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Water Disinfection Byproducts Increase Natural Transformation Rates of Environmental DNA in Acinetobacter baylyi ADP1

Mantilla-Calderon, David, Plewa, Michael J., Michoud, Grégoire, Fodelianakis, Stelios, Daffonchio, Daniele, Hong, Pei-Ying
Environmental science & technology 2019 v.53 no.11 pp. 6520-6528
Acinetobacter, DNA, DNA damage, DNA repair, antibiotic resistance, byproducts, cell membranes, disinfection, drinking water, gene expression regulation, genes, horizontal gene transfer, metagenomics, models, mutagens, oxidative stress, transcription (genetics), virulence
The process of natural transformation allows for the stable uptake, integration, and functional expression of extracellular DNA. This mechanism of horizontal gene transfer has been widely linked to the acquisition of antibiotic resistance and virulence factors. Here, we demonstrate that bromoacetic acid (BAA)—a regulated drinking water disinfection byproduct (DBP)—can stimulate natural transformation rates in the model organism Acinetobacter baylyi ADP1. We demonstrate that transformation stimulation in response to BAA is concentration-dependent and is linked to the ability of this compound to generate DNA damage via oxidative stress. In presence of BAA, transcription of recA was upregulated 20–40% compared to the nontreated controls, indicating that this component of the DNA damage response could be associated with the increase in transformation. Other genes associated with DNA translocation across the cytoplasmic membrane (i.e., pilX, comA) did not exhibit increased transcription in the presence of BAA, indicating that the enhancement of transformation is not associated with increased translocation rates of environmental DNA. Overall, these results lead us to speculate that elevated recA transcription levels could lead to increased integration rates of foreign DNA within the recipient cell during DNA repair. Lastly, we show that an artificial DBP cocktail simulating the environmental concentrations of five water DBP classes stimulates natural transformation by almost 2-fold. The results of this study suggest that mutagens like DBPs may play an important role in enhancing the fixation rates of extracellular DNA in the environmental metagenome.