Antidepressant fluoxetine induces multiple antibiotics resistance in Escherichia coli via ROS-mediated mutagenesis
Antibiotic resistance poses a great threat to global public health. Overuse of antibiotics is generally considered as the major factor contributing to it. However, little is known about whether non-antibiotic drugs could play potential roles in the emergence of antibiotic resistance. We aimed to inv...
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Published in | Environment international Vol. 120; pp. 421 - 430 |
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Main Authors | , , , , , , , |
Format | Journal Article |
Language | English |
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Elsevier Ltd
01.11.2018
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Abstract | Antibiotic resistance poses a great threat to global public health. Overuse of antibiotics is generally considered as the major factor contributing to it. However, little is known about whether non-antibiotic drugs could play potential roles in the emergence of antibiotic resistance.
We aimed to investigate whether antidepressant fluoxetine induces multiple antibiotic resistances and reveal underlying mechanisms.
Escherichia coli K12 was exposed to different concentrations of fluoxetine (0, 0.5, 5, 50 and 100 mg/L) and the resistant strains were isolated by plating on antibiotic containing plates. Resistant strains were randomly selected to determine the increase of minimum inhibition concentration (MIC) of multiple antibiotics. Genome-wide DNA sequencing was performed on cells cultured in lysogeny broth (LB) without any fluoxetine or antibiotics exposure. RNA sequencing and proteomic profiling of isolated mutants grown in LB with 100 mg/L fluoxetine were analyzed to reveal the underlying mechanisms.
Exposure of Escherichia coli to fluoxetine at 5–100 mg/L after repeated subculture in LB for 30 days promoted its mutation frequency resulting in increased resistance against the antibiotics chloramphenicol, amoxicillin and tetracycline. This increase was up to 5.0 × 107 fold in a dose-time pattern. Isolated mutants with resistance to one of these antibiotics also exhibited multiple resistances against fluoroquinolone, aminoglycoside, β-lactams, tetracycline and chloramphenicol. According to global transcriptional and proteomic analyses, the AcrAB-TolC pump together with the YadG/YadH transporter, a Tsx channel and the MdtEF-TolC pump have been triggered to export the antibiotics to the exterior of the cell. Whole-genome DNA analysis of the mutants further revealed that ROS-mediated mutagenesis (e.g., deletion, insertion, and substitution) of DNA-binding transcriptional regulators (e.g., marR, rob, sdiA, cytR and crp) to up-regulate the expression of efflux pumps, may further enhance the antibiotic efflux.
Our findings for the first time demonstrated that the exposure to antidepressant fluoxetine induces multiple antibiotic resistance in E. coli via the ROS-mediated mutagenesis.
•The exposure to antidepressant fluoxetine induces multiple antibiotic resistance in E. coli K12.•Multiple efflux pumps have been triggered by fluoxetine to export antibiotics.•ROS-mediated mutagenesis induced by fluoxetine enhances antibiotic efflux.•It is required to evaluate the potential impact of such chemicals on AMR. |
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AbstractList | Antibiotic resistance poses a great threat to global public health. Overuse of antibiotics is generally considered as the major factor contributing to it. However, little is known about whether non-antibiotic drugs could play potential roles in the emergence of antibiotic resistance.
We aimed to investigate whether antidepressant fluoxetine induces multiple antibiotic resistances and reveal underlying mechanisms.
Escherichia coli K12 was exposed to different concentrations of fluoxetine (0, 0.5, 5, 50 and 100 mg/L) and the resistant strains were isolated by plating on antibiotic containing plates. Resistant strains were randomly selected to determine the increase of minimum inhibition concentration (MIC) of multiple antibiotics. Genome-wide DNA sequencing was performed on cells cultured in lysogeny broth (LB) without any fluoxetine or antibiotics exposure. RNA sequencing and proteomic profiling of isolated mutants grown in LB with 100 mg/L fluoxetine were analyzed to reveal the underlying mechanisms.
Exposure of Escherichia coli to fluoxetine at 5–100 mg/L after repeated subculture in LB for 30 days promoted its mutation frequency resulting in increased resistance against the antibiotics chloramphenicol, amoxicillin and tetracycline. This increase was up to 5.0 × 107 fold in a dose-time pattern. Isolated mutants with resistance to one of these antibiotics also exhibited multiple resistances against fluoroquinolone, aminoglycoside, β-lactams, tetracycline and chloramphenicol. According to global transcriptional and proteomic analyses, the AcrAB-TolC pump together with the YadG/YadH transporter, a Tsx channel and the MdtEF-TolC pump have been triggered to export the antibiotics to the exterior of the cell. Whole-genome DNA analysis of the mutants further revealed that ROS-mediated mutagenesis (e.g., deletion, insertion, and substitution) of DNA-binding transcriptional regulators (e.g., marR, rob, sdiA, cytR and crp) to up-regulate the expression of efflux pumps, may further enhance the antibiotic efflux.
Our findings for the first time demonstrated that the exposure to antidepressant fluoxetine induces multiple antibiotic resistance in E. coli via the ROS-mediated mutagenesis.
