Adaptive evolution of escherichia coli to ciprofloxacin in controlled stress environments: Contrasting patterns of resistance in spatially varying versus uniformly mixed concentration conditions

Jinzi Deng, Lang Zhou, Robert A. Sanford, Lauren A. Shechtman, Yiran Dong, Reinaldo E. Alcalde, Mayandi Sivaguru, Glenn A. Fried, Charles J. Werth, Bruce W. Fouke

Research output: Contribution to journalArticle

Abstract

A microfluidic gradient chamber (MGC) and a homogeneous batch culturing system were used to evaluate whether spatial concentration gradients of the antibiotic ciprofloxacin allow development of greater antibiotic resistance in Escherichia coli strain 307 (E. coli 307) compared to exclusively temporal concentration gradients, as indicated in an earlier study. A linear spatial gradient of ciprofloxacin and Luria-Bertani broth (LB) medium was established and maintained by diffusion over 5 days across a well array in the MGC, with relative concentrations along the gradient of 1.7-7.7× the original minimum inhibitory concentration (MICoriginal). The E. coli biomass increased in wells with lower ciprofloxacin concentrations, and only a low level of resistance to ciprofloxacin was detected in the recovered cells (?2× MICoriginal). Homogeneous batch culture experiments were performed with the same temporal exposure history to ciprofloxacin concentration, the same and higher initial cell densities, and the same and higher nutrient (i.e., LB) concentrations as in the MGC. In all batch experiments, E. coli 307 developed higher ciprofloxacin resistance after exposure, ranging from 4 to 24× MICoriginal in all replicates. Hence, these results suggest that the presence of spatial gradients appears to reduce the driving force for E. coli 307 adaptation to ciprofloxacin, which suggests that results from batch experiments may over predict the development of antibiotic resistance in natural environments.

Original languageEnglish (US)
Pages (from-to)7996-8005
Number of pages10
JournalEnvironmental Science and Technology
Volume53
Issue number14
DOIs
StatePublished - Jul 16 2019

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Ciprofloxacin
Escherichia coli
antibiotic resistance
Microfluidics
experiment
antibiotics
Anti-Bacterial Agents
well
nutrient
biomass
history
Experiments
Nutrients
Biomass
exposure

ASJC Scopus subject areas

  • Chemistry(all)
  • Environmental Chemistry

Cite this

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title = "Adaptive evolution of escherichia coli to ciprofloxacin in controlled stress environments: Contrasting patterns of resistance in spatially varying versus uniformly mixed concentration conditions",
abstract = "A microfluidic gradient chamber (MGC) and a homogeneous batch culturing system were used to evaluate whether spatial concentration gradients of the antibiotic ciprofloxacin allow development of greater antibiotic resistance in Escherichia coli strain 307 (E. coli 307) compared to exclusively temporal concentration gradients, as indicated in an earlier study. A linear spatial gradient of ciprofloxacin and Luria-Bertani broth (LB) medium was established and maintained by diffusion over 5 days across a well array in the MGC, with relative concentrations along the gradient of 1.7-7.7× the original minimum inhibitory concentration (MICoriginal). The E. coli biomass increased in wells with lower ciprofloxacin concentrations, and only a low level of resistance to ciprofloxacin was detected in the recovered cells (?2× MICoriginal). Homogeneous batch culture experiments were performed with the same temporal exposure history to ciprofloxacin concentration, the same and higher initial cell densities, and the same and higher nutrient (i.e., LB) concentrations as in the MGC. In all batch experiments, E. coli 307 developed higher ciprofloxacin resistance after exposure, ranging from 4 to 24× MICoriginal in all replicates. Hence, these results suggest that the presence of spatial gradients appears to reduce the driving force for E. coli 307 adaptation to ciprofloxacin, which suggests that results from batch experiments may over predict the development of antibiotic resistance in natural environments.",
author = "Jinzi Deng and Lang Zhou and Sanford, {Robert A.} and Shechtman, {Lauren A.} and Yiran Dong and Alcalde, {Reinaldo E.} and Mayandi Sivaguru and Fried, {Glenn A.} and Werth, {Charles J.} and Fouke, {Bruce W.}",
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T1 - Adaptive evolution of escherichia coli to ciprofloxacin in controlled stress environments

T2 - Contrasting patterns of resistance in spatially varying versus uniformly mixed concentration conditions

AU - Deng, Jinzi

AU - Zhou, Lang

AU - Sanford, Robert A.

AU - Shechtman, Lauren A.

AU - Dong, Yiran

AU - Alcalde, Reinaldo E.

AU - Sivaguru, Mayandi

AU - Fried, Glenn A.

AU - Werth, Charles J.

AU - Fouke, Bruce W.

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Y1 - 2019/7/16

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AB - A microfluidic gradient chamber (MGC) and a homogeneous batch culturing system were used to evaluate whether spatial concentration gradients of the antibiotic ciprofloxacin allow development of greater antibiotic resistance in Escherichia coli strain 307 (E. coli 307) compared to exclusively temporal concentration gradients, as indicated in an earlier study. A linear spatial gradient of ciprofloxacin and Luria-Bertani broth (LB) medium was established and maintained by diffusion over 5 days across a well array in the MGC, with relative concentrations along the gradient of 1.7-7.7× the original minimum inhibitory concentration (MICoriginal). The E. coli biomass increased in wells with lower ciprofloxacin concentrations, and only a low level of resistance to ciprofloxacin was detected in the recovered cells (?2× MICoriginal). Homogeneous batch culture experiments were performed with the same temporal exposure history to ciprofloxacin concentration, the same and higher initial cell densities, and the same and higher nutrient (i.e., LB) concentrations as in the MGC. In all batch experiments, E. coli 307 developed higher ciprofloxacin resistance after exposure, ranging from 4 to 24× MICoriginal in all replicates. Hence, these results suggest that the presence of spatial gradients appears to reduce the driving force for E. coli 307 adaptation to ciprofloxacin, which suggests that results from batch experiments may over predict the development of antibiotic resistance in natural environments.

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