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Antibiotic tolerance in environmentally stressed Bacillus subtilis: physical barriers and induction of a viable but nonculturable state

Bacterial communities exposed to rapid changes in their habitat encounter different forms of stress. Fluctuating conditions of the microenvironment drive microorganisms to develop several stress responses to sustain growth and division, like altering gene expression and changing the cell's phys...

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Autores principales: Morawska, Luiza P, Kuipers, Oscar P
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10117730/
https://www.ncbi.nlm.nih.gov/pubmed/37223363
http://dx.doi.org/10.1093/femsml/uqac010
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author Morawska, Luiza P
Kuipers, Oscar P
author_facet Morawska, Luiza P
Kuipers, Oscar P
author_sort Morawska, Luiza P
collection PubMed
description Bacterial communities exposed to rapid changes in their habitat encounter different forms of stress. Fluctuating conditions of the microenvironment drive microorganisms to develop several stress responses to sustain growth and division, like altering gene expression and changing the cell's physiology. It is commonly known that these protection systems may give rise to differently adapted subpopulations and indirectly impact bacterial susceptibility to antimicrobials. This study focuses on the adaptation of a soil-dwelling bacterium, Bacillus subtilis, to sudden osmotic changes, including transient and sustained osmotic upshift. Here, we demonstrate that physiological changes caused by pre-exposure to osmotic stress facilitate B. subtilis' entry into a quiescent state, helping them survive when exposed to a lethal antibiotic concentration. We show that the adaptation to transient osmotic upshift with 0.6 M NaCl causes decreased metabolic rates and lowered antibiotic-mediated ROS production when cells were exposed to the aminoglycoside antibiotic kanamycin. Using a microfluidic platform combined with time-lapse microscopy, we followed the uptake of fluorescently labelled kanamycin and examined the metabolic activity of differently preadapted populations at a single-cell level. The microfluidics data revealed that under the conditions tested, B. subtilis escapes from the bactericidal activity of kanamycin by entering into a nongrowing dormant state. Combining single-cell studies and population-wide analysis of differently preadapted cultures, we demonstrate that kanamycin-tolerant B. subtilis cells are entrapped in a viable but nonculturable (VBNC) state.
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spelling pubmed-101177302023-05-23 Antibiotic tolerance in environmentally stressed Bacillus subtilis: physical barriers and induction of a viable but nonculturable state Morawska, Luiza P Kuipers, Oscar P Microlife Research Article Bacterial communities exposed to rapid changes in their habitat encounter different forms of stress. Fluctuating conditions of the microenvironment drive microorganisms to develop several stress responses to sustain growth and division, like altering gene expression and changing the cell's physiology. It is commonly known that these protection systems may give rise to differently adapted subpopulations and indirectly impact bacterial susceptibility to antimicrobials. This study focuses on the adaptation of a soil-dwelling bacterium, Bacillus subtilis, to sudden osmotic changes, including transient and sustained osmotic upshift. Here, we demonstrate that physiological changes caused by pre-exposure to osmotic stress facilitate B. subtilis' entry into a quiescent state, helping them survive when exposed to a lethal antibiotic concentration. We show that the adaptation to transient osmotic upshift with 0.6 M NaCl causes decreased metabolic rates and lowered antibiotic-mediated ROS production when cells were exposed to the aminoglycoside antibiotic kanamycin. Using a microfluidic platform combined with time-lapse microscopy, we followed the uptake of fluorescently labelled kanamycin and examined the metabolic activity of differently preadapted populations at a single-cell level. The microfluidics data revealed that under the conditions tested, B. subtilis escapes from the bactericidal activity of kanamycin by entering into a nongrowing dormant state. Combining single-cell studies and population-wide analysis of differently preadapted cultures, we demonstrate that kanamycin-tolerant B. subtilis cells are entrapped in a viable but nonculturable (VBNC) state. Oxford University Press 2022-06-29 /pmc/articles/PMC10117730/ /pubmed/37223363 http://dx.doi.org/10.1093/femsml/uqac010 Text en © The Author(s) 2022. Published by Oxford University Press on behalf of FEMS. https://creativecommons.org/licenses/by-nc/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (https://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
spellingShingle Research Article
Morawska, Luiza P
Kuipers, Oscar P
Antibiotic tolerance in environmentally stressed Bacillus subtilis: physical barriers and induction of a viable but nonculturable state
title Antibiotic tolerance in environmentally stressed Bacillus subtilis: physical barriers and induction of a viable but nonculturable state
title_full Antibiotic tolerance in environmentally stressed Bacillus subtilis: physical barriers and induction of a viable but nonculturable state
title_fullStr Antibiotic tolerance in environmentally stressed Bacillus subtilis: physical barriers and induction of a viable but nonculturable state
title_full_unstemmed Antibiotic tolerance in environmentally stressed Bacillus subtilis: physical barriers and induction of a viable but nonculturable state
title_short Antibiotic tolerance in environmentally stressed Bacillus subtilis: physical barriers and induction of a viable but nonculturable state
title_sort antibiotic tolerance in environmentally stressed bacillus subtilis: physical barriers and induction of a viable but nonculturable state
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10117730/
https://www.ncbi.nlm.nih.gov/pubmed/37223363
http://dx.doi.org/10.1093/femsml/uqac010
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