Quorum sensing governs a transmissive Legionella subpopulation at the pathogen vacuole periphery

The Gram-negative bacterium Legionella pneumophila is the causative agent of Legionnaires' disease and replicates in amoebae and macrophages within a distinct compartment, the Legionella -containing vacuole (LCV). The facultative intracellular pathogen switches between a replicative, non-virule...

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Published inEMBO reports Vol. 22; no. 9; pp. e52972 - n/a
Main Authors Striednig, Bianca, Lanner, Ulrike, Niggli, Selina, Katic, Ana, Vormittag, Simone, Brülisauer, Sabrina, Hochstrasser, Ramon, Kaech, Andres, Welin, Amanda, Flieger, Antje, Ziegler, Urs, Schmidt, Alexander, Hilbi, Hubert, Personnic, Nicolas
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 06.09.2021
Springer Nature B.V
EMBO Press
John Wiley and Sons Inc
Subjects
Amoeba
Bacteria
Cell division
Clusters
EMBO20
EMBO23
EMBO37
Flagella
flagellum
Heterogeneity
Intracellular
Legionella
Legionella pneumophila
Legionnaire's disease
Legionnaires' disease
Legionnaires' disease bacterium
Life cycles
Life Sciences
Lysis
Macrophages
pathogen vacuole
Pathogens
Phagocytes
phenotypic heterogeneity
Proteins
proteome
Proteomes
Proteomics
Quorum sensing
Subpopulations
Switches
Virulence
phenotypic heterogeneity
quorum sensing
flagellum
pathogen vacuole
proteome
Signal Transduction
Microbiology, Virology & Host Pathogen Interaction
flagellum pathogen vacuole phenotypic heterogeneity proteome quorum sensing Subject Categories Membranes & Trafficking Microbiology, Virology & Host Pathogen Interaction Signal Transduction
quorum sensing Subject Categories Membranes & Trafficking
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Abstract The Gram-negative bacterium Legionella pneumophila is the causative agent of Legionnaires' disease and replicates in amoebae and macrophages within a distinct compartment, the Legionella -containing vacuole (LCV). The facultative intracellular pathogen switches between a replicative, non-virulent and a non-replicating, virulent/transmissive phase. Here, we show on a single-cell level that at late stages of infection, individual motile (P flaA -GFP-positive) and virulent (P ralF - and P sidC -GFP-positive) L. pneumophila emerge in the cluster of non-growing bacteria within an LCV. Comparative proteomics of P flaA -GFP-positive and P flaA -GFP-negative L. pneumophila subpopulations reveals distinct proteomes with flagellar proteins or cell division proteins being preferentially produced by the former or the latter, respectively. Toward the end of an infection cycle (˜ 48 h), the P flaA -GFP-positive L. pneumophila subpopulation emerges at the cluster periphery, predominantly escapes the LCV, and spreads from the bursting host cell. These processes are mediated by the Legionella quorum sensing (Lqs) system. Thus, quorum sensing regulates the emergence of a subpopulation of transmissive L. pneumophila at the LCV periphery, and phenotypic heterogeneity underlies the intravacuolar bi-phasic life cycle of L. pneumophila . Synopsis Legionella forms a distinct vacuole in phagocytes, wherein the pathogen adopts a bi-phasic life cycle and phenotypic heterogeneity. Quorum sensing elicits a transmissive subpopulation at the vacuole periphery, which spearheads compartment exit and host cell lysis. Legionella pneumophila switches between a replicative and a virulent/transmissive phase in its unique intracellular vacuole. The intravacuolar bi-phasic life cycle displays phenotypic heterogeneity. Quorum sensing elicits a transmissive subpopulation at the vacuole periphery, promoting compartment exit and cell lysis. Graphical Abstract Legionella forms a distinct vacuole in phagocytes, wherein the pathogen adopts a bi-phasic life cycle and phenotypic heterogeneity. Quorum sensing elicits a transmissive subpopulation at the vacuole periphery, which spearheads compartment exit and host cell lysis.
