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Genetics. Nov 2002; 162(3): 1055–1062.
PMCID: PMC1462320

Enrichment and elimination of mutY mutators in Escherichia coli populations.


The kinetics of mutator sweeps was followed in two independent populations of Escherichia coli grown for up to 350 generations in glucose-limited continuous culture. A rapid elevation of mutation rates was observed in both populations within 120-150 generations, as was apparent from major increases in the proportion of the populations with unselected mutations in fhuA. The increase in mutation rates was due to sweeps by mutY mutators. In both cultures, the enrichment of mutators resulted from hitchhiking with identified beneficial mutations increasing fitness under glucose limitation; mutY hitchhiked with mgl mutations in one culture and ptsG in the other. In both cases, mutators were enriched to constitute close to 100% of the population before a periodic selection event reduced the frequency of unselected mutations and mutators in the cultures. The high proportion of mutators persisted for 150 generations in one population but began to be eliminated within 50 generations in the other. The persistence of mutator, as well as experimental data showing that mutY bacteria were as fit as near-isogenic mutY(+) bacteria in competition experiments, suggest that mutator load by deleterious mutations did not explain the rapidly diminishing proportion of mutators in the populations. The nonmutators sweeping out mutators were also unlikely to have arisen by reversion or antimutator mutations; the mutY mutations were major deletions in each case and the bacteria sweeping out mutators contained intact mutY. By following mgl allele frequencies in one population, we discovered that mutators were outcompeted by bacteria that had rare mgl mutations previously as well as additional beneficial mutation(s). The pattern of appearance of mutY, but not its elimination, conforms to current models of mutator sweeps in bacterial populations. A mutator with a narrow mutational spectrum like mutY may be lost if the requirement for beneficial mutations is for changes other than GC --> TA transversions. Alternatively, epistatic interactions between mutator mutation and beneficial mutations need to be postulated to explain mutator elimination.

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Selected References

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  • ACOG. Committee opinion: number 277, November 2002. Patients, medicine and the interests of patients: applying general principles to gene patenting. Obstet Gynecol. 2002 Nov;100(5 Pt 1):1051–1056. [PubMed]
  • Curtis SJ, Epstein W. Phosphorylation of D-glucose in Escherichia coli mutants defective in glucosephosphotransferase, mannosephosphotransferase, and glucokinase. J Bacteriol. 1975 Jun;122(3):1189–1199. [PMC free article] [PubMed]
  • Death A, Notley L, Ferenci T. Derepression of LamB protein facilitates outer membrane permeation of carbohydrates into Escherichia coli under conditions of nutrient stress. J Bacteriol. 1993 Mar;175(5):1475–1483. [PMC free article] [PubMed]
  • Denamur Erick, Bonacorsi Stéphane, Giraud Antoine, Duriez Patrick, Hilali Farida, Amorin Christine, Bingen Edouard, Andremont Antoine, Picard Bertrand, Taddei François, et al. High frequency of mutator strains among human uropathogenic Escherichia coli isolates. J Bacteriol. 2002 Jan;184(2):605–609. [PMC free article] [PubMed]
  • Drake JW. A constant rate of spontaneous mutation in DNA-based microbes. Proc Natl Acad Sci U S A. 1991 Aug 15;88(16):7160–7164. [PMC free article] [PubMed]
  • Helling RB, Vargas CN, Adams J. Evolution of Escherichia coli during growth in a constant environment. Genetics. 1987 Jul;116(3):349–358. [PMC free article] [PubMed]
  • LeClerc JE, Li B, Payne WL, Cebula TA. High mutation frequencies among Escherichia coli and Salmonella pathogens. Science. 1996 Nov 15;274(5290):1208–1211. [PubMed]
  • Manch K, Notley-McRobb L, Ferenci T. Mutational adaptation of Escherichia coli to glucose limitation involves distinct evolutionary pathways in aerobic and oxygen-limited environments. Genetics. 1999 Sep;153(1):5–12. [PMC free article] [PubMed]
  • Mao EF, Lane L, Lee J, Miller JH. Proliferation of mutators in A cell population. J Bacteriol. 1997 Jan;179(2):417–422. [PMC free article] [PubMed]
  • Nghiem Y, Cabrera M, Cupples CG, Miller JH. The mutY gene: a mutator locus in Escherichia coli that generates G.C----T.A transversions. Proc Natl Acad Sci U S A. 1988 Apr;85(8):2709–2713. [PMC free article] [PubMed]
  • Notley L, Ferenci T. Differential expression of mal genes under cAMP and endogenous inducer control in nutrient-stressed Escherichia coli. Mol Microbiol. 1995 Apr;16(1):121–129. [PubMed]
  • Notley-McRobb L, Ferenci T. Adaptive mgl-regulatory mutations and genetic diversity evolving in glucose-limited Escherichia coli populations. Environ Microbiol. 1999 Feb;1(1):33–43. [PubMed]
  • Notley-McRobb L, Ferenci T. The generation of multiple co-existing mal-regulatory mutations through polygenic evolution in glucose-limited populations of Escherichia coli. Environ Microbiol. 1999 Feb;1(1):45–52. [PubMed]
  • Notley-McRobb L, Ferenci T. Experimental analysis of molecular events during mutational periodic selections in bacterial evolution. Genetics. 2000 Dec;156(4):1493–1501. [PMC free article] [PubMed]
  • Notley-McRobb L, Ferenci T. Substrate specificity and signal transduction pathways in the glucose-specific enzyme II (EII(Glc)) component of the Escherichia coli phosphotransferase system. J Bacteriol. 2000 Aug;182(16):4437–4442. [PMC free article] [PubMed]
  • Notley-McRobb Lucinda, King Thea, Ferenci Thomas. rpoS mutations and loss of general stress resistance in Escherichia coli populations as a consequence of conflict between competing stress responses. J Bacteriol. 2002 Feb;184(3):806–811. [PMC free article] [PubMed]
  • Notley-McRobb Lucinda, Pinto Rachel, Seeto Shona, Ferenci Thomas. Regulation of mutY and nature of mutator mutations in Escherichia coli populations under nutrient limitation. J Bacteriol. 2002 Feb;184(3):739–745. [PMC free article] [PubMed]
  • Tenaillon O, Toupance B, Le Nagard H, Taddei F, Godelle B. Mutators, population size, adaptive landscape and the adaptation of asexual populations of bacteria. Genetics. 1999 Jun;152(2):485–493. [PMC free article] [PubMed]
  • Radman M, Taddei F, Matic I. DNA repair systems and bacterial evolution. Cold Spring Harb Symp Quant Biol. 2000;65:11–19. [PubMed]
  • Tröbner W, Piechocki R. Competition between isogenic mutS and mut+ populations of Escherichia coli K12 in continuously growing cultures. Mol Gen Genet. 1984;198(1):175–176. [PubMed]
  • Rainey PB. Evolutionary genetics: The economics of mutation. Curr Biol. 1999 May 20;9(10):R371–R373. [PubMed]
  • Tröbner W, Piechocki R. Selection against hypermutability in Escherichia coli during long term evolution. Mol Gen Genet. 1984;198(1):177–178. [PubMed]
  • Sniegowski PD, Gerrish PJ, Lenski RE. Evolution of high mutation rates in experimental populations of E. coli. Nature. 1997 Jun 12;387(6634):703–705. [PubMed]

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