Cited by 62Evolution and Genetic DynamicsBacterial Genetics and BiotechnologyGenomics and Chromatin Dynamics

Parallel Genetic and Phenotypic Evolution of DNA Superhelicity in Experimental Populations of Escherichia coli

Crozat, E., Winkworth, C., Gaffe, J., Hallin, P. F., Riley, M. A., Lenski, R. E., Schneider, D.·2010·Molecular Biology and Evolution

Abstract

DNA supercoiling is the master function that interconnects chromosome structure and global gene transcription. This function has recently been shown to be under strong selection in Escherichia coli. During the evolution of 12 initially identical populations propagated in a defined environment for 20,000 generations, parallel increases in DNA supercoiling were observed in ten populations. The genetic changes associated with the increased supercoiling were examined in one population, and beneficial mutations in the genes topA (encoding topoisomerase I) and fis (encoding a histone-like protein) were identified. To elucidate the molecular basis and impact of these changes, we quantified the level of genetic, phenotypic, and molecular parallelism linked to DNA supercoiling in all 12 evolving populations. First, sequence determination of DNA topology-related loci revealed strong genetic parallelism, with mutations concentrated in three genes (topA, fis, and dusB), although the populations had different alleles at each locus. Statistical analyses of these polymorphisms implied the action of positive selection and, moreover, suggested that fis and dusB, which belong to the same operon, have related functions. Indeed, we demonstrated that DusB regulates the expression of fis by both experimental and phylogenetic analyses. Second, molecular analyses of five mutations in fis and dusB affecting the transcription, translation, and protein activity of Fis also revealed strong parallelism in the resulting phenotypic effects. Third, artificially increasing DNA supercoiling in one of the two populations that lacked DNA topology changes led to a significant fitness increase. The high levels of molecular and genetic parallelism, targeting a small subset of the many genes involved in DNA supercoiling, indicate that changes in DNA superhelicity have been important in the evolution of these populations. Surprisingly, however, most of the evolved alleles we tested had either no detectable or slightly deleterious effects on fitness, despite these signatures of positive selection.

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Crossref · 10.1093/molbev/msq099

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Authors
Crozat, E., Winkworth, C., Gaffe, J., Hallin, P. F., Riley, M. A., Lenski, R. E., & Schneider, D.
Affiliations
  • Centre National de la Recherche Scientifique (FR)
  • Technical University of Denmark (DK)
  • Michigan State University (US)
Corresponding author
Schneider, D.
Venue
Molecular Biology and Evolution
Published
2010-04-14
Volume
27
Issue
9
Pages
2113-2128
ISSN
  • 0737-4038 (ISSN-L)
  • 1537-1719
OpenAlex
W2167365021
Cited by
62
References
103
Citations by year
2026: 2 · 2025: 2 · 2024: 5 · 2023: 1 · 2022: 3 · 2021: 4 · 2020: 5 · 2019: 1 · 2018: 3 · 2017: 4 · 2016: 2 · 2015: 6 · 2014: 2 · 2013: 6 · 2012: 9
FWCI
3.95
Type
journal article
Language
en
Open access
closed
Locations
  • Molecular Biology and Evolution (publishedVersion)
  • PubMed (publishedVersion)
  • HAL (submittedVersion)
  • Technical University of Denmark, DTU Orbit (Technical University of Denmark, DTU) (submittedVersion)
Funders
Agence Nationale de la Recherche (ANR-08-GENM-0023)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
Keywords
DNA supercoiling, DNA superhelicity, parallel evolution, Escherichia coli, topA, topoisomerase I, FIS, positive selection, fitness effects of mutations, gene expression regulation, operon regulation, experimental evolution, chromosome structure
MeSH terms
DNA, Superhelical, Escherichia coli, Phenotype, Evolution, Molecular

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