AbstractList The Gram-negative bacterium Legionella pneumophila is the causative agent of Legionnaires' disease and replicates in amoebae and macrophages within a distinct compartment, the Legionella-containing vacuole (LCV). The facultative intracellular pathogen switches between a replicative, non-virulent and a non-replicating, virulent/transmissive phase. Here, we show on a single-cell level that at late stages of infection, individual motile (PflaA -GFP-positive) and virulent (PralF - and PsidC -GFP-positive) L. pneumophila emerge in the cluster of non-growing bacteria within an LCV. Comparative proteomics of PflaA -GFP-positive and PflaA -GFP-negative L. pneumophila subpopulations reveals distinct proteomes with flagellar proteins or cell division proteins being preferentially produced by the former or the latter, respectively. Toward the end of an infection cycle (˜ 48 h), the PflaA -GFP-positive L. pneumophila subpopulation emerges at the cluster periphery, predominantly escapes the LCV, and spreads from the bursting host cell. These processes are mediated by the Legionella quorum sensing (Lqs) system. Thus, quorum sensing regulates the emergence of a subpopulation of transmissive L. pneumophila at the LCV periphery, and phenotypic heterogeneity underlies the intravacuolar bi-phasic life cycle of L. pneumophila.The Gram-negative bacterium Legionella pneumophila is the causative agent of Legionnaires' disease and replicates in amoebae and macrophages within a distinct compartment, the Legionella-containing vacuole (LCV). The facultative intracellular pathogen switches between a replicative, non-virulent and a non-replicating, virulent/transmissive phase. Here, we show on a single-cell level that at late stages of infection, individual motile (PflaA -GFP-positive) and virulent (PralF - and PsidC -GFP-positive) L. pneumophila emerge in the cluster of non-growing bacteria within an LCV. Comparative proteomics of PflaA -GFP-positive and PflaA -GFP-negative L. pneumophila subpopulations reveals distinct proteomes with flagellar proteins or cell division proteins being preferentially produced by the former or the latter, respectively. Toward the end of an infection cycle (˜ 48 h), the PflaA -GFP-positive L. pneumophila subpopulation emerges at the cluster periphery, predominantly escapes the LCV, and spreads from the bursting host cell. These processes are mediated by the Legionella quorum sensing (Lqs) system. Thus, quorum sensing regulates the emergence of a subpopulation of transmissive L. pneumophila at the LCV periphery, and phenotypic heterogeneity underlies the intravacuolar bi-phasic life cycle of L. pneumophila.
The Gram-negative bacterium Legionella pneumophila is the causative agent of Legionnaires disease and replicates in amoebae and macrophages within a distinct compartment, the Legionella-containing vacuole (LCV). The facultative intracellular pathogen switches between a replicative, non-virulent and a non-replicating, virulent/transmissive phase. Here, we show on a single-cell level that at late stages of infection, individual motile (P-flaA-GFP-positive) and virulent (P-ralF- and P-sidC-GFP-positive) L. pneumophila emerge in the cluster of non-growing bacteria within an LCV. Comparative proteomics of P-flaA-GFP-positive and P-flaA-GFP-negative L. pneumophila subpopulations reveals distinct proteomes with flagellar proteins or cell division proteins being preferentially produced by the former or the latter, respectively. Toward the end of an infection cycle (similar to 48 h), the P-flaA-GFP-positive L. pneumophila subpopulation emerges at the cluster periphery, predominantly escapes the LCV, and spreads from the bursting host cell. These processes are mediated by the Legionella quorum sensing (Lqs) system. Thus, quorum sensing regulates the emergence of a subpopulation of transmissive L. pneumophila at the LCV periphery, and phenotypic heterogeneity underlies the intravacuolar bi-phasic life cycle of L. pneumophila.
