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

Abstract 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 s...

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Autores principales: Eleftheria Trampari, Emma R. Holden, Gregory J. Wickham, Anuradha Ravi, Leonardo de Oliveira Martins, George M. Savva, Mark A. Webber
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Publicado: Nature Portfolio 2021
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Acceso en línea:https://doaj.org/article/c9ba790d305b43acb0b9c148b1734630
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spelling oai:doaj.org-article:c9ba790d305b43acb0b9c148b17346302021-12-02T15:23:15ZExposure of Salmonella biofilms to antibiotic concentrations rapidly selects resistance with collateral tradeoffs10.1038/s41522-020-00178-02055-5008https://doaj.org/article/c9ba790d305b43acb0b9c148b17346302021-01-01T00:00:00Zhttps://doi.org/10.1038/s41522-020-00178-0https://doaj.org/toc/2055-5008Abstract 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.Eleftheria TrampariEmma R. HoldenGregory J. WickhamAnuradha RaviLeonardo de Oliveira MartinsGeorge M. SavvaMark A. WebberNature PortfolioarticleMicrobial ecologyQR100-130ENnpj Biofilms and Microbiomes, Vol 7, Iss 1, Pp 1-13 (2021)
institution DOAJ
collection DOAJ
language EN
topic Microbial ecology
QR100-130
spellingShingle Microbial ecology
QR100-130
Eleftheria Trampari
Emma R. Holden
Gregory J. Wickham
Anuradha Ravi
Leonardo de Oliveira Martins
George M. Savva
Mark A. Webber
Exposure of Salmonella biofilms to antibiotic concentrations rapidly selects resistance with collateral tradeoffs
description Abstract 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.
format article
author Eleftheria Trampari
Emma R. Holden
Gregory J. Wickham
Anuradha Ravi
Leonardo de Oliveira Martins
George M. Savva
Mark A. Webber
author_facet Eleftheria Trampari
Emma R. Holden
Gregory J. Wickham
Anuradha Ravi
Leonardo de Oliveira Martins
George M. Savva
Mark A. Webber
author_sort Eleftheria Trampari
title 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_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_sort exposure of salmonella biofilms to antibiotic concentrations rapidly selects resistance with collateral tradeoffs
publisher Nature Portfolio
publishDate 2021
url https://doaj.org/article/c9ba790d305b43acb0b9c148b1734630
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