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Cis-2-dodecenoic acid signal modulates virulence of Pseudomonas aeruginosa through interference with quorum sensing systems and T3SS.

Deng Y, Boon C, Chen S, Lim A, Zhang LH - BMC Microbiol. (2013)

Bottom Line: Furthermore, BDSF and some of its derivatives are also capable of inhibiting T3SS of P. aeruginosa at a micromolar level.Treatment with BDSF obviously reduced the virulence of P. aeruginosa in both HeLa cell and zebrafish infection models.These results depict that BDSF modulates virulence of P. aeruginosa through interference with QS systems and T3SS.

View Article: PubMed Central - HTML - PubMed

Affiliation: Institute of Molecular and Cell Biology, Proteos, 61 Biopolis Drive, Singapore, 138673, Singapore. ydeng@imcb.a-star.edu.sg.

ABSTRACT

Background: Cis-2-dodecenoic acid (BDSF) is well known for its important functions in intraspecies signaling in Burkholderia cenocepacia. Previous work has also established an important role of BDSF in interspecies and inter-kingdom communications. It was identified that BDSF modulates virulence of Pseudomonas aeruginosa. However, how BDSF interferes with virulence of P. aeruginosa is still not clear.

Results: We report here that BDSF mediates the cross-talk between B. cenocepacia and P. aeruginosa through interference with quorum sensing (QS) systems and type III secretion system (T3SS) of P. aeruginosa. Bioassay results revealed that exogenous addition of BDSF not only reduced the transcriptional expression of the regulator encoding gene of QS systems, i.e., lasR, pqsR, and rhlR, but also simultaneously decreased the production of QS signals including 3-oxo-C12-HSL, Pseudomonas quinolone signal (PQS) and C4-HSL, consequently resulting in the down-regulation of biofilm formation and virulence factor production of P. aeruginosa. Furthermore, BDSF and some of its derivatives are also capable of inhibiting T3SS of P. aeruginosa at a micromolar level. Treatment with BDSF obviously reduced the virulence of P. aeruginosa in both HeLa cell and zebrafish infection models.

Conclusions: These results depict that BDSF modulates virulence of P. aeruginosa through interference with QS systems and T3SS.

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Related in: MedlinePlus

Influence of BDSF on QS systems of P. aeruginosa. Effect of BDSF on the growth rate of P. aeruginosa PA14 (A), and on the transcriptional expression of lasR(B), pqsR(C), and rhlR(D), as determined by using corresponding promoter-lacZ fusion reporter strains. The data are the means of three repeats and error bars indicate the standard deviations.
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Figure 1: Influence of BDSF on QS systems of P. aeruginosa. Effect of BDSF on the growth rate of P. aeruginosa PA14 (A), and on the transcriptional expression of lasR(B), pqsR(C), and rhlR(D), as determined by using corresponding promoter-lacZ fusion reporter strains. The data are the means of three repeats and error bars indicate the standard deviations.

Mentions: It was found that there is a regulatory interaction between the different type QS systems, BDSF and AHL systems in B. cenocepacia[39,40]. Disruption of both BDSF synthase and receptor caused a substantial down-regulation of AHL signals production and AHL synthase gene expression in B. cenocepacia. Given the fact that B. cenocepacia and P. aeruginosa share the same niche in cystic fibrosis patent, we then hypothesized that BDSF may play a regulatory role in the QS systems of P. aeruginosa. To determine the influences of BDSF on the QS systems of P. aeruginosa, the promoter-lacZ fusion reporters were constructed to test the transcriptional expression of the regulator encoding gene of QS systems, i.e., lasR, pqsR and rhlR, in the absence and presence of BDSF. It was shown that exogenous addition of BDSF did not obviously affect the bacterial growth of P. aeruginosa PA14 (Figure 1A). But the transcriptional expressions of lasR, pqsR and rhlR were repressed by treatment with BDSF in a dosage-dependent manner. Addition of 0.25 mM BDSF resulted in 38%, 35% and 48% reduction of the expression of lasR, pqsR and rhlR, respectively (Figure 1B-D). To further investigate BDSF effect on the QS signal production of P. aeruginosa PA14, production of 3-oxo-C12-HSL, PQS, and C4-HSL were tested in the absence and presence of BDSF. Consistently, it was revealed that treatment with BDSF decreased the production of 3-oxo-C12-HSL, PQS and C4-HSL. As shown in Additional file 1: Figure S1, addition of BDSF slightly decreased the production of 3-oxo-C12-HSL; while obviously inhibited the production of PQS and C4-HSL.


