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Originally published as Genetics Published Articles Ahead of Print on October 16, 2004.

Genetics, Vol. 169, 523-532, February 2005, Copyright © 2005
doi:10.1534/genetics.104.035717

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Long-Term Experimental Evolution in Escherichia coli. XII. DNA Topology as a Key Target of Selection

Estelle Crozat*, Nadège Philippe*, Richard E. Lenski{dagger}, Johannes Geiselmann* and Dominique Schneider*,1

* Laboratoire Adaptation et Pathogénie des Microorganismes, Université Joseph Fourier, Institut Jean Roget, CNRS UMR 5163, F-38041 Grenoble, France
{dagger} Department of Microbiology and Molecular Genetics, Michigan State University, East Lansing, Michigan 48824

1 Corresponding author: Laboratoire Adaptation et Pathogénie des Microorganismes, Facultés Médecine/Pharmacie, Université Joseph Fourier, Institut Jean Roget, 38700 La Tronche, France.
E-mail: dominique.schneider{at}ujf-grenoble.fr

The genetic bases of adaptation are being investigated in 12 populations of Escherichia coli, founded from a common ancestor and serially propagated for 20,000 generations, during which time they achieved substantial fitness gains. Each day, populations alternated between active growth and nutrient exhaustion. DNA supercoiling in bacteria is influenced by nutritional state, and DNA topology helps coordinate the overall pattern of gene expression in response to environmental changes. We therefore examined whether the genetic controls over supercoiling might have changed during the evolution experiment. Parallel changes in topology occurred in most populations, with the level of DNA supercoiling increasing, usually in the first 2000 generations. Two mutations in the topA and fis genes that control supercoiling were discovered in a population that served as the focus for further investigation. Moving the mutations, alone and in combination, into the ancestral background had an additive effect on supercoiling, and together they reproduced the net change in DNA topology observed in this population. Moreover, both mutations were beneficial in competition experiments. Clonal interference involving other beneficial DNA topology mutations was also detected. These findings define a new class of fitness-enhancing mutations and indicate that the control of DNA supercoiling can be a key target of selection in evolving bacterial populations.




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