Costs and benefits of natural transformation in Acinetobacter baylyi

• Published in: BMC microbiology Vol. 17; no. 1; p. 34
• Main Authors: Hülter, Nils, Sørum, Vidar, Borch-Pedersen, Kristina, Liljegren, Mikkel M, Utnes, Ane L G, Primicerio, Raul, Harms, Klaus, Johnsen, Pål J
• Format: Journal Article
• Language: English
• Published: England BioMed Central Ltd 15.02.2017; BioMed Central; BMJ Publishing Group
• Subjects: Acinetobacter; Acinetobacter - enzymology; Acinetobacter - genetics; Acinetobacter - metabolism; Acinetobacter - radiation effects; Analysis; Bacterial Proteins - genetics; Bacterial Proteins - metabolism; Bacterial Proteins - radiation effects; Basale biofag: 470; Basic biosciences: 470; Biological Evolution; Cost-Benefit Analysis; DNA Damage - radiation effects; DNA repair; DNA Repair - physiology; DNA Repair - radiation effects; DNA, Bacterial - genetics; DNA, Bacterial - radiation effects; Evolution & development; Exodeoxyribonuclease V - metabolism; Exodeoxyribonuclease V - radiation effects; Gene Deletion; Gene Transfer, Horizontal - genetics; Gene Transfer, Horizontal - radiation effects; General microbiology: 472; Generell mikrobiologi: 472; Genes; Genes, Bacterial - genetics; Genes, Bacterial - radiation effects; Genomes; Genomics; Hypotheses; Matematikk og Naturvitenskap: 400; Mathematics and natural science: 400; Membrane Proteins - genetics; Membrane Proteins - radiation effects; Mutation; Mutation - genetics; Mutation - radiation effects; Phenotype; Physiological aspects; Plasmids; Prokaryotes; Recombination, Genetic - radiation effects; Streptococcus infections; Stress, Physiological; Survival; Transformation, Bacterial - genetics; Transformation, Bacterial - radiation effects; Ultraviolet Rays - adverse effects; VDP; Germany; Competence; Bacterial evolution; DprA; DNA repair; Natural transformation; Horizontal gene transfer
• ISSN: 1471-2180; 1471-2180
• DOI: 10.1186/s12866-017-0953-2

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. 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. 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.