Escherichia coli survival in response to ciprofloxacin antibiotic stress correlates with increased nucleoid length and effective misfolded protein management
The evolution of antibiotic resistance is a fundamental problem in disease management but is rarely quantified on a single-cell level owing to challenges associated with capturing the spatial and temporal variation across a population. To evaluate cell biological phenotypic responses, we tracked the...
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Format: | Article |
Language: | English |
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The Royal Society
2023-08-01
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Series: | Royal Society Open Science |
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Online Access: | https://royalsocietypublishing.org/doi/10.1098/rsos.230338 |
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author | George Butler Julia Bos Robert H. Austin Sarah R. Amend Kenneth J. Pienta |
author_facet | George Butler Julia Bos Robert H. Austin Sarah R. Amend Kenneth J. Pienta |
author_sort | George Butler |
collection | DOAJ |
description | The evolution of antibiotic resistance is a fundamental problem in disease management but is rarely quantified on a single-cell level owing to challenges associated with capturing the spatial and temporal variation across a population. To evaluate cell biological phenotypic responses, we tracked the single-cell dynamics of filamentous bacteria through time in response to ciprofloxacin antibiotic stress. We measured the degree of phenotypic variation in nucleoid length and the accumulation of protein damage under ciprofloxacin antibiotic and quantified the impact on bacterial survival. Increased survival was correlated with increased nucleoid length and the variation in this response was inversely correlated with antibiotic concentration. Survival time was also increased through clearance of misfolded proteins, an unexpected mechanism of stress relief deployed by the filamentous bacteria. Our results reveal a diverse range of survival tactics employed by bacteria in response to ciprofloxacin and suggest potential evolutionary routes to resistance. |
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format | Article |
id | doaj.art-911f187d3923462ea7670716e393fb3c |
institution | Directory Open Access Journal |
issn | 2054-5703 |
language | English |
last_indexed | 2024-03-12T16:14:37Z |
publishDate | 2023-08-01 |
publisher | The Royal Society |
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series | Royal Society Open Science |
spelling | doaj.art-911f187d3923462ea7670716e393fb3c2023-08-09T07:05:25ZengThe Royal SocietyRoyal Society Open Science2054-57032023-08-0110810.1098/rsos.230338Escherichia coli survival in response to ciprofloxacin antibiotic stress correlates with increased nucleoid length and effective misfolded protein managementGeorge Butler0Julia Bos1Robert H. Austin2Sarah R. Amend3Kenneth J. Pienta4Cancer Ecology Center, The Brady Urological Institute, Johns Hopkins School of Medicine, Baltimore, MD, USAInstitut Pasteur, Université de Paris Cité, CNRS UMR 3525, Unité Plasticité du Génome Bactérien, Paris, FranceDepartment of Physics, Princeton University, Princeton, NJ, USACancer Ecology Center, The Brady Urological Institute, Johns Hopkins School of Medicine, Baltimore, MD, USACancer Ecology Center, The Brady Urological Institute, Johns Hopkins School of Medicine, Baltimore, MD, USAThe evolution of antibiotic resistance is a fundamental problem in disease management but is rarely quantified on a single-cell level owing to challenges associated with capturing the spatial and temporal variation across a population. To evaluate cell biological phenotypic responses, we tracked the single-cell dynamics of filamentous bacteria through time in response to ciprofloxacin antibiotic stress. We measured the degree of phenotypic variation in nucleoid length and the accumulation of protein damage under ciprofloxacin antibiotic and quantified the impact on bacterial survival. Increased survival was correlated with increased nucleoid length and the variation in this response was inversely correlated with antibiotic concentration. Survival time was also increased through clearance of misfolded proteins, an unexpected mechanism of stress relief deployed by the filamentous bacteria. Our results reveal a diverse range of survival tactics employed by bacteria in response to ciprofloxacin and suggest potential evolutionary routes to resistance.https://royalsocietypublishing.org/doi/10.1098/rsos.230338filamentationevolutionresistanceantibiotics |
spellingShingle | George Butler Julia Bos Robert H. Austin Sarah R. Amend Kenneth J. Pienta Escherichia coli survival in response to ciprofloxacin antibiotic stress correlates with increased nucleoid length and effective misfolded protein management Royal Society Open Science filamentation evolution resistance antibiotics |
title | Escherichia coli survival in response to ciprofloxacin antibiotic stress correlates with increased nucleoid length and effective misfolded protein management |
title_full | Escherichia coli survival in response to ciprofloxacin antibiotic stress correlates with increased nucleoid length and effective misfolded protein management |
title_fullStr | Escherichia coli survival in response to ciprofloxacin antibiotic stress correlates with increased nucleoid length and effective misfolded protein management |
title_full_unstemmed | Escherichia coli survival in response to ciprofloxacin antibiotic stress correlates with increased nucleoid length and effective misfolded protein management |
title_short | Escherichia coli survival in response to ciprofloxacin antibiotic stress correlates with increased nucleoid length and effective misfolded protein management |
title_sort | escherichia coli survival in response to ciprofloxacin antibiotic stress correlates with increased nucleoid length and effective misfolded protein management |
topic | filamentation evolution resistance antibiotics |
url | https://royalsocietypublishing.org/doi/10.1098/rsos.230338 |
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