Cis-2-dodecenoic acid signal modulates virulence of Pseudomonas aeruginosa through interference with quorum sensing systems and T3SS.

Deng Y, Boon C, Chen S, Lim A, Zhang LH - BMC Microbiol. (2013)

Influence of BDSF on QS systems of P. aeruginosa. Effect of BDSF on the growth rate of P. aeruginosa PA14 (A), and on the transcriptional expression of lasR(B), pqsR(C), and rhlR(D), as determined by using corresponding promoter-lacZ fusion reporter strains. The data are the means of three repeats and error bars indicate the standard deviations.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4016476&req=5

Figure 1: Influence of BDSF on QS systems of P. aeruginosa. Effect of BDSF on the growth rate of P. aeruginosa PA14 (A), and on the transcriptional expression of lasR(B), pqsR(C), and rhlR(D), as determined by using corresponding promoter-lacZ fusion reporter strains. The data are the means of three repeats and error bars indicate the standard deviations.
Mentions: It was found that there is a regulatory interaction between the different type QS systems, BDSF and AHL systems in B. cenocepacia[39,40]. Disruption of both BDSF synthase and receptor caused a substantial down-regulation of AHL signals production and AHL synthase gene expression in B. cenocepacia. Given the fact that B. cenocepacia and P. aeruginosa share the same niche in cystic fibrosis patent, we then hypothesized that BDSF may play a regulatory role in the QS systems of P. aeruginosa. To determine the influences of BDSF on the QS systems of P. aeruginosa, the promoter-lacZ fusion reporters were constructed to test the transcriptional expression of the regulator encoding gene of QS systems, i.e., lasR, pqsR and rhlR, in the absence and presence of BDSF. It was shown that exogenous addition of BDSF did not obviously affect the bacterial growth of P. aeruginosa PA14 (Figure 1A). But the transcriptional expressions of lasR, pqsR and rhlR were repressed by treatment with BDSF in a dosage-dependent manner. Addition of 0.25 mM BDSF resulted in 38%, 35% and 48% reduction of the expression of lasR, pqsR and rhlR, respectively (Figure 1B-D). To further investigate BDSF effect on the QS signal production of P. aeruginosa PA14, production of 3-oxo-C12-HSL, PQS, and C4-HSL were tested in the absence and presence of BDSF. Consistently, it was revealed that treatment with BDSF decreased the production of 3-oxo-C12-HSL, PQS and C4-HSL. As shown in Additional file 1: Figure S1, addition of BDSF slightly decreased the production of 3-oxo-C12-HSL; while obviously inhibited the production of PQS and C4-HSL.

Bottom Line: Furthermore, BDSF and some of its derivatives are also capable of inhibiting T3SS of P. aeruginosa at a micromolar level.Treatment with BDSF obviously reduced the virulence of P. aeruginosa in both HeLa cell and zebrafish infection models.These results depict that BDSF modulates virulence of P. aeruginosa through interference with QS systems and T3SS.

View Article: PubMed Central - HTML - PubMed

Affiliation: Institute of Molecular and Cell Biology, Proteos, 61 Biopolis Drive, Singapore, 138673, Singapore. ydeng@imcb.a-star.edu.sg.

ABSTRACT

Background: Cis-2-dodecenoic acid (BDSF) is well known for its important functions in intraspecies signaling in Burkholderia cenocepacia. Previous work has also established an important role of BDSF in interspecies and inter-kingdom communications. It was identified that BDSF modulates virulence of Pseudomonas aeruginosa. However, how BDSF interferes with virulence of P. aeruginosa is still not clear.

Results: We report here that BDSF mediates the cross-talk between B. cenocepacia and P. aeruginosa through interference with quorum sensing (QS) systems and type III secretion system (T3SS) of P. aeruginosa. Bioassay results revealed that exogenous addition of BDSF not only reduced the transcriptional expression of the regulator encoding gene of QS systems, i.e., lasR, pqsR, and rhlR, but also simultaneously decreased the production of QS signals including 3-oxo-C12-HSL, Pseudomonas quinolone signal (PQS) and C4-HSL, consequently resulting in the down-regulation of biofilm formation and virulence factor production of P. aeruginosa. Furthermore, BDSF and some of its derivatives are also capable of inhibiting T3SS of P. aeruginosa at a micromolar level. Treatment with BDSF obviously reduced the virulence of P. aeruginosa in both HeLa cell and zebrafish infection models.

Conclusions: These results depict that BDSF modulates virulence of P. aeruginosa through interference with QS systems and T3SS.

Show MeSH
Related in: MedlinePlus