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
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2014
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/f677a952e21146b2ba80c5a167a99004
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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
work_keys_str_mv	AT kaitlinjflynn integrativeconjugativeelementiceboxconfersoxidativestressresistancetonamedcontentcontenttypegenusspecieslegionellapneumophilanamedcontentitalictoggleyesinvitroitalicandinmacrophages AT michelesswanson integrativeconjugativeelementiceboxconfersoxidativestressresistancetonamedcontentcontenttypegenusspecieslegionellapneumophilanamedcontentitalictoggleyesinvitroitalicandinmacrophages
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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

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