Escherichia coli Competence Gene Homologs Are Essential for Competitive Fitness and the Use of DNA as a Nutrient

Abstract

Natural genetic competence is the ability of cells to take up extracellular DNA and is an important mechanism for horizontal gene transfer. Another potential benefit of natural competence is that exogenous DNA can serve as a nutrient source for starving bacteria because the ability to "eat" DNA is necessary for competitive survival in environments containing limited nutrients. We show here that eight Escherichia coli genes, identified as homologs of com genes in Haemophilus influenzae and Neisseria gonorrhoeae, are necessary for the use of extracellular DNA as the sole source of carbon and energy. These genes also confer a competitive advantage to E. coli during long-term stationary-phase incubation. We also show that homologs of these genes are found throughout the proteobacteria, suggesting that the use of DNA as a nutrient may be a widespread phenomenon.

Characterization of bacterial DNA binding to human neutrophil surface

“…Extracellular DNA has been detected in virtually all environments inhabited by bacteria, 16,18,19,[50][51][52] and has also been implicated as a major structural component of bacterial biofilms. 24,25,53 Thus, it is possible that bacterial DNA recognition by a surface receptor has evolved as a signal to alert the immune system to the presence of bacterial invasion, mainly in infections which course with bacteria growing as biofilms.…”

“…In fact, previous studies have shown that Escherichia coli strains that consume DNA are more fit than those mutants unable to metabolize DNA. 19 On the other hand, several independent observations have adjudicated an important role for DNA in the formation and composition of biofilms, which are structured communities of cells enclosed in self-produced hydrated polymeric matrix adherent to an inert or living surface. 24,25 Thus, we hypothesized that extracellular DNA in bacterial microenvironments might be recognized by a neutrophil surface molecule able to trigger neutrophil activation.…”

“…4,15 Several studies have demonstrated the presence of extracellular DNA in bacterial cultures. [16][17][18][19] Naturally transformable bacterial species release chromosomal DNA into culture media. [19][20][21][22][23] Extracellular bacterial DNA has also been proposed to play a role as a nutrient during starvation.…”

“…[16][17][18][19] Naturally transformable bacterial species release chromosomal DNA into culture media. [19][20][21][22][23] Extracellular bacterial DNA has also been proposed to play a role as a nutrient during starvation. In fact, previous studies have shown that Escherichia coli strains that consume DNA are more fit than those mutants unable to metabolize DNA.…”

The Evolution of Natural Competence: Disentangling Costs and Benefits of Sex in Bacteria

“…It has been shown in several species that bacteria can indeed use DNA as a nutrient (Jorgensen et al 1994;Finkel and Kolter 2001;Palchevskiy and Finkel 2006;Pinchuk et al 2008). For example, Escherichia coli can grow on DNA as the sole source of carbon and energy (Finkel and Kolter 2001), and eight genes have been identified that are necessary for DNA uptake and that provide a competitive advantage during stationary phase (Palchevskiy and Finkel 2006). Pinchuk et al (2008) reported that Shawanella spp.…”