Symbiont-Mediated Defense against <named-content content-type="genus-species">Legionella pneumophila</named-content> in Amoebae

ABSTRACT Legionella pneumophila is an important opportunistic pathogen for which environmental reservoirs are crucial for the infection of humans. In the environment, free-living amoebae represent key hosts providing nutrients and shelter for highly efficient intracellular proliferation of L. pneumo...

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Autores principales:	Lena König, Cecilia Wentrup, Frederik Schulz, Florian Wascher, Sarah Escola, Michele S. Swanson, Carmen Buchrieser, Matthias Horn
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	amoeba Legionella antimicrobial defense coinfection endosymbionts protists Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/d5736ccbd5bf4404863ec21a6bad8be6
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spelling	oai:doaj.org-article:d5736ccbd5bf4404863ec21a6bad8be62021-11-15T15:55:25ZSymbiont-Mediated Defense against <named-content content-type="genus-species">Legionella pneumophila</named-content> in Amoebae10.1128/mBio.00333-192150-7511https://doaj.org/article/d5736ccbd5bf4404863ec21a6bad8be62019-06-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00333-19https://doaj.org/toc/2150-7511ABSTRACT Legionella pneumophila is an important opportunistic pathogen for which environmental reservoirs are crucial for the infection of humans. In the environment, free-living amoebae represent key hosts providing nutrients and shelter for highly efficient intracellular proliferation of L. pneumophila, which eventually leads to lysis of the protist. However, the significance of other bacterial players for L. pneumophila ecology is poorly understood. In this study, we used a ubiquitous amoeba and bacterial endosymbiont to investigate the impact of this common association on L. pneumophila infection. We demonstrate that L. pneumophila proliferation was severely suppressed in Acanthamoeba castellanii harboring the chlamydial symbiont Protochlamydia amoebophila. The amoebae survived the infection and were able to resume growth. Different environmental amoeba isolates containing the symbiont were equally well protected as different L. pneumophila isolates were diminished, suggesting ecological relevance of this symbiont-mediated defense. Furthermore, protection was not mediated by impaired L. pneumophila uptake. Instead, we observed reduced virulence of L. pneumophila released from symbiont-containing amoebae. Pronounced gene expression changes in the presence of the symbiont indicate that interference with the transition to the transmissive phase impedes the L. pneumophila infection. Finally, our data show that the defensive response of amoebae harboring P. amoebophila leaves the amoebae with superior fitness reminiscent of immunological memory. Given that mutualistic associations between bacteria and amoebae are widely distributed, P. amoebophila and potentially other amoeba endosymbionts could be key in shaping environmental survival, abundance, and virulence of this important pathogen, thereby affecting the frequency of human infection. IMPORTANCE Bacterial pathogens are generally investigated in the context of disease. To prevent outbreaks, it is essential to understand their lifestyle and interactions with other microbes in their natural environment. Legionella pneumophila is an important human respiratory pathogen that survives and multiplies in biofilms or intracellularly within protists, such as amoebae. Importantly, transmission to humans occurs from these environmental sources. Legionella infection generally leads to rapid host cell lysis. It was therefore surprising to observe that amoebae, including fresh environmental isolates, were well protected during Legionella infection when the bacterial symbiont Protochlamydia amoebophila was also present. Legionella was not prevented from invading amoebae but was impeded in its ability to develop fully virulent progeny and were ultimately cleared in the presence of the symbiont. This study highlights how ecology and virulence of an important human pathogen is affected by a defensive amoeba symbiont, with possibly major consequences for public health.Lena KönigCecilia WentrupFrederik SchulzFlorian WascherSarah EscolaMichele S. SwansonCarmen BuchrieserMatthias HornAmerican Society for MicrobiologyarticleamoebaLegionellaantimicrobial defensecoinfectionendosymbiontsprotistsMicrobiologyQR1-502ENmBio, Vol 10, Iss 3 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	amoeba Legionella antimicrobial defense coinfection endosymbionts protists Microbiology QR1-502
