TheLegionella pneumophilaorphan sensor kinase LqsT regulates competence and pathogen–host interactions as a component of the LAI-1 circuit

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SummaryLegionella pneumophilais an amoeba-resistant opportunistic pathogen that performs cell–cell communication through the signalling molecule 3-hydroxypentadecane-4-one (LAI-1,Legionellaautoinducer-1). Thelqs(Legionellaquorum 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-typeL. pneumophila, strains lackinglqsTor bothlqsSandlqsTshow increased salt resistance, greatly enhanced natural competence for DNA acquisition and impaired uptake by phagocytes. Sensitive novel single round growth assays and competition experiments usingAcanthamoeba castellaniirevealed that ΔlqsTand ΔlqsSlqsT, as well as ΔlqsAand otherlqsmutant strains are impaired for intracellular growth and cannot compete against wild-type bacteria upon co-infection. In contrast to the ΔlqsSstrain, ΔlqsTdoes not produce extracellular filaments. The phenotypes of the ΔlqsSlqsTstrain are partially complemented by eitherlqsTorlqsS, but are not reversed by overexpression oflqsA, suggesting that LqsT and LqsS are the sole LAI-1-responsive sensor kinases inL. pneumophila. In agreement with the different phenotypes of the ΔlqsTand ΔlqsSstrains,lqsTandlqsSare differentially expressed in the post-exponential growth phase, and transcriptome studies indicated that 90% of the genes, which are downregulated in absence oflqsT, are upregulated in absence oflqsS. 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 theL. pneumophilaLqs system comprising two partially antagonistic LAI-1-responsive sensor kinases, LqsT and LqsS, which regulate distinct pools of genes implicated in pathogen–host cell interactions, competence, expression of a genomic island or production of extracellular filaments.

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