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Originally published as Genetics Published Articles Ahead of Print on February 2, 2009.
Genetics, Vol. 181, 1521-1533, April 2009, Copyright © 2009
doi:10.1534/genetics.108.099523
Episodic Selection and the Maintenance of Competence and Natural Transformation in Bacillus subtilis
P. J. Johnsen*,
,
D. Dubnau
and
B. R. Levin,1
* Department of Pharmacy, Faculty of Medicine, University of Tromsø, 9037 Tromsø, Norway, Public Health Research Institute and Department of Microbiology and Molecular Genetics, University of Medicine and Dentistry of New Jersey, Newark, New Jersey 07103 and Department of Biology, Rollins Research Center, Emory University, Atlanta, Georgia 30322
1 Corresponding author: Department of Biology, Emory University, 1510 Clifton Rd., Atlanta, GA 30322.
E-mail: blevin{at}emory.edu
We present a new hypothesis for the selective pressures responsible for maintaining natural competence and transformation. Our hypothesis is based in part on the observation that in Bacillus subtilis, where transformation is widespread, competence is associated with periods of nongrowth in otherwise growing populations. As postulated for the phenomenon of persistence, the short-term fitness cost associated with the production of transiently nongrowing bacteria can be compensated for and the capacity to produce these competent cells can be favored due to episodes where the population encounters conditions that kill dividing bacteria. With the aid of a mathematical model, we demonstrate that under realistic conditions this "episodic selection" for transiently nongrowing (persisting) bacteria can maintain competence for the uptake and expression of exogenous DNA transformation. We also show that these conditions for maintaining competence are dramatically augmented even by rare episodes where selection favors transformants. Using experimental populations of B. subtilis and antibiotic-mediated episodic selection, we test and provide support for the validity of the assumptions behind this model and the predictions generated from our analysis of its properties. We discuss the potential generality of episodic selection for the maintenance of competence in other naturally transforming species of bacteria and critically evaluate other hypotheses for the maintenance (and evolution) of competence and their relationship to this hypothesis.
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Genetics 2009 181: NP.
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