spellingShingle	amoeba Legionella antimicrobial defense coinfection endosymbionts protists Microbiology QR1-502 Lena König Cecilia Wentrup Frederik Schulz Florian Wascher Sarah Escola Michele S. Swanson Carmen Buchrieser Matthias Horn Symbiont-Mediated Defense against <named-content content-type="genus-species">Legionella pneumophila</named-content> in Amoebae
description	ABSTRACT Legionella pneumophila is an important opportunistic pathogen for which environmental reservoirs are crucial for the infection of humans. In the environment, free-living amoebae represent key hosts providing nutrients and shelter for highly efficient intracellular proliferation of L. pneumophila, which eventually leads to lysis of the protist. However, the significance of other bacterial players for L. pneumophila ecology is poorly understood. In this study, we used a ubiquitous amoeba and bacterial endosymbiont to investigate the impact of this common association on L. pneumophila infection. We demonstrate that L. pneumophila proliferation was severely suppressed in Acanthamoeba castellanii harboring the chlamydial symbiont Protochlamydia amoebophila. The amoebae survived the infection and were able to resume growth. Different environmental amoeba isolates containing the symbiont were equally well protected as different L. pneumophila isolates were diminished, suggesting ecological relevance of this symbiont-mediated defense. Furthermore, protection was not mediated by impaired L. pneumophila uptake. Instead, we observed reduced virulence of L. pneumophila released from symbiont-containing amoebae. Pronounced gene expression changes in the presence of the symbiont indicate that interference with the transition to the transmissive phase impedes the L. pneumophila infection. Finally, our data show that the defensive response of amoebae harboring P. amoebophila leaves the amoebae with superior fitness reminiscent of immunological memory. Given that mutualistic associations between bacteria and amoebae are widely distributed, P. amoebophila and potentially other amoeba endosymbionts could be key in shaping environmental survival, abundance, and virulence of this important pathogen, thereby affecting the frequency of human infection. IMPORTANCE Bacterial pathogens are generally investigated in the context of disease. To prevent outbreaks, it is essential to understand their lifestyle and interactions with other microbes in their natural environment. Legionella pneumophila is an important human respiratory pathogen that survives and multiplies in biofilms or intracellularly within protists, such as amoebae. Importantly, transmission to humans occurs from these environmental sources. Legionella infection generally leads to rapid host cell lysis. It was therefore surprising to observe that amoebae, including fresh environmental isolates, were well protected during Legionella infection when the bacterial symbiont Protochlamydia amoebophila was also present. Legionella was not prevented from invading amoebae but was impeded in its ability to develop fully virulent progeny and were ultimately cleared in the presence of the symbiont. This study highlights how ecology and virulence of an important human pathogen is affected by a defensive amoeba symbiont, with possibly major consequences for public health.
format	article
author	Lena König Cecilia Wentrup Frederik Schulz Florian Wascher Sarah Escola Michele S. Swanson Carmen Buchrieser Matthias Horn
author_facet	Lena König Cecilia Wentrup Frederik Schulz Florian Wascher Sarah Escola Michele S. Swanson Carmen Buchrieser Matthias Horn
author_sort	Lena König
title	Symbiont-Mediated Defense against <named-content content-type="genus-species">Legionella pneumophila</named-content> in Amoebae
title_short	Symbiont-Mediated Defense against <named-content content-type="genus-species">Legionella pneumophila</named-content> in Amoebae
title_full	Symbiont-Mediated Defense against <named-content content-type="genus-species">Legionella pneumophila</named-content> in Amoebae
title_fullStr	Symbiont-Mediated Defense against <named-content content-type="genus-species">Legionella pneumophila</named-content> in Amoebae
title_full_unstemmed	Symbiont-Mediated Defense against <named-content content-type="genus-species">Legionella pneumophila</named-content> in Amoebae
title_sort	symbiont-mediated defense against <named-content content-type="genus-species">legionella pneumophila</named-content> in amoebae
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/d5736ccbd5bf4404863ec21a6bad8be6
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Symbiont-Mediated Defense against <named-content content-type="genus-species">Legionella pneumophila</named-content> in Amoebae

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