The origin of mutants under selection: How natural selection mimics mutability (adaptive mutation)

  • Maisnier-Patin S
  • Roth J
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Abstract

Selection detects mutants but does not cause mutations. Contrary to this dictum, Cairns and Foster plated a leaky lac mutant of E. coli on lactose medium and saw revertant (Lac+) colonies accumulate with time above the non-growing lawn. This result suggested that bacteria mutagenize their own genome when growth is blocked. However, the conclusion is suspect in the light of recent evidence that revertant colonies are initiated by pre-existing cells with multiple copies the conjugative F’lac plasmid that carries the lac mutation. In some plated cells, the plasmid includes a tandem lac duplication and provides sufficient LacZ to support slow growth leading to an unstable Lac+ colony. Other plated cells have multiple copies of a simple F’lac and sufficient LacZ activity for plasmid replication but not cell division. Repeated plasmid replication in non-growing cells increases the likelihood of a reversion event. Reversion to lac+ triggers exponential cell growth leading to a stable Lac+ revertant colony. Cells with multiple copies of the F’lac plasmid have an increased mutation rate, because the plasmid encodes the error-prone (mutagenic) DNA polymerase, DinB. Without DinB, unstable and stable Lac+ revertant types form in equal numbers and arise with no mutagenesis. Amplification and selection are central to behavior of the Cairns-Foster system, while mutagenesis is a system-specific side-effect of dinB-lac co-amplification. Study this system has revealed several general principles: a) In all populations, gene duplications are frequent stable genetic polymorphisms. b) Common near-neutral mutant alleles can gain a positive phenotype when amplified and c) Natural selection can operate without cell division on variability generated by over- replication of local genome sub-regions.

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Authors

  • Sophie Maisnier-Patin

  • John R Roth

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