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Copyright Ó 2009 by the Genetics Society of America 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 andMolecular 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 Manuscript received December 9, 2008 Accepted for publication January 25, 2009 ABSTRACT 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 thesecompetent 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 theseconditions 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 ofepisodic 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.


ACTERIA may not have sex often, but when they do, it can be really good, at least evolutionarily. Sex, or more precisely recombination, broadly defined toinclude the acquisition and incorporation of DNA by horizontal gene transfer (HGT) from other organisms, enables bacteria to sample and obtain genes from the entire prokaryotic, archeal, and even eukaryotic DNA ‘‘sequence space.’’ As a result, the rate of adaptive evolution in bacteria need not be limited by the slow pace of sequential selection for small genetic changes generated by mutation. Throughhorizontal transfer, bacteria can acquire genes that have already passed through the gauntlet of natural selection in the same or even distantly related species living in different habitats. For many bacterial species it is clear that genes from without play a prominent role in adaptive evolution as a source of genetic variation and particularly so for habitat-and-niche expansion (Shea et al.1996; Bergstrom et al. 2000; Levin and Bergstrom 2000; Ochman et al. 2000; Koonin et al. 2001; Cazalet et al. 2004; Thomas

1 Corresponding author: Department of Biology, Emory University, 1510 Clifton Rd., Atlanta, GA 30322. E-mail:

and Nielsen 2005; Coleman et al. 2006; Gal-Mor and Finlay 2006). Not so clear is how the capacity for HGT evolved and is maintained. Despite itsconsiderable value for the adaptation and long-term survival of bacterial populations, the ability to acquire genes from without, to ‘‘explore the fitness landscape’’ (Dubnau 1999), need not have been the selective force responsible for the evolution and maintenance of the machinery required for that capacity. In fact, for two of the three mechanisms of HGT, conjugation and transduction, it has been...
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