Surface growth ofPseudomonas aeruginosareveals a regulatory effect of 3- oxo-C₁₂-homoserine lactone in absence of its cognate receptor, LasR

Abstract

Successful colonization of a multitude of ecological niches by the bacteriumPseudomonas aeruginosarelies on its ability to respond to concentrations of self-produced signal molecules. This intercellular communication system known as quorum sensing (QS) tightly regulates the expression of virulence determinants and a diversity of survival functions, including those required for social behaviours. In planktonic cultures ofP. aeruginosa, the transcriptional regulator LasR is generally considered on top of the QS circuitry hierarchy; its activation relies on binding to 3-oxo-C12-homoserine lactone (3-oxo-C12-HSL), a product of the LasI synthase. Transcription oflasIis activated by LasR, resulting in a positive feedback loop. Few studies have looked at the function of QS during surface growth even thoughP. aeruginosatypically lives in biofilm-like communities under natural conditions. Here, we show that surface-grownP. aeruginosareadily produces 3-oxo-C12-HSL in absence of LasR, and that this phenotype is frequent upon surface association in naturally occurring environmental and clinical LasR-defective isolates, suggesting a conserved alternative function for the signal. Indeed, even in the absence of the cognate regulator LasR, 3-oxo-C12-HSL upregulates the autologous expression of pyocyanin and of LasR-controlled virulence determinants in neighboring cells. This highlights a possible role for 3-oxo-C12-HSL in shaping community responses and provides a possible evolutive benefit for mixed populations to carry LasR-defective cells, a common feature of natural ofP. aeruginosa.