The Gram‐negative bacterium Legionella pneumophila is the causative agent of Legionnaires' disease and replicates in amoebae and macrophages within a distinct compartment, the Legionella‐containing vacuole (LCV). The facultative intracellular pathogen switches between a replicative, non‐virulent and a non‐replicating, virulent/transmissive phase. Here, we show on a single‐cell level that at late stages of infection, individual motile (PflaA‐GFP‐positive) and virulent (PralF‐ and PsidC‐GFP‐positive) L. pneumophila emerge in the cluster of non‐growing bacteria within an LCV. Comparative proteomics of PflaA‐GFP‐positive and PflaA‐GFP‐negative L. pneumophila subpopulations reveals distinct proteomes with flagellar proteins or cell division proteins being preferentially produced by the former or the latter, respectively. Toward the end of an infection cycle (˜ 48 h), the PflaA‐GFP‐positive L. pneumophila subpopulation emerges at the cluster periphery, predominantly escapes the LCV, and spreads from the bursting host cell. These processes are mediated by the Legionella quorum sensing (Lqs) system. Thus, quorum sensing regulates the emergence of a subpopulation of transmissive L. pneumophila at the LCV periphery, and phenotypic heterogeneity underlies the intravacuolar bi‐phasic life cycle of L. pneumophila. Synopsis Legionella forms a distinct vacuole in phagocytes, wherein the pathogen adopts a bi‐phasic life cycle and phenotypic heterogeneity. Quorum sensing elicits a transmissive subpopulation at the vacuole periphery, which spearheads compartment exit and host cell lysis. Legionella pneumophila switches between a replicative and a virulent/transmissive phase in its unique intracellular vacuole. The intravacuolar bi‐phasic life cycle displays phenotypic heterogeneity. Quorum sensing elicits a transmissive subpopulation at the vacuole periphery, promoting compartment exit and cell lysis. Legionella forms a distinct vacuole in phagocytes, wherein the pathogen adopts a bi‐phasic life cycle and phenotypic heterogeneity. Quorum sensing elicits a transmissive subpopulation at the vacuole periphery, which spearheads compartment exit and host cell lysis.
The Gram‐negative bacterium Legionella pneumophila is the causative agent of Legionnaires' disease and replicates in amoebae and macrophages within a distinct compartment, the Legionella‐containing vacuole (LCV). The facultative intracellular pathogen switches between a replicative, non‐virulent and a non‐replicating, virulent/transmissive phase. Here, we show on a single‐cell level that at late stages of infection, individual motile (PflaA‐GFP‐positive) and virulent (PralF‐ and PsidC‐GFP‐positive) L. pneumophila emerge in the cluster of non‐growing bacteria within an LCV. Comparative proteomics of PflaA‐GFP‐positive and PflaA‐GFP‐negative L. pneumophila subpopulations reveals distinct proteomes with flagellar proteins or cell division proteins being preferentially produced by the former or the latter, respectively. Toward the end of an infection cycle (˜ 48 h), the PflaA‐GFP‐positive L. pneumophila subpopulation emerges at the cluster periphery, predominantly escapes the LCV, and spreads from the bursting host cell. These processes are mediated by the Legionella quorum sensing (Lqs) system. Thus, quorum sensing regulates the emergence of a subpopulation of transmissive L. pneumophila at the LCV periphery, and phenotypic heterogeneity underlies the intravacuolar bi‐phasic life cycle of L. pneumophila.
