The Role of Reactive Oxygen Species in Antibiotic-Induced Cell Death in Burkholderia cepacia Complex Bacteria

PLoS One. 2016 Jul 20;11(7):e0159837. doi: 10.1371/journal.pone.0159837. eCollection 2016.

Abstract

It was recently proposed that bactericidal antibiotics, besides through specific drug-target interactions, kill bacteria by a common mechanism involving the production of reactive oxygen species (ROS). However, this mechanism involving the production of hydroxyl radicals has become the subject of a lot of debate. Since the contribution of ROS to antibiotic mediated killing most likely depends on the conditions, differences in experimental procedures are expected to be at the basis of the conflicting results. In the present study different methods (ROS specific stainings, gene-expression analyses, electron paramagnetic resonance, genetic and phenotypic experiments, detection of protein carbonylation and DNA oxidation) to measure the production of ROS upon antibiotic treatment in Burkholderia cepacia complex (Bcc) bacteria were compared. Different classes of antibiotics (tobramycin, ciprofloxacin, meropenem) were included, and both planktonic and biofilm cultures were studied. Our results indicate that some of the methods investigated were not sensitive enough to measure antibiotic induced production of ROS, including the spectrophotometric detection of protein carbonylation. Secondly, other methods were found to be useful only in specific conditions. For example, an increase in the expression of OxyR was measured in Burkholderia cenocepacia K56-2 after treatment with ciprofloxacin or meropenem (both in biofilms and planktonic cultures) but not after treatment with tobramycin. In addition results vary with the experimental conditions and the species tested. Nevertheless our data strongly suggest that ROS contribute to antibiotic mediated killing in Bcc species and that enhancing ROS production or interfering with the protection against ROS may form a novel strategy to improve antibiotic treatment.

MeSH terms

  • Anti-Bacterial Agents / pharmacokinetics*
  • Anti-Bacterial Agents / pharmacology
  • Biofilms / drug effects
  • Biofilms / growth & development
  • Burkholderia Infections / drug therapy
  • Burkholderia Infections / metabolism*
  • Burkholderia Infections / microbiology
  • Burkholderia cepacia complex / drug effects
  • Burkholderia cepacia complex / growth & development
  • Burkholderia cepacia complex / metabolism*
  • Cell Death / drug effects
  • Ciprofloxacin / pharmacology
  • Gene Expression Regulation, Bacterial / drug effects
  • Meropenem
  • Microbial Sensitivity Tests
  • Reactive Oxygen Species / metabolism*
  • Repressor Proteins / biosynthesis
  • Thienamycins / pharmacology
  • Tobramycin / pharmacology

Substances

  • Anti-Bacterial Agents
  • Reactive Oxygen Species
  • Repressor Proteins
  • Thienamycins
  • Ciprofloxacin
  • Meropenem
  • Tobramycin

Grants and funding

This work was financially supported by FWO-Vlaanderen. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.