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Insertion Sequence-Driven Evolution of Escherichia coli in Chemostats

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Abstract

Insertion sequence (IS) elements are present in almost all bacterial genomes and are mobile enough to provide genomic tools to differentiate closely related isolates. They can be used to estimate genetic diversity and identify fitness-enhancing mutations during evolution experiments. Here, we determined the genomic distribution of eight IS elements in 120 genomes sampled from Escherichia coli populations that evolved in glucose- and phosphate-limited chemostats by comparison to the ancestral pattern. No significant differential transposition of the various IS types was detected across the environments. The phylogenies revealed substantial diversity amongst clones sampled from each chemostat, consistent with the phenotypic diversity within populations. Two IS-related changes were common to independent chemostats, suggesting parallel evolution. One of them corresponded to insertions of IS1 elements within rpoS encoding the master regulator of stress conditions. The other parallel event was an IS5-dependent deletion including mutY involved in DNA repair, thereby providing the molecular mechanism of generation of mutator clones in these evolving populations. These deletions occurred in different co-existing genotypes within single populations and were of various sizes. Moreover, differential locations of IS elements combined with their transpositional activity provided evolved clones with different phenotypic landscapes. Therefore, IS elements strongly influenced the evolutionary processes in continuous E. coli cultures by providing a way to modify both the global regulatory network and the mutation rates of evolving cells.

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Acknowledgments

We thank Thu Betteridge for technical support. This work was supported by the French Centre National de la Recherche Scientifique (CNRS), the University Joseph Fourier Grenoble, and the grant ANR-08-BLAN-0283-01 from the french Agence Nationale de la Recherche (ANR) program Blanc to D.S.

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Authors and Affiliations

  1. Laboratoire Adaptation et Pathogénie des Microorganismes, Université Joseph Fourier Grenoble 1, BP 170, 38042, Grenoble Cedex 9, France

    Joël Gaffé, Evelyne Coursange & Dominique Schneider

  2. CNRS UMR5163, 38042, Grenoble Cedex 9, France

    Joël Gaffé, Evelyne Coursange & Dominique Schneider

  3. School of Molecular Bioscience, The University of Sydney, Sydney, NSW, Australia

    Christopher McKenzie, Ram P. Maharjan & Tom Ferenci

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  1. Joël Gaffé
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  2. Christopher McKenzie
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  3. Ram P. Maharjan
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  4. Evelyne Coursange
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  5. Tom Ferenci
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  6. Dominique Schneider
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Correspondence to Dominique Schneider.

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Gaffé, J., McKenzie, C., Maharjan, R.P. et al. Insertion Sequence-Driven Evolution of Escherichia coli in Chemostats. J Mol Evol 72, 398–412 (2011). https://doi.org/10.1007/s00239-011-9439-2

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