Integrative Conjugative Element ICE-βox Confers Oxidative Stress Resistance to <named-content content-type="genus-species">Legionella pneumophila</named-content> <italic toggle="yes">In Vitro</italic> and in Macrophages

ABSTRACT Integrative conjugative elements (ICEs) are mobile blocks of DNA that can contribute to bacterial evolution by self-directed transmission of advantageous traits. Here, we analyze the activity of a putative 65-kb ICE harbored by Legionella pneumophila using molecular genetics, conjugation as...

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Autores principales: Kaitlin J. Flynn, Michele S. Swanson
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Publicado: American Society for Microbiology 2014
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spelling oai:doaj.org-article:f677a952e21146b2ba80c5a167a990042021-11-15T15:47:39ZIntegrative Conjugative Element ICE-βox Confers Oxidative Stress Resistance to <named-content content-type="genus-species">Legionella pneumophila</named-content> <italic toggle="yes">In Vitro</italic> and in Macrophages10.1128/mBio.01091-142150-7511https://doaj.org/article/f677a952e21146b2ba80c5a167a990042014-07-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01091-14https://doaj.org/toc/2150-7511ABSTRACT Integrative conjugative elements (ICEs) are mobile blocks of DNA that can contribute to bacterial evolution by self-directed transmission of advantageous traits. Here, we analyze the activity of a putative 65-kb ICE harbored by Legionella pneumophila using molecular genetics, conjugation assays, a phenotype microarray screen, and macrophage infections. The element transferred to a naive L. pneumophila strain, integrated site-specifically, and conferred increased resistance to oxacillin, penicillin, hydrogen peroxide, and bleach. Furthermore, the element increased survival of L. pneumophila within restrictive mouse macrophages. In particular, this ICE protects L. pneumophila from phagocyte oxidase activity, since mutation of the macrophage NADPH oxidase eliminated the fitness difference between strains that carried and those that lacked the mobile element. Renamed ICE-βox (for β-lactam antibiotics and oxidative stress), this transposable element is predicted to contribute to the emergence of L. pneumophila strains that are more fit in natural and engineered water systems and in macrophages. IMPORTANCE Bacteria evolve rapidly by acquiring new traits via horizontal gene transfer. Integrative conjugative elements (ICEs) are mobile blocks of DNA that encode the machinery necessary to spread among bacterial populations. ICEs transfer antibiotic resistance and other bacterial survival factors as cargo genes carried within the element. Here, we show that Legionella pneumophila, the causative agent of Legionnaires’ disease, carries ICE-βox, which enhances the resistance of this opportunistic pathogen to bleach and β-lactam antibiotics. Moreover, L. pneumophila strains encoding ICE-βox are more resistant to macrophages that carry phagocyte oxidase. Accordingly, ICE-βox is predicted to increase the fitness of L. pneumophila in natural and engineered waters and in humans. To our knowledge, this is the first description of an ICE that confers oxidative stress resistance to a nosocomial pathogen.Kaitlin J. FlynnMichele S. SwansonAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 5, Iss 3 (2014)
institution DOAJ
collection DOAJ
language EN
topic Microbiology
QR1-502
spellingShingle Microbiology
QR1-502
Kaitlin J. Flynn
Michele S. Swanson
Integrative Conjugative Element ICE-βox Confers Oxidative Stress Resistance to <named-content content-type="genus-species">Legionella pneumophila</named-content> <italic toggle="yes">In Vitro</italic> and in Macrophages
description ABSTRACT Integrative conjugative elements (ICEs) are mobile blocks of DNA that can contribute to bacterial evolution by self-directed transmission of advantageous traits. Here, we analyze the activity of a putative 65-kb ICE harbored by Legionella pneumophila using molecular genetics, conjugation assays, a phenotype microarray screen, and macrophage infections. The element transferred to a naive L. pneumophila strain, integrated site-specifically, and conferred increased resistance to oxacillin, penicillin, hydrogen peroxide, and bleach. Furthermore, the element increased survival of L. pneumophila within restrictive mouse macrophages. In particular, this ICE protects L. pneumophila from phagocyte oxidase activity, since mutation of the macrophage NADPH oxidase eliminated the fitness difference between strains that carried and those that lacked the mobile element. Renamed ICE-βox (for β-lactam antibiotics and oxidative stress), this transposable element is predicted to contribute to the emergence of L. pneumophila strains that are more fit in natural and engineered water systems and in macrophages. IMPORTANCE Bacteria evolve rapidly by acquiring new traits via horizontal gene transfer. Integrative conjugative elements (ICEs) are mobile blocks of DNA that encode the machinery necessary to spread among bacterial populations. ICEs transfer antibiotic resistance and other bacterial survival factors as cargo genes carried within the element. Here, we show that Legionella pneumophila, the causative agent of Legionnaires’ disease, carries ICE-βox, which enhances the resistance of this opportunistic pathogen to bleach and β-lactam antibiotics. Moreover, L. pneumophila strains encoding ICE-βox are more resistant to macrophages that carry phagocyte oxidase. Accordingly, ICE-βox is predicted to increase the fitness of L. pneumophila in natural and engineered waters and in humans. To our knowledge, this is the first description of an ICE that confers oxidative stress resistance to a nosocomial pathogen.
format article
author Kaitlin J. Flynn
Michele S. Swanson
author_facet Kaitlin J. Flynn
Michele S. Swanson
author_sort Kaitlin J. Flynn
title Integrative Conjugative Element ICE-βox Confers Oxidative Stress Resistance to <named-content content-type="genus-species">Legionella pneumophila</named-content> <italic toggle="yes">In Vitro</italic> and in Macrophages
title_short Integrative Conjugative Element ICE-βox Confers Oxidative Stress Resistance to <named-content content-type="genus-species">Legionella pneumophila</named-content> <italic toggle="yes">In Vitro</italic> and in Macrophages
title_full Integrative Conjugative Element ICE-βox Confers Oxidative Stress Resistance to <named-content content-type="genus-species">Legionella pneumophila</named-content> <italic toggle="yes">In Vitro</italic> and in Macrophages
title_fullStr Integrative Conjugative Element ICE-βox Confers Oxidative Stress Resistance to <named-content content-type="genus-species">Legionella pneumophila</named-content> <italic toggle="yes">In Vitro</italic> and in Macrophages
title_full_unstemmed Integrative Conjugative Element ICE-βox Confers Oxidative Stress Resistance to <named-content content-type="genus-species">Legionella pneumophila</named-content> <italic toggle="yes">In Vitro</italic> and in Macrophages
title_sort integrative conjugative element ice-βox confers oxidative stress resistance to <named-content content-type="genus-species">legionella pneumophila</named-content> <italic toggle="yes">in vitro</italic> and in macrophages
publisher American Society for Microbiology
publishDate 2014
url https://doaj.org/article/f677a952e21146b2ba80c5a167a99004
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