•The exposure to antidepressant fluoxetine induces multiple antibiotic resistance in E. coli K12.•Multiple efflux pumps have been triggered by fluoxetine to export antibiotics.•ROS-mediated mutagenesis induced by fluoxetine enhances antibiotic efflux.•It is required to evaluate the potential impact of such chemicals on AMR. Antibiotic resistance poses a great threat to global public health. Overuse of antibiotics is generally considered as the major factor contributing to it. However, little is known about whether non-antibiotic drugs could play potential roles in the emergence of antibiotic resistance. We aimed to investigate whether antidepressant fluoxetine induces multiple antibiotic resistances and reveal underlying mechanisms. Escherichia coli K12 was exposed to different concentrations of fluoxetine (0, 0.5, 5, 50 and 100 mg/L) and the resistant strains were isolated by plating on antibiotic containing plates. Resistant strains were randomly selected to determine the increase of minimum inhibition concentration (MIC) of multiple antibiotics. Genome-wide DNA sequencing was performed on cells cultured in lysogeny broth (LB) without any fluoxetine or antibiotics exposure. RNA sequencing and proteomic profiling of isolated mutants grown in LB with 100 mg/L fluoxetine were analyzed to reveal the underlying mechanisms. Exposure of Escherichia coli to fluoxetine at 5-100 mg/L after repeated subculture in LB for 30 days promoted its mutation frequency resulting in increased resistance against the antibiotics chloramphenicol, amoxicillin and tetracycline. This increase was up to 5.0 × 10 fold in a dose-time pattern. Isolated mutants with resistance to one of these antibiotics also exhibited multiple resistances against fluoroquinolone, aminoglycoside, β-lactams, tetracycline and chloramphenicol. According to global transcriptional and proteomic analyses, the AcrAB-TolC pump together with the YadG/YadH transporter, a Tsx channel and the MdtEF-TolC pump have been triggered to export the antibiotics to the exterior of the cell. Whole-genome DNA analysis of the mutants further revealed that ROS-mediated mutagenesis (e.g., deletion, insertion, and substitution) of DNA-binding transcriptional regulators (e.g., marR, rob, sdiA, cytR and crp) to up-regulate the expression of efflux pumps, may further enhance the antibiotic efflux. Our findings for the first time demonstrated that the exposure to antidepressant fluoxetine induces multiple antibiotic resistance in E. coli via the ROS-mediated mutagenesis. |
Author | Mao, Likai Chen, Zhaoyu Jin, Min Lu, Ji Li, Junwen Guo, Jianhua Nguyen, Son Hoang Yuan, Zhiguo |
Author_xml | – sequence: 1 givenname: Min orcidid: 0000-0002-6012-8466 surname: Jin fullname: Jin, Min organization: Advanced Water Management Centre (AWMC), University of Queensland, St Lucia, Brisbane, QLD 4072, Australia – sequence: 2 givenname: Ji surname: Lu fullname: Lu, Ji organization: Advanced Water Management Centre (AWMC), University of Queensland, St Lucia, Brisbane, QLD 4072, Australia – sequence: 3 givenname: Zhaoyu surname: Chen fullname: Chen, Zhaoyu organization: Advanced Water Management Centre (AWMC), University of Queensland, St Lucia, Brisbane, QLD 4072, Australia – sequence: 4 givenname: Son Hoang surname: Nguyen fullname: Nguyen, Son Hoang organization: Institute for Molecular Bioscience, University of Queensland, St Lucia, Brisbane, Queensland 4072, Australia – sequence: 5 givenname: Likai surname: Mao fullname: Mao, Likai organization: Advanced Water Management Centre (AWMC), University of Queensland, St Lucia, Brisbane, QLD 4072, Australia – sequence: 6 givenname: Junwen surname: Li fullname: Li, Junwen organization: Department of Environment and Health, Tianjin Institute of Environmental & Operational Medicine, Key Laboratory of Risk Assessment and Control for Environment & Food Safety, Tianjin 300050, China – sequence: 7 givenname: Zhiguo surname: Yuan fullname: Yuan, Zhiguo organization: Advanced Water Management Centre (AWMC), University of Queensland, St Lucia, Brisbane, QLD 4072, Australia – sequence: 8 givenname: Jianhua orcidid: 0000-0002-4732-9175 surname: Guo fullname: Guo, Jianhua email: j.guo@awmc.uq.edu.au organization: Advanced Water Management Centre (AWMC), University of Queensland, St Lucia, Brisbane, QLD 4072, Australia |
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Keywords | ROS-mediated mutagenesis Multiple antibiotic resistance Antimicrobial resistance Antidepressant fluoxetine Escherichia coli AcrAB-TolC |
Language | English |
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Snippet | Antibiotic resistance poses a great threat to global public health. Overuse of antibiotics is generally considered as the major factor contributing to it.... |
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SubjectTerms | AcrAB-TolC Anti-Bacterial Agents - pharmacology Antidepressant fluoxetine Antidepressive Agents - pharmacology Antimicrobial resistance Drug Resistance, Multiple, Bacterial - drug effects Escherichia coli Escherichia coli - drug effects Escherichia coli - physiology Escherichia coli Proteins - metabolism Fluoxetine - pharmacology Membrane Transport Proteins - metabolism Microbial Sensitivity Tests Multiple antibiotic resistance Mutagenesis Proteomics Reactive Oxygen Species - metabolism ROS-mediated mutagenesis |
Title | Antidepressant fluoxetine induces multiple antibiotics resistance in Escherichia coli via ROS-mediated mutagenesis |
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