AUTHOR=Barbey Corinne , Chane Andrea , Burini Jean-François , Maillot Olivier , Merieau Annabelle , Gallique Mathias , Beury-Cirou Amélie , Konto-Ghiorghi Yoan , Feuilloley Marc , Gobert Virginie , Latour Xavier 

TITLE=A Rhodococcal Transcriptional Regulatory Mechanism Detects the Common Lactone Ring of AHL Quorum-Sensing Signals and Triggers the Quorum-Quenching Response

JOURNAL=Frontiers in Microbiology

VOLUME=9

YEAR=2018

URL=https://www.frontiersin.org/journals/microbiology/articles/10.3389/fmicb.2018.02800

DOI=10.3389/fmicb.2018.02800

ISSN=1664-302X

ABSTRACT=<p>The biocontrol agent <italic>Rhodococcus erythropolis</italic> disrupts virulence of plant and human Gram-negative pathogens by catabolizing their <italic>N</italic>-acyl-homoserine lactones. This quorum-quenching activity requires the expression of the <italic>qsd</italic> (<underline>q</underline>uorum-sensing <underline>s</underline>ignal <underline>d</underline>egradation) operon, which encodes the lactonase QsdA and the fatty acyl-CoA ligase QsdC, involved in the catabolism of lactone ring and acyl chain moieties of signaling molecules, respectively. Here, we demonstrate the regulation of <italic>qsd</italic> operon expression by a TetR-like family repressor, QsdR. This repression was lifted by adding the pathogen quorum signal or by deleting the <italic>qsdR</italic> gene, resulting in enhanced lactone degrading activity. Using interactomic approaches and transcriptional fusion strategy, the <italic>qsd</italic> operon derepression was elucidated: it is operated by the binding of the common part of signaling molecules, the homoserine lactone ring, to the effector-receiving domain of QsdR, preventing a physical binding of QsdR to the <italic>qsd</italic> promoter region. To our knowledge, this is the first evidence revealing quorum signals as inducers of the suitable quorum-quenching pathway, confirming this TetR-like protein as a lactone sensor. This regulatory mechanism designates the <italic>qsd</italic> operon as encoding a global disrupting pathway for degrading a wide range of signal substrates, allowing a broad spectrum anti-virulence activity mediated by the rhodococcal biocontrol agent. Understanding the regulation mechanisms of <italic>qsd</italic> operon expression led also to the development of biosensors useful to monitor <italic>in situ</italic> the presence of exogenous signals and quorum-quenching activity.</p>