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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Main Authors: George Butler, Julia Bos, Robert H. Austin, Sarah R. Amend, Kenneth J. Pienta
Format: Article
Language:English
Published: The Royal Society 2023-08-01
Series:Royal Society Open Science
Subjects:
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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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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