ABSTRACT
BACKGROUND: Natural transformation enables acquisition of adaptive traits and drives genome evolution in prokaryotes. Yet, the selective forces responsible for the evolution and maintenance of natural transformation remain elusive since taken-up DNA has also been hypothesized to provide benefits such as nutrients or templates for DNA repair to individual cells. RESULTS: We investigated the immediate effects of DNA uptake and recombination on the naturally competent bacterium Acinetobacter baylyi in both benign and genotoxic conditions. In head-to-head competition experiments between DNA uptake-proficient and -deficient strains, we observed a fitness benefit of DNA uptake independent of UV stress. This benefit was found with both homologous and heterologous DNA and was independent of recombination. Recombination with taken-up DNA reduced survival of transformed cells with increasing levels of UV-stress through interference with nucleotide excision repair, suggesting that DNA strand breaks occur during recombination attempts with taken-up DNA. Consistent with this, we show that absence of RecBCD and RecFOR recombinational DNA repair pathways strongly decrease natural transformation. CONCLUSIONS: Our data show a physiological benefit of DNA uptake unrelated to recombination. In contrast, recombination during transformation is a strand break inducing process that represents a previously unrecognized cost of natural transformation.
Subject(s)
Acinetobacter/genetics , Acinetobacter/radiation effects , Biological Evolution , Cost-Benefit Analysis , Transformation, Bacterial/genetics , Transformation, Bacterial/radiation effects , Acinetobacter/enzymology , Acinetobacter/metabolism , Bacterial Proteins/genetics , Bacterial Proteins/metabolism , Bacterial Proteins/radiation effects , DNA Damage/radiation effects , DNA Repair/physiology , DNA Repair/radiation effects , DNA, Bacterial/genetics , DNA, Bacterial/radiation effects , Exodeoxyribonuclease V/metabolism , Exodeoxyribonuclease V/radiation effects , Gene Deletion , Gene Transfer, Horizontal/genetics , Gene Transfer, Horizontal/radiation effects , Genes, Bacterial/genetics , Genes, Bacterial/radiation effects , Membrane Proteins/genetics , Membrane Proteins/radiation effects , Mutation/genetics , Mutation/radiation effects , Phenotype , Recombination, Genetic/radiation effects , Stress, Physiological , Survival , Ultraviolet Rays/adverse effectsABSTRACT
Natural transformation in bacteria facilitates the uptake and genomic integration of exogenous DNA. This allows horizontal exchange of adaptive traits not easily achieved by point mutations, and has a major role in the acquisition of adaptive traits exemplified by antibiotic resistance determinants and vaccination escape. Mechanisms of DNA uptake and genomic integration are well described for several naturally transformable bacterial species; however, the selective forces responsible for its evolution and maintenance are still controversial. In this study we evolved transformation-proficient and -deficient Acinetobacter baylyi for 175 days in serial transfer cultures where stress was included. We found that natural transformation-proficient populations adapted better to active growth and early stationary phase. This advantage was offset by the reduced performance in the late stationary/death phase. We demonstrate fitness trade-offs between adaptation to active growth and survival in stationary/death phase caused by antagonistic pleiotropy. The presented data suggest that the widely held assumption that recombination speeds up adaptation by rapid accumulation of multiple adaptive mutations in the same genetic background is not sufficient to fully account for the maintenance of natural transformation in bacteria.
