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ESBL-plasmid carriage in E. coli enhances in vitro bacterial competition fitness and serum resistance in some strains of pandemic sequence types without overall fitness cost

BACKGROUND: Extended spectrum beta lactamase (ESBL)-producing extraintestinal pathogenic Escherichia coli infections are of global interest because of their clinical and economic impact. The ESBL resistance genes disseminate through plasmids, and are found in successful global lineages such as ST131...

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Autores principales: Ranjan, Amit, Scholz, Julia, Semmler, Torsten, Wieler, Lothar H., Ewers, Christa, Müller, Stefanie, Pickard, Derek J., Schierack, Peter, Tedin, Karsten, Ahmed, Niyaz, Schaufler, Katharina, Guenther, Sebastian
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6003029/
https://www.ncbi.nlm.nih.gov/pubmed/29983750
http://dx.doi.org/10.1186/s13099-018-0243-z
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author Ranjan, Amit
Scholz, Julia
Semmler, Torsten
Wieler, Lothar H.
Ewers, Christa
Müller, Stefanie
Pickard, Derek J.
Schierack, Peter
Tedin, Karsten
Ahmed, Niyaz
Schaufler, Katharina
Guenther, Sebastian
author_facet Ranjan, Amit
Scholz, Julia
Semmler, Torsten
Wieler, Lothar H.
Ewers, Christa
Müller, Stefanie
Pickard, Derek J.
Schierack, Peter
Tedin, Karsten
Ahmed, Niyaz
Schaufler, Katharina
Guenther, Sebastian
author_sort Ranjan, Amit
collection PubMed
description BACKGROUND: Extended spectrum beta lactamase (ESBL)-producing extraintestinal pathogenic Escherichia coli infections are of global interest because of their clinical and economic impact. The ESBL resistance genes disseminate through plasmids, and are found in successful global lineages such as ST131 and ST648. The carriage of plasmids has been suggested to result in a fitness burden, but recently it was shown that ESBL-plasmids enhanced virulence in pandemic ST131 and ST648 lineages without affecting their fitness. Herein, we investigated the influence of ESBL-plasmids on bacterial competition and serum resistance, both of which are essential characteristics of ExPEC during infections. METHODS: Triplets of ESBL-plasmid-carrying wildtype (WT), plasmid-cured variant (PCV) and transformant (T) of five ExPEC strains of ST131 and ST648 were used for bacterial competition experiments with colicin-producing commensal E. coli, competitive adhesion experiments and serum survival. In addition, resilience after SDS, acid, osmotic challenges and RNA sequence data were analyzed. RESULTS: In all five strains tested, ESBL-plasmid carriage did not negatively influence E. coli fitness in direct bacterial competition with commensal E. coli in vitro. That is, WTs did not show any disadvantages when compared to their isogenic plasmid-free PCV. For one strain we even found the opposite as PCV17433 was out-competed by a commensal strain, which suggests an even protective role of the ESBL-plasmid carried by the WT17433. Similarly, in the serum-resistance experiments, the PCVs of two strains (PCV17433 and PCV17887) were more sensitive to serum, unlike WTs and Ts. The observed inter-strain differences could be explained by the different genetic content of plasmids carried in those strains. CONCLUSIONS: Overall, we found no compelling evidence for an increased burden resulting from the carriage of ESBL-plasmids in the absence of antimicrobial selection pressure in the strains of pandemic ST131 and ST648; rather, the possession of certain ESBL-plasmids was beneficial for some strains in regarding competition fitness and serum survival. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s13099-018-0243-z) contains supplementary material, which is available to authorized users.
