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Research Article

Sublethal Exposure to Commercial Formulations of the Herbicides Dicamba, 2,4-Dichlorophenoxyacetic Acid, and Glyphosate Cause Changes in Antibiotic Susceptibility in Escherichia coli and Salmonella enterica serovar Typhimurium

Brigitta Kurenbach, Delphine Marjoshi, Carlos F. Amábile-Cuevas, Gayle C. Ferguson, William Godsoe, Paddy Gibson, Jack A. Heinemann
Stephen J. Giovannoni, Editor
Brigitta Kurenbach
aSchool of Biological Sciences, University of Canterbury, Christchurch, New Zealand
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Delphine Marjoshi
aSchool of Biological Sciences, University of Canterbury, Christchurch, New Zealand
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Carlos F. Amábile-Cuevas
bFundación Lusara, Mexico City, Mexico
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Gayle C. Ferguson
cInstitute of Natural and Mathematical Sciences, Massey University, Palmerston North, New Zealand
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William Godsoe
dBio-Protection Centre, Lincoln University, Lincoln, New Zealand
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Paddy Gibson
aSchool of Biological Sciences, University of Canterbury, Christchurch, New Zealand
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Jack A. Heinemann
aSchool of Biological Sciences, University of Canterbury, Christchurch, New Zealand
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Stephen J. Giovannoni
Oregon State University
Roles: Editor
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DOI: 10.1128/mBio.00009-15
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ABSTRACT

Biocides, such as herbicides, are routinely tested for toxicity but not for sublethal effects on microbes. Many biocides are known to induce an adaptive multiple-antibiotic resistance phenotype. This can be due to either an increase in the expression of efflux pumps, a reduced synthesis of outer membrane porins, or both. Exposures of Escherichia coli and Salmonella enterica serovar Typhimurium to commercial formulations of three herbicides—dicamba (Kamba), 2,4-dichlorophenoxyacetic acid (2,4-D), and glyphosate (Roundup)—were found to induce a changed response to antibiotics. Killing curves in the presence and absence of sublethal herbicide concentrations showed that the directions and the magnitudes of responses varied by herbicide, antibiotic, and species. When induced, MICs of antibiotics of five different classes changed up to 6-fold. In some cases the MIC increased, and in others it decreased. Herbicide concentrations needed to invoke the maximal response were above current food maximum residue levels but within application levels for all herbicides. Compounds that could cause induction had additive effects in combination. The role of soxS, an inducer of the AcrAB efflux pump, was tested in β-galactosidase assays with soxS-lacZ fusion strains of E. coli. Dicamba was a moderate inducer of the sox regulon. Growth assays with Phe-Arg β-naphtylamide (PAβN), an efflux pump inhibitor, confirmed a significant role of efflux in the increased tolerance of E. coli to chloramphenicol in the presence of dicamba and to kanamycin in the presence of glyphosate. Pathways of exposure with relevance to the health of humans, domestic animals, and critical insects are discussed.

IMPORTANCE Increasingly common chemicals used in agriculture, domestic gardens, and public places can induce a multiple-antibiotic resistance phenotype in potential pathogens. The effect occurs upon simultaneous exposure to antibiotics and is faster than the lethal effect of antibiotics. The magnitude of the induced response may undermine antibiotic therapy and substantially increase the probability of spontaneous mutation to higher levels of resistance. The combination of high use of both herbicides and antibiotics in proximity to farm animals and important insects, such as honeybees, might also compromise their therapeutic effects and drive greater use of antibiotics. To address the crisis of antibiotic resistance requires broadening our view of environmental contributors to the evolution of resistance.

  • Copyright © 2015 Kurenbach et al.

This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-ShareAlike 3.0 Unported license, which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited.

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Sublethal Exposure to Commercial Formulations of the Herbicides Dicamba, 2,4-Dichlorophenoxyacetic Acid, and Glyphosate Cause Changes in Antibiotic Susceptibility in Escherichia coli and Salmonella enterica serovar Typhimurium
Brigitta Kurenbach, Delphine Marjoshi, Carlos F. Amábile-Cuevas, Gayle C. Ferguson, William Godsoe, Paddy Gibson, Jack A. Heinemann
mBio Mar 2015, 6 (2) e00009-15; DOI: 10.1128/mBio.00009-15

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Sublethal Exposure to Commercial Formulations of the Herbicides Dicamba, 2,4-Dichlorophenoxyacetic Acid, and Glyphosate Cause Changes in Antibiotic Susceptibility in Escherichia coli and Salmonella enterica serovar Typhimurium
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Sublethal Exposure to Commercial Formulations of the Herbicides Dicamba, 2,4-Dichlorophenoxyacetic Acid, and Glyphosate Cause Changes in Antibiotic Susceptibility in Escherichia coli and Salmonella enterica serovar Typhimurium
Brigitta Kurenbach, Delphine Marjoshi, Carlos F. Amábile-Cuevas, Gayle C. Ferguson, William Godsoe, Paddy Gibson, Jack A. Heinemann
mBio Mar 2015, 6 (2) e00009-15; DOI: 10.1128/mBio.00009-15
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