Long-Term Experimental Evolution in Escherichia coli. XII. DNA Topology as a Key Target of Selection

Abstract

The genetic bases of adaptation are being investigated in 12 populations of Escherichia coli, founded from a common ancestor and serially propagated for 20,000 generations, during which time they achieved substantial fitness gains. Each day, populations alternated between active growth and nutrient exhaustion. DNA supercoiling in bacteria is influenced by nutritional state, and DNA topology helps coordinate the overall pattern of gene expression in response to environmental changes. We therefore examined whether the genetic controls over supercoiling might have changed during the evolution experiment. Parallel changes in topology occurred in most populations, with the level of DNA supercoiling increasing, usually in the first 2000 generations. Two mutations in the topA and fis genes that control supercoiling were discovered in a population that served as the focus for further investigation. Moving the mutations, alone and in combination, into the ancestral background had an additive effect on supercoiling, and together they reproduced the net change in DNA topology observed in this population. Moreover, both mutations were beneficial in competition experiments. Clonal interference involving other beneficial DNA topology mutations was also detected. These findings define a new class of fitness-enhancing mutations and indicate that the control of DNA supercoiling can be a key target of selection in evolving bacterial populations.

Laboratory evolution of Geobacter sulfurreducens for enhanced growth on lactate via a single-base-pair substitution in a transcriptional regulator

“…This is because of the cells ability to more rapidly metabolize lactate, the sole electron donor and carbon source provided. Previous laboratory evolution studies have identified mutations in regulatory elements (Cooper et al, 2003;Crozat et al, 2005;Herring et al, 2006;Knight et al, 2006;D'Argenio et al, 2007;Giraud et al, 2008 et al, 2010), but these were all within global regulatory 'hubs' that subsequently affected gene expression on a large scale. In contrast, this study offers the finding of a mutated transcriptional regulator that appears to have a very narrow gene target, repression of two genes that encode for a single key enzyme.…”

Historical contingency and the evolution of a key innovation in an experimental population ofEscherichia coli

“…Ten populations evolved increased DNA supercoiling (27), and those populations examined to date show parallel changes in global gene-expression profiles (4,28,29). At least three genes have substitutions in all 12 populations (30,31), and several others have substitutions in many populations (27)(28)(29)(30), even though most loci harbor no substitutions in any of them (32). At the same time, there has also been some divergence between populations.…”

“…All evolved higher maximum growth rates on glucose, shorter lag phases upon transfer into fresh medium, reduced peak population densities, and larger average cell sizes relative to their ancestor (22)(23)(24)(25)(26). Ten populations evolved increased DNA supercoiling (27), and those populations examined to date show parallel changes in global gene-expression profiles (4,28,29). At least three genes have substitutions in all 12 populations (30,31), and several others have substitutions in many populations (27)(28)(29)(30), even though most loci harbor no substitutions in any of them (32).…”

“…In media containing other carbon sources, such as maltose or lactose, the variation in performance is much greater (34). And while the same genes often harbor substitutions, the precise location and details of the mutations almost always differ between the populations (27)(28)(29)(30)(31).…”

Complex Genetic Changes in Strains of Saccharomyces cerevisiae Derived by Selection in the Laboratory

“…The traits generated are generally genetic and quantitative, increase directionally throughout the period of selection, and involve both regulatory and structural adaptations (Castle 1951;Paquin and Adams 1983a,b;Cohan and Hoffmann 1986;Lenski and Travisano 1994;Ferea et al 1999;De Visser and Lenski 2002;Dunham et al 2002;Buckling et al 2003;Cooper et al 2003;Elena and Lenski 2003;Riehle et al 2003;Zeyl et al 2003Zeyl et al , 2005Laurie et al 2004;Crozat et al 2005;Grimberg and Zeyl 2005;Rifkin et al 2005;De Visser and Rozen 2006;Pelosi et al 2006). These studies, however, can be intensive in both labor and resources.…”