Skip to main content
NCBI home page
Genetics logoLink to Genetics
. 2000 Jan;154(1):49–59. doi: 10.1093/genetics/154.1.49

Some features of the mutability of bacteria during nonlethal selection.

V G Godoy 1, F S Gizatullin 1, M S Fox 1
PMCID: PMC1460914  PMID: 10628968

Abstract

We describe the mutability of the Trp(-) chromosomal +1 frameshift mutation trpE7999 during nonlethal selection, finding that the appearance of Trp(+) revertants behaves similarly to that of episomal Lac(+) revertants. In addition, we show that a feature of the Lac(+) and Trp(+) mutability is the accumulation of Trp(+) and Lac(+) revertants with additional unselected mutations, most of which are not due to heritable mutators. The cells undergoing nonlethal selection apparently experience an epigenetic change resulting in a subset of bacteria with elevated mutability that often remain hypermutable for the duration of selection. The epigenetic change provoked by nonlethal selection appears to be mediated by a unique function provided by the F'128 episome.

Full Text

The Full Text of this article is available as a PDF (192.3 KB).

Selected References

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

  1. Andersson D. I., Slechta E. S., Roth J. R. Evidence that gene amplification underlies adaptive mutability of the bacterial lac operon. Science. 1998 Nov 6;282(5391):1133–1135. doi: 10.1126/science.282.5391.1133. [DOI] [PubMed] [Google Scholar]
  2. Bronson M. J., Yanofsky C. Letter to the editor: Characterization of mutations in the tryptophan operon of Escherichia coli by RNA nucleotide sequencing. J Mol Biol. 1974 Oct 5;88(4):913–915. doi: 10.1016/0022-2836(74)90407-0. [DOI] [PubMed] [Google Scholar]
  3. Brotcorne-Lannoye A., Maenhaut-Michel G. Role of RecA protein in untargeted UV mutagenesis of bacteriophage lambda: evidence for the requirement for the dinB gene. Proc Natl Acad Sci U S A. 1986 Jun;83(11):3904–3908. doi: 10.1073/pnas.83.11.3904. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Cairns J., Foster P. L. Adaptive reversion of a frameshift mutation in Escherichia coli. Genetics. 1991 Aug;128(4):695–701. doi: 10.1093/genetics/128.4.695. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cupples C. G., Miller J. H. A set of lacZ mutations in Escherichia coli that allow rapid detection of each of the six base substitutions. Proc Natl Acad Sci U S A. 1989 Jul;86(14):5345–5349. doi: 10.1073/pnas.86.14.5345. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Foster P. L. Adaptive mutation: has the unicorn landed? Genetics. 1998 Apr;148(4):1453–1459. doi: 10.1093/genetics/148.4.1453. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Foster P. L., Cairns J. Mechanisms of directed mutation. Genetics. 1992 Aug;131(4):783–789. doi: 10.1093/genetics/131.4.783. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Foster P. L. Nonadaptive mutations occur on the F' episome during adaptive mutation conditions in Escherichia coli. J Bacteriol. 1997 Mar;179(5):1550–1554. doi: 10.1128/jb.179.5.1550-1554.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Foster P. L. Population dynamics of a Lac- strain of Escherichia coli during selection for lactose utilization. Genetics. 1994 Oct;138(2):253–261. doi: 10.1093/genetics/138.2.253. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Foster P. L., Trimarchi J. M. Adaptive reversion of a frameshift mutation in Escherichia coli by simple base deletions in homopolymeric runs. Science. 1994 Jul 15;265(5170):407–409. doi: 10.1126/science.8023164. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Foster P. L., Trimarchi J. M. Conjugation is not required for adaptive reversion of an episomal frameshift mutation in Escherichia coli. J Bacteriol. 1995 Nov;177(22):6670–6671. doi: 10.1128/jb.177.22.6670-6671.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Foster P. L., Trimarchi J. M., Maurer R. A. Two enzymes, both of which process recombination intermediates, have opposite effects on adaptive mutation in Escherichia coli. Genetics. 1996 Jan;142(1):25–37. doi: 10.1093/genetics/142.1.25. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hall B. G. Spontaneous point mutations that occur more often when advantageous than when neutral. Genetics. 1990 Sep;126(1):5–16. doi: 10.1093/genetics/126.1.5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Harris R. S., Bull H. J., Rosenberg S. M. A direct role for DNA polymerase III in adaptive reversion of a frameshift mutation in Escherichia coli. Mutat Res. 1997 Apr 14;375(1):19–24. doi: 10.1016/s0027-5107(96)00244-8. [DOI] [PubMed] [Google Scholar]