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spelling pubmed-60030292018-07-06 ESBL-plasmid carriage in E. coli enhances in vitro bacterial competition fitness and serum resistance in some strains of pandemic sequence types without overall fitness cost Ranjan, Amit Scholz, Julia Semmler, Torsten Wieler, Lothar H. Ewers, Christa Müller, Stefanie Pickard, Derek J. Schierack, Peter Tedin, Karsten Ahmed, Niyaz Schaufler, Katharina Guenther, Sebastian Gut Pathog Research BACKGROUND: Extended spectrum beta lactamase (ESBL)-producing extraintestinal pathogenic Escherichia coli infections are of global interest because of their clinical and economic impact. The ESBL resistance genes disseminate through plasmids, and are found in successful global lineages such as ST131 and ST648. The carriage of plasmids has been suggested to result in a fitness burden, but recently it was shown that ESBL-plasmids enhanced virulence in pandemic ST131 and ST648 lineages without affecting their fitness. Herein, we investigated the influence of ESBL-plasmids on bacterial competition and serum resistance, both of which are essential characteristics of ExPEC during infections. METHODS: Triplets of ESBL-plasmid-carrying wildtype (WT), plasmid-cured variant (PCV) and transformant (T) of five ExPEC strains of ST131 and ST648 were used for bacterial competition experiments with colicin-producing commensal E. coli, competitive adhesion experiments and serum survival. In addition, resilience after SDS, acid, osmotic challenges and RNA sequence data were analyzed. RESULTS: In all five strains tested, ESBL-plasmid carriage did not negatively influence E. coli fitness in direct bacterial competition with commensal E. coli in vitro. That is, WTs did not show any disadvantages when compared to their isogenic plasmid-free PCV. For one strain we even found the opposite as PCV17433 was out-competed by a commensal strain, which suggests an even protective role of the ESBL-plasmid carried by the WT17433. Similarly, in the serum-resistance experiments, the PCVs of two strains (PCV17433 and PCV17887) were more sensitive to serum, unlike WTs and Ts. The observed inter-strain differences could be explained by the different genetic content of plasmids carried in those strains. CONCLUSIONS: Overall, we found no compelling evidence for an increased burden resulting from the carriage of ESBL-plasmids in the absence of antimicrobial selection pressure in the strains of pandemic ST131 and ST648; rather, the possession of certain ESBL-plasmids was beneficial for some strains in regarding competition fitness and serum survival. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s13099-018-0243-z) contains supplementary material, which is available to authorized users. BioMed Central 2018-06-15 /pmc/articles/PMC6003029/ /pubmed/29983750 http://dx.doi.org/10.1186/s13099-018-0243-z Text en © The Author(s) 2018 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided 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 Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Ranjan, Amit
Scholz, Julia
Semmler, Torsten
Wieler, Lothar H.
Ewers, Christa
Müller, Stefanie
Pickard, Derek J.
Schierack, Peter
Tedin, Karsten
Ahmed, Niyaz
Schaufler, Katharina
Guenther, Sebastian
ESBL-plasmid carriage in E. coli enhances in vitro bacterial competition fitness and serum resistance in some strains of pandemic sequence types without overall fitness cost
title ESBL-plasmid carriage in E. coli enhances in vitro bacterial competition fitness and serum resistance in some strains of pandemic sequence types without overall fitness cost
title_full ESBL-plasmid carriage in E. coli enhances in vitro bacterial competition fitness and serum resistance in some strains of pandemic sequence types without overall fitness cost
title_fullStr ESBL-plasmid carriage in E. coli enhances in vitro bacterial competition fitness and serum resistance in some strains of pandemic sequence types without overall fitness cost
title_full_unstemmed ESBL-plasmid carriage in E. coli enhances in vitro bacterial competition fitness and serum resistance in some strains of pandemic sequence types without overall fitness cost
title_short ESBL-plasmid carriage in E. coli enhances in vitro bacterial competition fitness and serum resistance in some strains of pandemic sequence types without overall fitness cost
title_sort esbl-plasmid carriage in e. coli enhances in vitro bacterial competition fitness and serum resistance in some strains of pandemic sequence types without overall fitness cost
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6003029/
https://www.ncbi.nlm.nih.gov/pubmed/29983750
http://dx.doi.org/10.1186/s13099-018-0243-z
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