolide antibiotic tylosin. A preferred pathway from tylactone to tylosin. J Antibiot (Tokyo) 1983 Feb;36(2):131–141. doi: 10.7164/antibiotics.36.131. [DOI] [PubMed] [Google Scholar]
  4. Benigni R., Petrov P. A., Carere A. Estimate of the genome size by renaturation studies in Streptomyces. Appl Microbiol. 1975 Aug;30(2):324–326. doi: 10.1128/am.30.2.324-326.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Drake J. W., Baltz R. H. The biochemistry of mutagenesis. Annu Rev Biochem. 1976;45:11–37. doi: 10.1146/annurev.bi.45.070176.000303. [DOI] [PubMed] [Google Scholar]
  6. Drake J. W. Comparative rates of spontaneous mutation. Nature. 1969 Mar 22;221(5186):1132–1132. doi: 10.1038/2211132a0. [DOI] [PubMed] [Google Scholar]
  7. Fishman S. E., Hershberger C. L. Amplified DNA in Streptomyces fradiae. J Bacteriol. 1983 Aug;155(2):459–466. doi: 10.1128/jb.155.2.459-466.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Gottesman S. Genetic control of the SOS system in E. coli. Cell. 1981 Jan;23(1):1–2. doi: 10.1016/0092-8674(81)90261-0. [DOI] [PubMed] [Google Scholar]
  9. Hopwood D. A. Genetic analysis and genome structure in Streptomyces coelicolor. Bacteriol Rev. 1967 Dec;31(4):373–403. doi: 10.1128/br.31.4.373-403.1967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Hopwood D. A., Merrick M. J. Genetics of antibiotic production. Bacteriol Rev. 1977 Sep;41(3):595–635. doi: 10.1128/br.41.3.595-635.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Ikenaga M., Ichikawa-Ryo H., Kondo S. The major cause of inactivation and mutation by 4-nitroquinoline 1-oixde in Escherichia coli: excisable 4NQO-purine adducts. J Mol Biol. 1975 Feb 25;92(2):341–356. doi: 10.1016/0022-2836(75)90233-8. [DOI] [PubMed] [Google Scholar]
  12. Ishii Y., Kondo S. Comparative analysis of deletion and base-change mutabilities of Escherichia coli B strains differing in DNA repair capacity (wild-type, uvrA-, polA-, recA-) by various mutagens. Mutat Res. 1975 Jan;27(1):27–44. doi: 10.1016/0027-5107(75)90271-7. [DOI] [PubMed] [Google Scholar]
  13. Kondo S., Ichikawa H., Iwo K., Kato T. Base-change mutagenesis and prophage induction in strains of Escherichia coli with different DNA repair capacities. Genetics. 1970 Oct;66(2):187–217. doi: 10.1093/genetics/66.2.187. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Lindahl T. DNA repair enzymes. Annu Rev Biochem. 1982;51:61–87. doi: 10.1146/annurev.bi.51.070182.000425. [DOI] [PubMed] [Google Scholar]
  15. McPartland A., Green L., Echols H. Control of recA gene RNA in E. coli: regulatory and signal genes. Cell. 1980 Jul;20(3):731–737. doi: 10.1016/0092-8674(80)90319-0. [DOI] [PubMed] [Google Scholar]
  16. Ono H., Hintermann G., Crameri R., Wallis G., Hütter R. Reiterated DNA sequences in a mutant strain of Streptomyces glaucescens and cloning of the sequence in Escherichia coli. Mol Gen Genet. 1982;186(1):106–110. doi: 10.1007/BF00422920. [DOI] [PubMed] [Google Scholar]
  17. Phizicky E. M., Roberts J. W. Induction of SOS functions: regulation of proteolytic activity of E. coli RecA protein by interaction with DNA and nucleoside triphosphate. Cell. 1981 Jul;25(1):259–267. doi: 10.1016/0092-8674(81)90251-8. [DOI] [PubMed] [Google Scholar]
  18. Prakash L. Characterization of postreplication repair in Saccharomyces cerevisiae and effects of rad6, rad18, rev3 and rad52 mutations. Mol Gen Genet. 1981;184(3):471–478. doi: 10.1007/BF00352525. [DOI] [PubMed] [Google Scholar]
  19. Prakash L., Higgins D. Role of DNA repair in ethyl methanesulfonate-induced mutagenesis in Saccharomyces cerevisiae. Carcinogenesis. 1982;3(4):439–444. doi: 10.1093/carcin/3.4.439. [DOI] [PubMed] [Google Scholar]
  20. Prakash L. Lack of chemically induced mutation in repair-deficient mutants of yeast. Genetics. 1974 Dec;78(4):1101–1118. doi: 10.1093/genetics/78.4.1101. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Ray U., Bartenstein L., Drake J. W. Inactivation of bacteriophage T4 by ethyl methanesulfonate: influence of host and viral genotypes. J Virol. 1972 Mar;9(3):440–447. doi: 10.1128/jvi.9.3.440-447.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Robinson M., Lewis E., Napier E. Occurrence of reiterated DNA sequences in strains of Streptomyces produced by an interspecific protoplast fusion. Mol Gen Genet. 1981;182(2):336–340. doi: 10.1007/BF00269680. [DOI] [PubMed] [Google Scholar]
  23. Schrempf H. Deletion and amplification of DNA sequences in melanin-negative variants of Streptomyces reticuli. Mol Gen Genet. 1983;189(3):501–505. doi: 10.1007/BF00325917. [DOI] [PubMed] [Google Scholar]
  24. Schrempf H. Plasmid loss and changes within the chromosomal DNA of Streptomyces reticuli. J Bacteriol. 1982 Aug;151(2):701–707. doi: 10.1128/jb.151.2.701-707.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Sedgwick S. G., Yarranton G. T. How cells in distress use SOS. Nature. 1982 Apr 15;296(5858):606–607. doi: 10.1038/296606a0. [DOI] [PubMed] [Google Scholar]
  26. Seno E. T., Baltz R. H. Properties of S-adenosyl-L-methionine:macrocin O-methyltransferase in extracts of Streptomyces fradiae strains which produce normal or elevated levels of tylosin and in mutants blocked in specific O-methylations. Antimicrob Agents Chemother. 1981 Sep;20(3):370–377. doi: 10.1128/aac.20.3.370. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Seno E. T., Baltz R. H. S-Adenosyl-L-methionine: macrocin O-methyltransferase activities in a series of Streptomyces fradiae mutants that produce different levels of the macrolide antibiotic tylosin. Antimicrob Agents Chemother. 1982 May;21(5):758–763. doi: 10.1128/aac.21.5.758. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Shanabruch W. G., Rein R. P., Behlau I., Walker G. C. Mutagenesis, by methylating and ethylating agents, in mutH, mutL, mutS, and uvrD mutants of Salmonella typhimurium LT2. J Bacteriol. 1983 Jan;153(1):33–44. doi: 10.1128/jb.153.1.33-44.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]

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