Abstract
Species from the Burkholderia cepacia complex (Bcc) share a canonical LuxI/LuxR quorum sensing (QS) regulation system named CepI/CepR, which mainly relies on the acyl-homoserine lactone (AHL), octanoyl-homoserine lactone (C8-HSL) as signaling molecule. Burkholderia ambifaria is one of the least virulent Bcc species, more often isolated from rhizospheres where it exerts a plant growth-promoting activity. However, clinical strains of B. ambifaria display distinct features, such as phase variation and higher virulence properties. Notably, we previously reported that under laboratory conditions, only clinical strains of the B. ambifaria species produced 4-hydroxy-3-methyl-2-alkylquinolines (HMAQs) via expression of the hmqABCDEFG operon. HMAQs are the methylated counterparts of the 4-hydroxy-2-alkylquinolines (HAQs) produced by the opportunistic human pathogen Pseudomonas aeruginosa, in which they globally contribute to the bacterial virulence and survival. We have found that unlike P. aeruginosa’s HAQs, HMAQs do not induce their own production. However, they indirectly regulate the expression of the hmqABCDEFG operon. In B. ambifaria, a strong link between CepI/CepR-based QS and HMAQs is proposed, as we have previously reported an increased production of C8-HSL in HMAQ-negative mutants. Here, we report the identification of all AHLs produced by the clinical B. ambifaria strain HSJ1, namely C6-HSL, C8-HSL, C10-HSL, 3OHC8-HSL, 3OHC10-HSL, and 3OHC12-HSL. Production of significant levels of hydroxylated AHLs prompted the identification of a second complete LuxI/LuxR-type QS system relying on 3OHC10-HSL and 3OHC12-HSL, that we have named CepI2/CepR2. The connection between these two QS systems and the hmqABCDEFG operon, responsible for HMAQs biosynthesis, was investigated. The CepI/CepR system strongly induced the operon, while the second system appears moderately involved. On the other hand, a HMAQ-negative mutant overproduces AHLs from both QS systems. Even if HMAQs are not classical QS signals, their effect on AHL-based QS system still gives them a part to play in the QS circuitry in B. ambifaria and thus, on regulation of various phenotypes.
Highlights
Cell–cell communication in bacteria occurs via the production of signal molecules that are released and captured in the microenvironment
The pqsABCDE operon is directly and indirectly influenced by the two acyl-homoserine lactone (AHL)-based quorum sensing (QS) systems, but is positively autoinduced via the binding of HHQ or PQS ligands to the LysR-type regulator MvfR (PqsR) (McGrath et al, 2004; Xiao et al, 2006). While no such regulator has yet been identified for B. ambifaria (Vial et al, 2008), we investigated whether HMAQ-C7:2 induces the transcription of the hmqABCDEFG operon in strain HSJ1
We have identified a second LuxIR-type QS system in the HSJ1 strain, and we have characterized AHLs produced by each synthase
Summary
Cell–cell communication in bacteria occurs via the production of signal molecules that are released and captured in the microenvironment. When the bacterial population grows, the local concentration of signals increases, until it reaches a threshold able to trigger regulatory cascades This communication based on the census of the population is named quorum sensing (QS) and it allows the coordination of collective behaviors such as the production of virulence factors or biofilm formation (Fuqua and Winans, 1994; Williams, 2007). The QS circuitry of this bacterium is composed of two LuxI/LuxRtype systems, named LasI/LasR and RhlI/RhlR Besides these two QS systems based on signal molecules belonging to the AHL family, P. aeruginosa possesses a third QS system relying on 4-hydroxy-2-alkylquinolines (HAQs) molecules. The three QS systems in P. aeruginosa are hierarchically organized but intertwined; for example, the two AHL-based systems directly or indirectly induce the pqsABCDE operon, required for HAQ production, while some HAQs autoinduce their own biosynthesis but do not influence the production of AHLs (Déziel et al, 2005)
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