Sublethal Exposure to Commercial Formulations of the Herbicides Dicamba, 2,4-Dichlorophenoxyacetic Acid, and Glyphosate Cause Changes in Antibiotic Susceptibility in <named-content content-type="genus-species">Escherichia coli</named-content> and <named-content content-type="genus-species">Salmonella enterica</named-content> serovar Typhimurium

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...

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Autores principales:	Brigitta Kurenbach, Delphine Marjoshi, Carlos F. Amábile-Cuevas, Gayle C. Ferguson, William Godsoe, Paddy Gibson, Jack A. Heinemann
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Lenguaje:	EN
Publicado:	American Society for Microbiology 2015
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/07fac9d179354426a85c8b4f8f6dec04
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spelling	oai:doaj.org-article:07fac9d179354426a85c8b4f8f6dec042021-11-15T15:41:33ZSublethal Exposure to Commercial Formulations of the Herbicides Dicamba, 2,4-Dichlorophenoxyacetic Acid, and Glyphosate Cause Changes in Antibiotic Susceptibility in <named-content content-type="genus-species">Escherichia coli</named-content> and <named-content content-type="genus-species">Salmonella enterica</named-content> serovar Typhimurium10.1128/mBio.00009-152150-7511https://doaj.org/article/07fac9d179354426a85c8b4f8f6dec042015-05-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00009-15https://doaj.org/toc/2150-7511ABSTRACT 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.Brigitta KurenbachDelphine MarjoshiCarlos F. Amábile-CuevasGayle C. FergusonWilliam GodsoePaddy GibsonJack A. HeinemannAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 6, Iss 2 (2015)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Brigitta Kurenbach Delphine Marjoshi Carlos F. Amábile-Cuevas Gayle C. Ferguson William Godsoe Paddy Gibson Jack A. Heinemann Sublethal Exposure to Commercial Formulations of the Herbicides Dicamba, 2,4-Dichlorophenoxyacetic Acid, and Glyphosate Cause Changes in Antibiotic Susceptibility in <named-content content-type="genus-species">Escherichia coli</named-content> and <named-content content-type="genus-species">Salmonella enterica</named-content> serovar Typhimurium
description	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.
format	article
author	Brigitta Kurenbach Delphine Marjoshi Carlos F. Amábile-Cuevas Gayle C. Ferguson William Godsoe Paddy Gibson Jack A. Heinemann
author_facet	Brigitta Kurenbach Delphine Marjoshi Carlos F. Amábile-Cuevas Gayle C. Ferguson William Godsoe Paddy Gibson Jack A. Heinemann
author_sort	Brigitta Kurenbach
title	Sublethal Exposure to Commercial Formulations of the Herbicides Dicamba, 2,4-Dichlorophenoxyacetic Acid, and Glyphosate Cause Changes in Antibiotic Susceptibility in <named-content content-type="genus-species">Escherichia coli</named-content> and <named-content content-type="genus-species">Salmonella enterica</named-content> serovar Typhimurium
title_short	Sublethal Exposure to Commercial Formulations of the Herbicides Dicamba, 2,4-Dichlorophenoxyacetic Acid, and Glyphosate Cause Changes in Antibiotic Susceptibility in <named-content content-type="genus-species">Escherichia coli</named-content> and <named-content content-type="genus-species">Salmonella enterica</named-content> serovar Typhimurium
title_full	Sublethal Exposure to Commercial Formulations of the Herbicides Dicamba, 2,4-Dichlorophenoxyacetic Acid, and Glyphosate Cause Changes in Antibiotic Susceptibility in <named-content content-type="genus-species">Escherichia coli</named-content> and <named-content content-type="genus-species">Salmonella enterica</named-content> serovar Typhimurium
title_fullStr	Sublethal Exposure to Commercial Formulations of the Herbicides Dicamba, 2,4-Dichlorophenoxyacetic Acid, and Glyphosate Cause Changes in Antibiotic Susceptibility in <named-content content-type="genus-species">Escherichia coli</named-content> and <named-content content-type="genus-species">Salmonella enterica</named-content> serovar Typhimurium
title_full_unstemmed	Sublethal Exposure to Commercial Formulations of the Herbicides Dicamba, 2,4-Dichlorophenoxyacetic Acid, and Glyphosate Cause Changes in Antibiotic Susceptibility in <named-content content-type="genus-species">Escherichia coli</named-content> and <named-content content-type="genus-species">Salmonella enterica</named-content> serovar Typhimurium
title_sort	sublethal exposure to commercial formulations of the herbicides dicamba, 2,4-dichlorophenoxyacetic acid, and glyphosate cause changes in antibiotic susceptibility in <named-content content-type="genus-species">escherichia coli</named-content> and <named-content content-type="genus-species">salmonella enterica</named-content> serovar typhimurium
publisher	American Society for Microbiology
publishDate	2015
url	https://doaj.org/article/07fac9d179354426a85c8b4f8f6dec04
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