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The L egionella pneumophila orphan sensor kinase LqsT regulates competence and pathogen–host interactions as a component of the LAI ‐1 circuit
Author(s) -
Kessler Aline,
Schell Ursula,
Sahr Tobias,
Tiaden André,
Harrison Christopher,
Buchrieser Carmen,
Hilbi Hubert
Publication year - 2013
Publication title -
environmental microbiology
Language(s) - English
Resource type - Journals
SCImago Journal Rank - 1.954
H-Index - 188
eISSN - 1462-2920
pISSN - 1462-2912
DOI - 10.1111/j.1462-2920.2012.02889.x
Subject(s) - biology , quorum sensing , legionella pneumophila , effector , response regulator , mutant , gene , kinase , autoinducer , phenotype , genetics , microbiology and biotechnology , wild type , bacteria , virulence
Summary L egionella pneumophila is an amoeba‐resistant opportunistic pathogen that performs cell–cell communication through the signalling molecule 3‐hydroxypentadecane‐4‐one ( LAI ‐1, L egionella autoinducer‐1). The lqs ( L egionella 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 A canthamoeba castellanii revealed that Δ lqsT and Δ lqsS ‐Δ lqsT , as well as Δ 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 Δ lqsS strain, Δ lqsT does not produce extracellular filaments. The phenotypes of the Δ lqsS ‐Δ 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 Δ lqsT and Δ 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 pathogen–host cell interactions, competence, expression of a genomic island or production of extracellular filaments.