Journal
ENVIRONMENTAL MICROBIOLOGY
Volume 15, Issue 2, Pages 646-662Publisher
WILEY
DOI: 10.1111/j.1462-2920.2012.02889.x
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Funding
- Max von Pettenkofer Institute, Ludwig-Maximilians University Munich
- German Research Foundation (DFG) [HI 1511/2-1, SPP 1617]
- Swiss National Science Foundation (SNF) [31003A_125369 Sinergia, CRSI33_130016]
- Institut Pasteur
- LabEx program IBEID
- Centre National de la Recherche Scientifique (CNRS)
- Institut Carnot-Pasteur MI
- Fondation pour la Recherche Medicale (FRM)
- French region Ile-de-France (DIM Malinf)
- ERA-Net PathoGenoMics [ANR-10-PATH-004]
- Swiss National Science Foundation (SNF) [CRSI33_130016] Funding Source: Swiss National Science Foundation (SNF)
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Legionella pneumophila is an amoeba-resistant opportunistic pathogen that performs cellcell communication through the signalling molecule 3-hydroxypentadecane-4-one (LAI-1, Legionella autoinducer-1). The lqs (Legionella quorum sensing) gene cluster encodes the LAI-1 autoinducer synthase LqsA, the cognate sensor kinase LqsS and the response regulator LqsR. Here we show that the Lqs system includes an orphan homologue of LqsS termed LqsT. Compared with wild-type L.?pneumophila, strains lacking lqsT or both lqsS and lqsT show increased salt resistance, greatly enhanced natural competence for DNA acquisition and impaired uptake by phagocytes. Sensitive novel single round growth assays and competition experiments using Acanthamoeba castellanii revealed that ?lqsT and ?lqsS-?lqsT, as well as ?lqsA and other lqs mutant strains are impaired for intracellular growth and cannot compete against wild-type bacteria upon co-infection. In contrast to the ?lqsS strain, ?lqsT does not produce extracellular filaments. The phenotypes of the ?lqsS-?lqsT strain are partially complemented by either lqsT or lqsS, but are not reversed by overexpression of lqsA, suggesting that LqsT and LqsS are the sole LAI-1-responsive sensor kinases in L.?pneumophila. In agreement with the different phenotypes of the ?lqsT and ?lqsS strains, lqsT and lqsS are differentially expressed in the post-exponential growth phase, and transcriptome studies indicated that 90% of the genes, which are downregulated in absence of lqsT, are upregulated in absence of lqsS. Reciprocally regulated genes encode components of a 133?kb genomic fitness island or translocated effector proteins implicated in virulence. Together, these results reveal a unique organization of the L.?pneumophila Lqs system comprising two partially antagonistic LAI-1-responsive sensor kinases, LqsT and LqsS, which regulate distinct pools of genes implicated in pathogenhost cell interactions, competence, expression of a genomic island or production of extracellular filaments.
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