Bacterial Evolution Through the Selective Loss of Beneficial Genes: Trade-Offs in Expression Involving Two Loci

Corresponding author: Roberto Kolter, Harvard Medical School, 200 Longwood Ave., Boston, MA 02115., rkolter{at}hms.harvard.edu (E-mail)

Communicating editor: J. B. WALSH

The loss of preexisting genes or gene activities during evolution is a major mechanism of ecological specialization. Evolutionary processes that can account for gene loss or inactivation have so far been restricted to one of two mechanisms: direct selection for the loss of gene activities that are disadvantageous under the conditions of selection (i.e., antagonistic pleiotropy) and selection-independent genetic drift of neutral (or nearly neutral) mutations (i.e., mutation accumulation). In this study we demonstrate with an evolved strain of Escherichia coli that a third, distinct mechanism exists by which gene activities can be lost. This selection-dependent mechanism involves the expropriation of one gene's upstream regulatory element by a second gene via a homologous recombination event. Resulting from this genetic exchange is the activation of the second gene and a concomitant inactivation of the first gene. This gene-for-gene expression tradeoff provides a net fitness gain, even if the forfeited activity of the first gene can play a positive role in fitness under the conditions of selection.

This article has been cited by other articles:

				S. C. Sleight, C. Orlic, D. Schneider, and R. E. Lenski Genetic Basis of Evolutionary Adaptation by Escherichia coli to Stressful Cycles of Freezing, Thawing and Growth Genetics, September 1, 2008; 180(1): 431 - 443. [Abstract] [Full Text] [PDF]

				P. Sliwa and R. Korona Loss of dispensable genes is not adaptive in yeast PNAS, December 6, 2005; 102(49): 17670 - 17674. [Abstract] [Full Text] [PDF]

				S. Ullrich, M. Kube, S. Schubbe, R. Reinhardt, and D. Schuler A Hypervariable 130-Kilobase Genomic Region of Magnetospirillum gryphiswaldense Comprises a Magnetosome Island Which Undergoes Frequent Rearrangements during Stationary Growth J. Bacteriol., November 1, 2005; 187(21): 7176 - 7184. [Abstract] [Full Text] [PDF]

				R. J. Whitaker and J. F. Banfield Population Dynamics Through the Lens of Extreme Environments Reviews in Mineralogy and Geochemistry, January 1, 2005; 59(1): 259 - 277. [Full Text] [PDF]

				D. Faure, R. Frederick, D. Wloch, P. Portier, M. Blot, and J. Adams Genomic Changes Arising in Long-Term Stab Cultures of Escherichia coli J. Bacteriol., October 1, 2004; 186(19): 6437 - 6442. [Abstract] [Full Text] [PDF]