  15. Harris R. S., Feng G., Ross K. J., Sidhu R., Thulin C., Longerich S., Szigety S. K., Winkler M. E., Rosenberg S. M. Mismatch repair protein MutL becomes limiting during stationary-phase mutation. Genes Dev. 1997 Sep 15;11(18):2426–2437. doi: 10.1101/gad.11.18.2426. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Harris R. S., Longerich S., Rosenberg S. M. Recombination in adaptive mutation. Science. 1994 Apr 8;264(5156):258–260. doi: 10.1126/science.8146657. [DOI] [PubMed] [Google Scholar]
  17. Kennedy A. R., Fox M., Murphy G., Little J. B. Relationship between x-ray exposure and malignant transformation in C3H 10T1/2 cells. Proc Natl Acad Sci U S A. 1980 Dec;77(12):7262–7266. doi: 10.1073/pnas.77.12.7262. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kim S. R., Maenhaut-Michel G., Yamada M., Yamamoto Y., Matsui K., Sofuni T., Nohmi T., Ohmori H. Multiple pathways for SOS-induced mutagenesis in Escherichia coli: an overexpression of dinB/dinP results in strongly enhancing mutagenesis in the absence of any exogenous treatment to damage DNA. Proc Natl Acad Sci U S A. 1997 Dec 9;94(25):13792–13797. doi: 10.1073/pnas.94.25.13792. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Loeb L. A. Transient expression of a mutator phenotype in cancer cells. Science. 1997 Sep 5;277(5331):1449–1450. doi: 10.1126/science.277.5331.1449. [DOI] [PubMed] [Google Scholar]
  20. Low K. B. Escherichia coli K-12 F-prime factors, old and new. Bacteriol Rev. 1972 Dec;36(4):587–607. doi: 10.1128/br.36.4.587-607.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Meuth M., Richards B., Schneider B. The conditional mutator phenotype in human tumor cells: correction. Science. 1999 Jan 29;283(5402):641–641. doi: 10.1126/science.283.5402.639d. [DOI] [PubMed] [Google Scholar]
  22. Miller J. H. Spontaneous mutators in bacteria: insights into pathways of mutagenesis and repair. Annu Rev Microbiol. 1996;50:625–643. doi: 10.1146/annurev.micro.50.1.625. [DOI] [PubMed] [Google Scholar]
  23. Ninio J. Transient mutators: a semiquantitative analysis of the influence of translation and transcription errors on mutation rates. Genetics. 1991 Nov;129(3):957–962. doi: 10.1093/genetics/129.3.957. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Peters J. E., Benson S. A. Redundant transfer of F' plasmids occurs between Escherichia coli cells during nonlethal selections. J Bacteriol. 1995 Feb;177(3):847–850. doi: 10.1128/jb.177.3.847-850.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Radicella J. P., Park P. U., Fox M. S. Adaptive mutation in Escherichia coli: a role for conjugation. Science. 1995 Apr 21;268(5209):418–420. doi: 10.1126/science.7716545. [DOI] [PubMed] [Google Scholar]
  26. Richards B., Zhang H., Phear G., Meuth M. Conditional mutator phenotypes in hMSH2-deficient tumor cell lines. Science. 1997 Sep 5;277(5331):1523–1526. doi: 10.1126/science.277.5331.1523. [DOI] [PubMed] [Google Scholar]
  27. Rosche W. A., Foster P. L. The role of transient hypermutators in adaptive mutation in Escherichia coli. Proc Natl Acad Sci U S A. 1999 Jun 8;96(12):6862–6867. doi: 10.1073/pnas.96.12.6862. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Rosenberg S. M., Harris R. S., Longerich S., Galloway A. M. Recombination-dependent mutation in non-dividing cells. Mutat Res. 1996 Feb 19;350(1):69–76. doi: 10.1016/0027-5107(95)00092-5. [DOI] [PubMed] [Google Scholar]
  29. Rosenberg S. M., Harris R. S., Torkelson J. Molecular handles on adaptive mutation. Mol Microbiol. 1995 Oct;18(2):185–189. doi: 10.1111/j.1365-2958.1995.mmi_18020185.x. [DOI] [PubMed] [Google Scholar]
  30. Rosenberg S. M., Thulin C., Harris R. S. Transient and heritable mutators in adaptive evolution in the lab and in nature. Genetics. 1998 Apr;148(4):1559–1566. doi: 10.1093/genetics/148.4.1559. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Torkelson J., Harris R. S., Lombardo M. J., Nagendran J., Thulin C., Rosenberg S. M. Genome-wide hypermutation in a subpopulation of stationary-phase cells underlies recombination-dependent adaptive mutation. EMBO J. 1997 Jun 2;16(11):3303–3311. doi: 10.1093/emboj/16.11.3303. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES