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The pleotropic Legionella transcription factor LvbR links the Lqs and c-di-GMP regulatory networks to control biofilm architecture and virulence


Hochstrasser, Ramon; Kessler, Aline; Sahr, Tobias; Simon, Sylvia; Schell, Ursula; Gomez-Valero, Laura; Buchrieser, Carmen; Hilbi, Hubert (2019). The pleotropic Legionella transcription factor LvbR links the Lqs and c-di-GMP regulatory networks to control biofilm architecture and virulence. Environmental Microbiology, 21(3):1035-1053.

Abstract

The causative agent of Legionnaires' pneumonia, Legionella pneumophila, colonizes amoebae and biofilms in the environment. The opportunistic pathogen employs the Lqs (Legionella quorum sensing) system and the signaling molecule LAI-1 (Legionella autoinducer-1) to regulate virulence, motility, natural competence, and expression of a 133 kb genomic island, including a putative novel regulator. Here, we show that the regulator termed LvbR is an LqsS-regulated, pleotropic transcription factor that binds to the promoter of lpg1056/hnox1 (encoding an inhibitor of the diguanylate cyclase Lpg1057), and thus regulates proteins involved in c-di-GMP metabolism. LvbR determines biofilm architecture, since L. pneumophila lacking lvbR accumulates less sessile biomass and forms homogeneous mat-like structures, while the parental strain develops more compact bacterial aggregates. Comparative transcriptomics of sessile and planktonic ΔlvbR or ΔlqsR mutant strains revealed concerted (virulence, fitness island, metabolism) and reciprocally (motility) regulated genes in biofilm and broth, respectively. Moreover, ΔlvbR is hyper-competent for DNA uptake, defective for phagocyte infection, outcompeted by the parental strain in amoebae co-infections, and impaired for cell migration inhibition. Taken together, our results indicate that L. pneumophila LvbR is a novel pleotropic transcription factor, which links the Lqs and c-di-GMP regulatory networks to control biofilm architecture and pathogen-host-cell interactions. This article is protected by copyright. All rights reserved.

Abstract

The causative agent of Legionnaires' pneumonia, Legionella pneumophila, colonizes amoebae and biofilms in the environment. The opportunistic pathogen employs the Lqs (Legionella quorum sensing) system and the signaling molecule LAI-1 (Legionella autoinducer-1) to regulate virulence, motility, natural competence, and expression of a 133 kb genomic island, including a putative novel regulator. Here, we show that the regulator termed LvbR is an LqsS-regulated, pleotropic transcription factor that binds to the promoter of lpg1056/hnox1 (encoding an inhibitor of the diguanylate cyclase Lpg1057), and thus regulates proteins involved in c-di-GMP metabolism. LvbR determines biofilm architecture, since L. pneumophila lacking lvbR accumulates less sessile biomass and forms homogeneous mat-like structures, while the parental strain develops more compact bacterial aggregates. Comparative transcriptomics of sessile and planktonic ΔlvbR or ΔlqsR mutant strains revealed concerted (virulence, fitness island, metabolism) and reciprocally (motility) regulated genes in biofilm and broth, respectively. Moreover, ΔlvbR is hyper-competent for DNA uptake, defective for phagocyte infection, outcompeted by the parental strain in amoebae co-infections, and impaired for cell migration inhibition. Taken together, our results indicate that L. pneumophila LvbR is a novel pleotropic transcription factor, which links the Lqs and c-di-GMP regulatory networks to control biofilm architecture and pathogen-host-cell interactions. This article is protected by copyright. All rights reserved.

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Additional indexing

Item Type:Journal Article, refereed, original work
Communities & Collections:04 Faculty of Medicine > Institute of Medical Microbiology
Dewey Decimal Classification:570 Life sciences; biology
610 Medicine & health
Scopus Subject Areas:Life Sciences > Microbiology
Life Sciences > Ecology, Evolution, Behavior and Systematics
Language:English
Date:1 March 2019
Deposited On:15 Mar 2019 13:40
Last Modified:29 Jul 2020 10:19
Publisher:Wiley-Blackwell Publishing, Inc.
ISSN:1462-2912
OA Status:Closed
Publisher DOI:https://doi.org/10.1111/1462-2920.14523
PubMed ID:30623561

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