Carriage of extended-spectrum beta-lactamase-plasmids does not reduce fitness but enhances virulence in some strains of pandemic E. coli lineages

Pathogenic ESBL-producing E. coli lineages occur frequently worldwide, not only in a human health context but in animals and the environment, also in settings with low antimicrobial pressures. This study investigated the fitness costs of ESBL-plasmids and their influence on chromosomally encoded fea...

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Main Authors: Katharina eSchaufler, Torsten eSemmler, Derek J Pickard, Maria ede Toro, Fernando ede la Cruz, Lothar H Wieler, Christa eEwers, Sebastian eGuenther
Format: Article
Language:English
Published: Frontiers Media S.A. 2016-03-01
Series:Frontiers in Microbiology
Subjects:
Online Access:http://journal.frontiersin.org/Journal/10.3389/fmicb.2016.00336/full
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spelling doaj-06eb6514d92b45febd68d6335212ed3f2020-11-25T01:40:08ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2016-03-01710.3389/fmicb.2016.00336181976Carriage of extended-spectrum beta-lactamase-plasmids does not reduce fitness but enhances virulence in some strains of pandemic E. coli lineagesKatharina eSchaufler0Torsten eSemmler1Derek J Pickard2Maria ede Toro3Fernando ede la Cruz4Lothar H Wieler5Christa eEwers6Sebastian eGuenther7Freie Universität BerlinRobert Koch InstituteWellcome Trust Sanger InstituteUniversidad de CantabriaUniversidad de CantabriaRobert Koch InstituteJustus-Liebig-Universität GiessenFreie Universität BerlinPathogenic ESBL-producing E. coli lineages occur frequently worldwide, not only in a human health context but in animals and the environment, also in settings with low antimicrobial pressures. This study investigated the fitness costs of ESBL-plasmids and their influence on chromosomally encoded features associated with virulence, such as those involved in the planktonic and sessile behaviors of ST131 and ST648 E. coli. ESBL-plasmid-carrying wild-type E. coli strains, their corresponding ESBL-plasmid-cured variants (PCV), and complementary ESBL-carrying transformants were comparatively analyzed using growth curves, Omnilog® phenotype microarray (PM) assays, macrocolony and biofilm formation, swimming motility, and RNA sequence analysis. Growth curves and PM results pointed towards similar growth and metabolic behaviors among the strains. Phenotypic differences in some strains were detected, including enhanced curli fimbriae and/or cellulose production as well as a reduced swimming capacity of some ESBL-carrying strains, as compared to their respective PCVs. RNA sequencing mostly confirmed the phenotypic results, suggesting that the chromosomally encoded csgD pathway is a key factor involved. These results contradict the hypothesis that ESBL-plasmid-carriage leads to a fitness loss in ESBL-carrying strains. Instead, the results indicate an influence of some ESBL-plasmids on chromosomally encoded features associated with virulence in some E. coli strains. In conclusion, apart from antibiotic resistance selective advantages, ESBL-plasmid-carriage may also lead to enhanced virulence or adaption to specific habitats in some strains of pandemic ESBL-producing E. coli lineages.http://journal.frontiersin.org/Journal/10.3389/fmicb.2016.00336/fullFitness costsBiofilm formationESBL-producing E. coliESBL-plasmidsenhanced virulencePlasmid and host interaction
collection DOAJ
language English
format Article
sources DOAJ
author Katharina eSchaufler
Torsten eSemmler
Derek J Pickard
Maria ede Toro
Fernando ede la Cruz
Lothar H Wieler
Christa eEwers
Sebastian eGuenther
spellingShingle Katharina eSchaufler
Torsten eSemmler
Derek J Pickard
Maria ede Toro
Fernando ede la Cruz
Lothar H Wieler
Christa eEwers
Sebastian eGuenther
Carriage of extended-spectrum beta-lactamase-plasmids does not reduce fitness but enhances virulence in some strains of pandemic E. coli lineages
Frontiers in Microbiology
Fitness costs
Biofilm formation
ESBL-producing E. coli
ESBL-plasmids
enhanced virulence
Plasmid and host interaction
author_facet Katharina eSchaufler
Torsten eSemmler
Derek J Pickard
Maria ede Toro
Fernando ede la Cruz
Lothar H Wieler
Christa eEwers
Sebastian eGuenther
author_sort Katharina eSchaufler
title Carriage of extended-spectrum beta-lactamase-plasmids does not reduce fitness but enhances virulence in some strains of pandemic E. coli lineages
title_short Carriage of extended-spectrum beta-lactamase-plasmids does not reduce fitness but enhances virulence in some strains of pandemic E. coli lineages
title_full Carriage of extended-spectrum beta-lactamase-plasmids does not reduce fitness but enhances virulence in some strains of pandemic E. coli lineages
title_fullStr Carriage of extended-spectrum beta-lactamase-plasmids does not reduce fitness but enhances virulence in some strains of pandemic E. coli lineages
title_full_unstemmed Carriage of extended-spectrum beta-lactamase-plasmids does not reduce fitness but enhances virulence in some strains of pandemic E. coli lineages
title_sort carriage of extended-spectrum beta-lactamase-plasmids does not reduce fitness but enhances virulence in some strains of pandemic e. coli lineages
publisher Frontiers Media S.A.
series Frontiers in Microbiology
issn 1664-302X
publishDate 2016-03-01
description Pathogenic ESBL-producing E. coli lineages occur frequently worldwide, not only in a human health context but in animals and the environment, also in settings with low antimicrobial pressures. This study investigated the fitness costs of ESBL-plasmids and their influence on chromosomally encoded features associated with virulence, such as those involved in the planktonic and sessile behaviors of ST131 and ST648 E. coli. ESBL-plasmid-carrying wild-type E. coli strains, their corresponding ESBL-plasmid-cured variants (PCV), and complementary ESBL-carrying transformants were comparatively analyzed using growth curves, Omnilog® phenotype microarray (PM) assays, macrocolony and biofilm formation, swimming motility, and RNA sequence analysis. Growth curves and PM results pointed towards similar growth and metabolic behaviors among the strains. Phenotypic differences in some strains were detected, including enhanced curli fimbriae and/or cellulose production as well as a reduced swimming capacity of some ESBL-carrying strains, as compared to their respective PCVs. RNA sequencing mostly confirmed the phenotypic results, suggesting that the chromosomally encoded csgD pathway is a key factor involved. These results contradict the hypothesis that ESBL-plasmid-carriage leads to a fitness loss in ESBL-carrying strains. Instead, the results indicate an influence of some ESBL-plasmids on chromosomally encoded features associated with virulence in some E. coli strains. In conclusion, apart from antibiotic resistance selective advantages, ESBL-plasmid-carriage may also lead to enhanced virulence or adaption to specific habitats in some strains of pandemic ESBL-producing E. coli lineages.
topic Fitness costs
Biofilm formation
ESBL-producing E. coli
ESBL-plasmids
enhanced virulence
Plasmid and host interaction
url http://journal.frontiersin.org/Journal/10.3389/fmicb.2016.00336/full
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