The Gram‐negative bacterium Legionella pneumophila is the causative agent of Legionnaires' disease and replicates in amoebae and macrophages within a distinct compartment, the Legionella ‐containing vacuole (LCV). The facultative intracellular pathogen switches between a replicative, non‐virulent and a non‐replicating, virulent/transmissive phase. Here, we show on a single‐cell level that at late stages of infection, individual motile (P flaA ‐GFP‐positive) and virulent (P ralF ‐ and P sidC ‐GFP‐positive) L. pneumophila emerge in the cluster of non‐growing bacteria within an LCV. Comparative proteomics of P flaA ‐GFP‐positive and P flaA ‐GFP‐negative L. pneumophila subpopulations reveals distinct proteomes with flagellar proteins or cell division proteins being preferentially produced by the former or the latter, respectively. Toward the end of an infection cycle (˜ 48 h), the P flaA ‐GFP‐positive L. pneumophila subpopulation emerges at the cluster periphery, predominantly escapes the LCV, and spreads from the bursting host cell. These processes are mediated by the Legionella quorum sensing (Lqs) system. Thus, quorum sensing regulates the emergence of a subpopulation of transmissive L. pneumophila at the LCV periphery, and phenotypic heterogeneity underlies the intravacuolar bi‐phasic life cycle of L. pneumophila . Legionella forms a distinct vacuole in phagocytes, wherein the pathogen adopts a bi‐phasic life cycle and phenotypic heterogeneity. Quorum sensing elicits a transmissive subpopulation at the vacuole periphery, which spearheads compartment exit and host cell lysis.
The Gram-negative bacterium Legionella pneumophila is the causative agent of Legionnaires' disease and replicates in amoebae and macrophages within a distinct compartment, the Legionellacontaining vacuole (LCV). The facultative intracellular pathogen switches between a replicative, non-virulent and a non-replicating, virulent/transmissive phase. Here, we show on a single-cell level that at late stages of infection, individual motile (P flaA-GFPpositive) and virulent (P ralF-and P sidC-GFP-positive) L. pneumophila emerge in the cluster of non-growing bacteria within an LCV. Comparative proteomics of P flaA-GFP-positive and P flaA-GFPnegative L. pneumophila subpopulations reveals distinct proteomes with flagellar proteins or cell division proteins being preferentially produced by the former or the latter, respectively. Toward the end of an infection cycle (~48 h), the P flaA-GFP-positive L. pneumophila subpopulation emerges at the cluster periphery, predominantly escapes the LCV, and spreads from the bursting host cell. These processes are mediated by the Legionella quorum sensing (Lqs) system. Thus, quorum sensing regulates the emergence of a subpopulation of transmissive L. pneumophila at the LCV periphery, and phenotypic heterogeneity underlies the intravacuolar bi-phasic life cycle of L. pneumophila.
The Gram-negative bacterium Legionella pneumophila is the causative agent of Legionnaires' disease and replicates in amoebae and macrophages within a distinct compartment, the Legionella -containing vacuole (LCV). The facultative intracellular pathogen switches between a replicative, non-virulent and a non-replicating, virulent/transmissive phase. Here, we show on a single-cell level that at late stages of infection, individual motile (P flaA -GFP-positive) and virulent (P ralF - and P sidC -GFP-positive) L. pneumophila emerge in the cluster of non-growing bacteria within an LCV. Comparative proteomics of P flaA -GFP-positive and P flaA -GFP-negative L. pneumophila subpopulations reveals distinct proteomes with flagellar proteins or cell division proteins being preferentially produced by the former or the latter, respectively. Toward the end of an infection cycle (˜ 48 h), the P flaA -GFP-positive L. pneumophila subpopulation emerges at the cluster periphery, predominantly escapes the LCV, and spreads from the bursting host cell. These processes are mediated by the Legionella quorum sensing (Lqs) system. Thus, quorum sensing regulates the emergence of a subpopulation of transmissive L. pneumophila at the LCV periphery, and phenotypic heterogeneity underlies the intravacuolar bi-phasic life cycle of L. pneumophila . Synopsis Legionella forms a distinct vacuole in phagocytes, wherein the pathogen adopts a bi-phasic life cycle and phenotypic heterogeneity. Quorum sensing elicits a transmissive subpopulation at the vacuole periphery, which spearheads compartment exit and host cell lysis. Legionella pneumophila switches between a replicative and a virulent/transmissive phase in its unique intracellular vacuole. The intravacuolar bi-phasic life cycle displays phenotypic heterogeneity. Quorum sensing elicits a transmissive subpopulation at the vacuole periphery, promoting compartment exit and cell lysis. Graphical Abstract Legionella forms a distinct vacuole in phagocytes, wherein the pathogen adopts a bi-phasic life cycle and phenotypic heterogeneity. Quorum sensing elicits a transmissive subpopulation at the vacuole periphery, which spearheads compartment exit and host cell lysis.
