Hydrogen peroxide-dependent DNA release and transfer of antibiotic resistance genes in Streptococcus gordonii

Abstract

Certain oral streptococci produce H 2O 2 under aerobic growth conditions to inhibit competing species like Streptococcus mutans. Additionally, H 2O 2 production causes the release of extracellular DNA (eDNA). eDNA can participate in several important functions: biofilm formation and cell-cell aggregation are supported by eDNA, while eDNA can serve as a nutrient and as an antimicrobial agent by chelating essential cations. eDNA contains DNA fragments of a size that has the potential to transfer genomic information. By using Streptococcus gordonii as a model organism for streptococcal H 2O 2 production, H 2O 2-dependent eDNA release was further investigated. Under defined growth conditions, the eDNA release process was shown to be entirely dependent on H 2O 2. Chromosomal DNA damage seems to be the intrinsic signal for the release, although only actively growing cells were proficient eDNA donors. Interestingly, the process of eDNA production was found to be coupled with the induction of the S. gordonii natural competence system. Consequently, the production of H 2O 2 triggered the transfer of antibiotic resistance genes. These results suggest that H 2O 2 is potentially much more than a simple toxic metabolic by-product; rather, its production could serve as an important environmental signal that facilitates species evolution by transfer of genetic information and an increase in the mutation rate. © 2011, American Society for Microbiology.