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Open Access Research article

A case of adaptation through a mutation in a tandem duplication during experimental evolution in Escherichia coli

Ram P Maharjan1, Joël Gaffé23, Jessica Plucain23, Martin Schliep1, Lei Wang45, Lu Feng45, Olivier Tenaillon67, Thomas Ferenci1 and Dominique Schneider23*

Author Affiliations

1 School of Molecular Bioscience, University of Sydney, Sydney, NSW, 2006, Australia

2 Laboratoire Adaptation et Pathogénie des Micro-organismes, Université Joseph Fourier Grenoble, BP 170, Grenoble cedex 9, F-38042, France

3 CNRS UMR5163, Grenoble cedex 9, F-38042, France

4 TEDA School of Biological Sciences and Biotechnology, Nankai University, 23 Hongda Street, Tianjin, 300457, P.R. China

5 Key Laboratory of Molecular Microbiology and Technology, Ministry of Education, 23 Hongda Street, Tianjin, 300457, P. R. China

6 INSERM, UMR-S 722, Paris, F-75018, France

7 Université Paris Diderot, Sorbonne Paris Cité, UMR-S 722 INSERM, Paris, F-75018, France

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BMC Genomics 2013, 14:441  doi:10.1186/1471-2164-14-441

Published: 3 July 2013

Abstract

Background

DNA duplications constitute important precursors for genome variation. Here we analyzed an unequal duplication harboring a beneficial mutation that may provide alternative evolutionary outcomes.

Results

We characterized this evolutionary event during experimental evolution for only 100 generations of an Escherichia coli strain under glucose limitation within chemostats. By combining Insertion Sequence based Restriction Length Polymorphism experiments, pulsed field gel electrophoresis and two independent genome re-sequencing experiments, we identified an evolved lineage carrying a 180 kb duplication of the 46’ region of the E. coli chromosome. This evolved duplication revealed a heterozygous state, with one copy harboring a 2668 bp deletion that included part of the ogrK gene and both the yegR and yegS genes. By genetically manipulating ancestral and evolved strains, we showed that the single yegS inactivation was sufficient to confer a frequency dependent fitness increase under the chemostat selective conditions in both the ancestor and evolved genetic contexts, implying that the duplication itself was not a direct fitness contributor. Nonetheless, the heterozygous duplicated state was relatively stable in the conditions prevailing during evolution in chemostats, in striking contrast to non selective conditions in which the duplication resolved at high frequency into either its ancestral or deleted copy.

Conclusions

Our results suggest that the duplication state may constitute a second order selection process providing higher evolutionary potential. Moreover, its heterozygous nature may provide differential evolutionary opportunities in alternating environments. Our results also highlighted how careful analyses of whole genome data are needed to identify such complex rearrangements.

Keywords:
Experimental evolution; Chemostats; Escherichia coli; Duplication; Heterozygous duplication; Insertion sequence elements; Frequency-dependent selection; Indirect selection