The α-hydroxyketone LAI-1 regulates motility, Lqs-dependent phosphorylation signalling and gene expression ofLegionella pneumophila

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Abstract

Summary

The causative agent of Legionnaires' disease,Legionella pneumophila, employs the autoinducer compound LAI-1 (3-hydroxypentadecane-4-one) for cell–cell communication. LAI-1 is produced and detected by the Lqs (Legionellaquorum sensing) system, comprising the autoinducer synthase LqsA, the sensor kinases LqsS and LqsT, as well as the response regulator LqsR. Lqs-regulated processes include pathogen–host interactions, production of extracellular filaments and natural competence for DNA uptake. Here we show that synthetic LAI-1 promotes the motility ofL. pneumophilaby signalling through LqsS/LqsT and LqsR. Upon addition of LAI-1, autophosphorylation of LqsS/LqsT by [γ-32P]-ATP was inhibited in a dose-dependent manner. In contrast, theVibrio choleraeautoinducer CAI-1 (3-hydroxytridecane-4-one) promoted the phosphorylation of LqsS (but not LqsT). LAI-1 did neither affect the stability of phospho-LqsS or phospho-LqsT, nor the dephosphorylation by LqsR. Transcriptome analysis ofL. pneumophilatreated with LAI-1 revealed that the compound positively regulates a number of genes, including the non-coding RNAsrsmYandrsmZ, and negatively regulates the RNA-binding global regulatorcrsA. Accordingly, LAI-1 controls the switch from the replicative to the transmissive growth phase ofL. pneumophila. In summary, the findings indicate that LAI-1 regulates motility and the biphasic life style ofL. pneumophilathrough LqsS- and LqsT-dependent phosphorylation signalling.

The environmental bacterium Legionella pneumophila causes a severe pneumonia termed Legionnaires′ disease. For cell-to-cell communication, the pathogen uses the small signaling molecule LAI-1, which is produced and detected by the Lqs (Legionella quorum sensing) system. We show that synthetic LAI-1 is recognized by the membrane-bound sensor kinases LqsS and LqsT, which transfer the phosphorylation signal to the response regulator LqsR. Thus, LAI-1 regulates gene expression and motility of L. pneumophila through Lqs-dependent signal transduction.

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