Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2009 Jun 2;106(22):9051-6.
doi: 10.1073/pnas.0902400106. Epub 2009 May 18.

A coordinated network of transporters with overlapping specificities provides a robust survival strategy

Affiliations

A coordinated network of transporters with overlapping specificities provides a robust survival strategy

Nir Tal et al. Proc Natl Acad Sci U S A. .

Abstract

Multidrug transporters provide a survival strategy for living organisms. As expected given their central role in survival, these transporters are ubiquitous, and in many genomes, several genes coding for putative transporters have been identified. However, in an organism such as Escherichia coli mutations in genes coding for transporters other than the major AcrAB-TolC multidrug efflux transporter have only a marginal effect on phenotype. Thus, whether the physiological role of the transporters identified is indeed drug export has been questioned. We show here that the minor effect of single mutations is due to the overlapping functionality of several transporters. This was revealed by generating multiple chromosomal deletion mutations in genes coding for transporters that share the same substrate and testing their effect on the resistance phenotype. In addition, complementation studies imply that AcrAB-TolC confers robust resistance provided that single-component transporters in the plasma membrane are functional. This finding supports the contention that hydrophobic drugs are removed in a 2-stage process: AcrAB-TolC removes substrates from the periplasmic space, while single-component transporters remove them from the cell. The overlapping specificities of the transporters ensure coverage of a wide range of xenobiotics and provide robustness in the response to environmental stress. This strategy also confers evolvability to the organism by reducing constraints on change and allowing the accumulation of nonlethal variation.

PubMed Disclaimer

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
The effect of MDT null mutations on the intrinsic resistance to acriflavine and ethidium. (A) Serial dilutions of overnight cultures were spotted (5 μL) on plates with or without toxic compounds (control). Growth was analyzed after overnight incubation at 37 °C. (B) Growth in liquid media was performed as described in Materials and Methods with increasing concentrations of ethidium. IC50 values were calculated from fits of the data obtained by Origin 8 software (the lowest R2 value is 0.93).
Fig. 2.
Fig. 2.
Plasmidic expression complements the defective phenotype only for exporters of the same type. (A and B) Cells harboring pT7–7, pEmrE, pMdfA, or pAcrA together with pAcrB (pAcrAB in short) were tested for resistance on solid media with acriflavine (A) or ethidium (B). Growth was analyzed after overnight incubation at 37 °C. (C) The indicated strains carrying plasmidic AcrAB were grown as illustrated in Fig. 1B, and the calculated IC50 values are shown.
Fig. 3.
Fig. 3.
Plasmidic EmrE and AcrAB are fully functional in all null strains. Cells harboring the indicated plasmids were spotted on plates with and without nalidixic acid (A) or with and without methyl viologen (B). Growth was analyzed after overnight incubation at 37 °C.
Fig. 4.
Fig. 4.
Plasmidic EmrE in ΔacrB cells confers full resistance to methyl viologen but only partial to ethidium and acriflavine. (A–C) WT and ΔacrB cells harboring pT7–7 or pEmrE were grown in liquid media with increasing concentrations of ethidium (A), acriflavine (B), or methyl viologen (C). IC50 values were calculated from fits of the data by Origin 8 software (the lowest R2 value is 0.95). (D) Ethidium efflux activity of EmrE. WT cells harboring pT7–7 (dotted line) or pEmrE (solid lines) and ΔacrB cells harboring pT7–7 (dashed-dotted line) or pEmrE (dashed lines) were assayed for ethidium efflux at the indicated concentrations. Glucose (0.36%) was added to initiate the active efflux of ethidium.
Fig. 5.
Fig. 5.
Model of functional interaction among AcrAB-TolC, EmrE and MdfA in E. coli. The single-component transporters, EmrE and MdfA, remove the drug (acriflavine or ethidium) from the cytoplasm and into the periplasm, where AcrAB-TolC captures it and extrudes it to the medium.

References

    1. Gottesman MM, Ling V. The molecular basis of multidrug resistance in cancer: The early years of P-glycoprotein research. FEBS Lett. 2006;580:998–1009. - PubMed
    1. Gottesman MM, Fojo T, Bates SE. Multidrug resistance in cancer: Role of ATP-dependent transporters. Nat Rev Cancer. 2002;2:48–58. - PubMed
    1. Nikaido H. Multiple antibiotic resistance and efflux. Curr Opin Microbiol. 1998;1:516–523. - PubMed
    1. Sulavik MC, et al. Antibiotic susceptibility profiles of Escherichia coli strains lacking multidrug efflux pump genes. Antimicrob Agents Chemother. 2001;45:1126–1136. - PMC - PubMed
    1. Nishino K, Yamaguchi A. Analysis of a complete library of putative drug transporter genes in Escherichia coli. J Bacteriol. 2001;183:5803–5812. - PMC - PubMed

Publication types

MeSH terms