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Exposure of Salmonella biofilms to antibiotic concentrations rapidly selects resistance with collateral tradeoffs

Most bacteria in nature exist in biofilms, which are inherently tolerant to antibiotics. There is currently very limited understanding of how biofilms evolve in response to sub-lethal concentrations of antimicrobials. In this study, we use a biofilm evolution model to study the effects of sub-inhibi...

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Autores principales: Trampari, Eleftheria, Holden, Emma R., Wickham, Gregory J., Ravi, Anuradha, Martins, Leonardo de Oliveira, Savva, George M., Webber, Mark A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7801651/
https://www.ncbi.nlm.nih.gov/pubmed/33431848
http://dx.doi.org/10.1038/s41522-020-00178-0
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author Trampari, Eleftheria
Holden, Emma R.
Wickham, Gregory J.
Ravi, Anuradha
Martins, Leonardo de Oliveira
Savva, George M.
Webber, Mark A.
author_facet Trampari, Eleftheria
Holden, Emma R.
Wickham, Gregory J.
Ravi, Anuradha
Martins, Leonardo de Oliveira
Savva, George M.
Webber, Mark A.
author_sort Trampari, Eleftheria
collection PubMed
description Most bacteria in nature exist in biofilms, which are inherently tolerant to antibiotics. There is currently very limited understanding of how biofilms evolve in response to sub-lethal concentrations of antimicrobials. In this study, we use a biofilm evolution model to study the effects of sub-inhibitory concentrations of three antibiotics on Salmonella Typhimurium biofilms. We show that biofilms rapidly evolve resistance to each antibiotic they are exposed to, demonstrating a strong selective pressure on biofilms from low antibiotic concentrations. While all antibiotics tested select for clinical resistance, there is no common mechanism. Adaptation to antimicrobials, however, has a marked cost for other clinically important phenotypes, including biofilm formation and virulence. Cefotaxime selects mutants with the greatest deficit in biofilm formation followed by azithromycin and then ciprofloxacin. Understanding the impacts of exposure of biofilms to antibiotics will help understand evolutionary trajectories and may help guide how best to use antibiotics in a biofilm context. Experimental evolution in combination with whole-genome sequencing is a powerful tool for the prediction of evolution trajectories associated with antibiotic resistance in biofilms.
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spelling pubmed-78016512021-01-21 Exposure of Salmonella biofilms to antibiotic concentrations rapidly selects resistance with collateral tradeoffs Trampari, Eleftheria Holden, Emma R. Wickham, Gregory J. Ravi, Anuradha Martins, Leonardo de Oliveira Savva, George M. Webber, Mark A. NPJ Biofilms Microbiomes Article Most bacteria in nature exist in biofilms, which are inherently tolerant to antibiotics. There is currently very limited understanding of how biofilms evolve in response to sub-lethal concentrations of antimicrobials. In this study, we use a biofilm evolution model to study the effects of sub-inhibitory concentrations of three antibiotics on Salmonella Typhimurium biofilms. We show that biofilms rapidly evolve resistance to each antibiotic they are exposed to, demonstrating a strong selective pressure on biofilms from low antibiotic concentrations. While all antibiotics tested select for clinical resistance, there is no common mechanism. Adaptation to antimicrobials, however, has a marked cost for other clinically important phenotypes, including biofilm formation and virulence. Cefotaxime selects mutants with the greatest deficit in biofilm formation followed by azithromycin and then ciprofloxacin. Understanding the impacts of exposure of biofilms to antibiotics will help understand evolutionary trajectories and may help guide how best to use antibiotics in a biofilm context. Experimental evolution in combination with whole-genome sequencing is a powerful tool for the prediction of evolution trajectories associated with antibiotic resistance in biofilms. Nature Publishing Group UK 2021-01-11 /pmc/articles/PMC7801651/ /pubmed/33431848 http://dx.doi.org/10.1038/s41522-020-00178-0 Text en © The Author(s) 2021 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Trampari, Eleftheria
Holden, Emma R.
Wickham, Gregory J.
Ravi, Anuradha
Martins, Leonardo de Oliveira
Savva, George M.
Webber, Mark A.
Exposure of Salmonella biofilms to antibiotic concentrations rapidly selects resistance with collateral tradeoffs
title Exposure of Salmonella biofilms to antibiotic concentrations rapidly selects resistance with collateral tradeoffs
title_full Exposure of Salmonella biofilms to antibiotic concentrations rapidly selects resistance with collateral tradeoffs
title_fullStr Exposure of Salmonella biofilms to antibiotic concentrations rapidly selects resistance with collateral tradeoffs
title_full_unstemmed Exposure of Salmonella biofilms to antibiotic concentrations rapidly selects resistance with collateral tradeoffs
title_short Exposure of Salmonella biofilms to antibiotic concentrations rapidly selects resistance with collateral tradeoffs
title_sort exposure of salmonella biofilms to antibiotic concentrations rapidly selects resistance with collateral tradeoffs
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7801651/
https://www.ncbi.nlm.nih.gov/pubmed/33431848
http://dx.doi.org/10.1038/s41522-020-00178-0
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