Interplay between three RND efflux pumps in doxycycline-selected strains of Burkholderia thailandensis

PLoS One. 2013 Dec 27;8(12):e84068. doi: 10.1371/journal.pone.0084068. eCollection 2013.

Abstract

Background: Efflux systems are involved in multidrug resistance in most Gram-negative non-fermentative bacteria. We have chosen Burkholderia thailandensis to dissect the development of multidrug resistance phenotypes under antibiotic pressure.

Methodology/principal findings: We used doxycycline selection to obtain several resistant B. thailandensis variants. The minimal inhibitory concentrations of a large panel of structurally unrelated antibiotics were determined ± the efflux pump inhibitor phenylalanine-arginine ß-naphthylamide (PAßN). Membrane proteins were identified by proteomic method and the expressions of major efflux pumps in the doxycycline selected variants were compared to those of the parental strains by a quantitative RT-PCR analysis. Doxycycline selected variants showed a multidrug resistance in two major levels corresponding to the overproduction of two efflux pumps depending on its concentration: AmrAB-OprA and BpeEF-OprC. The study of two mutants, each lacking one of these pumps, indicated that a third pump, BpeAB-OprB, could substitute for the defective pump. Surprisingly, we observed antagonistic effects between PAßN and aminoglycosides or some ß-lactams. PAßN induced the overexpression of AmrAB-OprA and BpeAB-OprB pump genes, generating this unexpected effect.

Conclusions/significance: These results may account for the weak activity of PAßN in some Gram-negative species. We clearly demonstrated two antagonistic effects of this molecule on bacterial cells: the blocking of antibiotic efflux and an increase in efflux pump gene expression. Thus, doxycycline is a very efficient RND efflux pump inducer and PAßN may promote the production of some efflux pumps. These results should be taken into account when considering antibiotic treatments and in future studies on efflux pump inhibitors.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Anti-Bacterial Agents / pharmacology*
  • Bacterial Outer Membrane Proteins / biosynthesis
  • Bacterial Proteins / antagonists & inhibitors
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism*
  • Burkholderia / drug effects*
  • Burkholderia / genetics
  • Burkholderia / metabolism*
  • Dipeptides / pharmacology
  • Doxycycline / pharmacology*
  • Drug Resistance, Multiple, Bacterial / drug effects
  • Drug Resistance, Multiple, Bacterial / genetics
  • Gene Expression Profiling
  • Gene Expression Regulation, Bacterial / drug effects
  • Microbial Sensitivity Tests
  • Mutation
  • Phenotype
  • Proteomics

Substances

  • Anti-Bacterial Agents
  • Bacterial Outer Membrane Proteins
  • Bacterial Proteins
  • Dipeptides
  • phenylalanine arginine beta-naphthylamide
  • Doxycycline

Grants and funding

This work was supported by the French Ministry of Defense (grant number PDH-2-NRBC-4-B-201) and by the Aix Marseille Université. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.