Author Lanner, Ulrike
Ziegler, Urs
Brülisauer, Sabrina
Hilbi, Hubert
Striednig, Bianca
Personnic, Nicolas
Niggli, Selina
Kaech, Andres
Hochstrasser, Ramon
Flieger, Antje
Vormittag, Simone
Katic, Ana
Schmidt, Alexander
Welin, Amanda
AuthorAffiliation 2 Proteomics Core Facility Biozentrum University of Basel Basel Switzerland
3 Center for Microscopy and Image Analysis University of Zürich Zürich Switzerland
4 Division of Inflammation and Infection Department of Biomedical and Clinical Sciences Linköping University Linköping Sweden
1 Institute of Medical Microbiology University of Zürich Zürich Switzerland
5 Division of Enteropathogenic Bacteria and Legionella Robert Koch Institute Wernigerode Germany
6 Present address: Department of Quantitative Biomedicine University of Zürich Zürich Switzerland
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– name: 6 Present address: Department of Quantitative Biomedicine University of Zürich Zürich Switzerland
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– name: 1 Institute of Medical Microbiology University of Zürich Zürich Switzerland
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Issue 9
Keywords phenotypic heterogeneity
quorum sensing
flagellum
pathogen vacuole
proteome
Signal Transduction
Microbiology, Virology & Host Pathogen Interaction
flagellum pathogen vacuole phenotypic heterogeneity proteome quorum sensing Subject Categories Membranes & Trafficking Microbiology, Virology & Host Pathogen Interaction Signal Transduction
quorum sensing Subject Categories Membranes & Trafficking
Language English
License Attribution-NonCommercial-NoDerivs
Distributed under a Creative Commons Attribution 4.0 International License: http://creativecommons.org/licenses/by/4.0
This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc-nd/4.0/ License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non‐commercial and no modifications or adaptations are made.
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content type line 14
content type line 23
These authors contributed equally to this work
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Snippet The Gram-negative bacterium Legionella pneumophila is the causative agent of Legionnaires' disease and replicates in amoebae and macrophages within a distinct...
The Gram‐negative bacterium Legionella pneumophila is the causative agent of Legionnaires' disease and replicates in amoebae and macrophages within a distinct...
The Gram-negative bacterium Legionella pneumophila is the causative agent of Legionnaires' disease and replicates in amoebae and macrophages within a distinct...
The Gram‐negative bacterium Legionella pneumophila is the causative agent of Legionnaires' disease and replicates in amoebae and macrophages within a distinct...
The Gram-negative bacterium Legionella pneumophila is the causative agent of Legionnaires disease and replicates in amoebae and macrophages within a distinct...
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StartPage e52972
SubjectTerms Amoeba
Bacteria
Cell division
Clusters
EMBO20
EMBO23
EMBO37
Flagella
flagellum
Heterogeneity
Intracellular
Legionella
Legionella pneumophila
Legionnaire's disease
Legionnaires' disease
Legionnaires' disease bacterium
Life cycles
Life Sciences
Lysis
Macrophages
pathogen vacuole
Pathogens
Phagocytes
phenotypic heterogeneity
Proteins
proteome
Proteomes
Proteomics
Quorum sensing
Subpopulations
Switches
Virulence
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Title Quorum sensing governs a transmissive Legionella subpopulation at the pathogen vacuole periphery
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Volume 22
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