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The Distinct Quorum Sensing Hierarchy of las and rhl in Pseudomonas sp. M18

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Abstract

Pseudomonas sp. M18 is a rhizosphere isolate capable of producing two kinds of antifungal agents: phenazine-1-carboxylic acid (PCA) and pyoluteorin. Recently, the two well-studied quorum sensing (QS) systems of Pseudomonas aeruginosa, LasR/LasI and RhlR/RhlI, have also been identified in this strain. However, in this study, through the use of lacZ translational fusion expression analysis and acyl-homoserine lactone thin-layer chromatography (TLC) bioassays, we clearly display a more complex and distinctive hierarchy of the las and rhl QS systems in strain M18. In this QS cascade, expression of rhlI was negatively controlled by the LasR/LasI QS system. In contrast with lasI, which negatively regulated the rhlR induction, lasR exerted a positive influence on rhlR expression during the log-phase. This interrelationship indicated that the response regulators (LasR and RhlR) of the QS system are expressed independently of their cognate synthases (LasI and RhlI). Furthermore, the las system also modulated the timing and magnitude of the rhlI and rhlR maximal expression. In addition, our data imply that the lasR gene exerts its negative control on PCA production through modulation of rhlI expression. Thus, interactions between the two QS systems are strain specific.

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References

  1. Juhas M, Eberl L, Tummler B (2005) Quorum sensing: the power of cooperation in the world of Pseudomonas. Environ Microbiol 7:459–471

    Article  CAS  PubMed  Google Scholar 

  2. Latifi A, Winson MK, Foglino M, Bycroft BW, Stewart GS, Lazdunski A, Williams P (1995) Multiple homologues of LuxR and LuxI control expression of virulence determinants and secondary metabolites through quorum sensing in Pseudomonas aeruginosa PAO1. Mol Microbiol 17:333–343

    Article  CAS  PubMed  Google Scholar 

  3. Schuster M, Greenberg EP (2007) Early activation of quorum sensing in Pseudomonas aeruginosa reveals the architecture of a complex regulon. BMC Genomics 8:287

    Article  PubMed  Google Scholar 

  4. Whiteley M, Lee KM, Greenberg EP (1999) Identification of genes controlled by quorum sensing in Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 96:13904–13909

    Article  CAS  PubMed  Google Scholar 

  5. Pesci EC, Pearson JP, Seed PC, Iglewski BH (1997) Regulation of las and rhl quorum sensing in Pseudomonas aeruginosa. J Bacteriol 179:3127–3132

    CAS  PubMed  Google Scholar 

  6. Latifi A, Foglino M, Tanaka K, Williams P, Lazdunski A (1996) A hierarchical quorum-sensing cascade in Pseudomonas aeruginosa links the transcriptional activators LasR and RhIR (VsmR) to expression of the stationary-phase sigma factor RpoS. Mol Microbiol 21:1137–1146

    Article  CAS  PubMed  Google Scholar 

  7. Chen Y, Wang X, Huang X, Zhang X, Xu Y (2008) Las-like quorum-sensing system negatively regulates both pyoluteorin and phenazine-1-carboxylic acid production in Pseudomonas sp. M18. Sci China C Life Sci 51:174–181

    Article  CAS  PubMed  Google Scholar 

  8. Huang X, Yan A, Zhang X, Xu Y (2006) Identification and characterization of a putative ABC transporter PltHIJKN required for pyoluteorin production in Pseudomonas sp. M18. Gene 376:68–78

    Article  CAS  PubMed  Google Scholar 

  9. Huang X, Zhu D, Ge Y, Hu H, Zhang X, Xu Y (2004) Identification and characterization of pltZ, a gene involved in the repression of pyoluteorin biosynthesis in Pseudomonas sp. M18. FEMS Microbiol Lett 232:197–202

    Article  CAS  PubMed  Google Scholar 

  10. Yan A, Huang X, Liu H, Dong D, Zhang D, Zhang X, Xu Y (2007) An rhl-like quorum-sensing system negatively regulates pyoluteorin production in Pseudomonas sp. M18. Microbiology 153:16–28

    Article  CAS  PubMed  Google Scholar 

  11. Dekimpe V, Deziel E (2009) Revisiting the quorum-sensing hierarchy in Pseudomonas aeruginosa: the transcriptional regulator RhlR regulates LasR-specific factors. Microbiology 155:712–723

    Article  CAS  PubMed  Google Scholar 

  12. King EO, Ward MK, Raney DE (1954) Two simple media for the demonstration of pyocyanin and fluorescin. J Lab Clin Med 44:301–307

    CAS  PubMed  Google Scholar 

  13. Levitch ME, Stadtman ER (1964) A study of the biosynthesis of phenazine-1-carboxylic acid. Arch Biochem Biophys 106:194–199

    Article  CAS  PubMed  Google Scholar 

  14. McClean KH, Winson MK, Fish L, Taylor A, Chhabra SR, Camara M, Daykin M, Lamb JH, Swift S, Bycroft BW, Stewart GS, Williams P (1997) Quorum sensing and Chromobacterium violaceum: exploitation of violacein production and inhibition for the detection of N-acylhomoserine lactones. Microbiology 143:3703–3711

    Article  CAS  PubMed  Google Scholar 

  15. Shaw PD, Ping G, Daly SL, Cha C, Cronan JE Jr, Rinehart KL, Farrand SK (1997) Detecting and characterizing N-acyl-homoserine lactone signal molecules by thin-layer chromatography. Proc Natl Acad Sci U S A 94:6036–6041

    Article  CAS  PubMed  Google Scholar 

  16. Duan K, Surette MG (2007) Environmental regulation of Pseudomonas aeruginosa PAO1 Las and Rhl quorum-sensing systems. J Bacteriol 189:4827–4836

    Article  CAS  PubMed  Google Scholar 

  17. Sandoz KM, Mitzimberg SM, Schuster M (2007) Social cheating in Pseudomonas aeruginosa quorum sensing. Proc Natl Acad Sci U S A 104:15876–15881

    Article  CAS  PubMed  Google Scholar 

  18. Kaufmann GF, Sartorio R, Lee SH, Rogers CJ, Meijler MM, Moss JA, Clapham B, Brogan AP, Dickerson TJ, Janda KD (2005) Revisiting quorum sensing: discovery of additional chemical and biological functions for 3-oxo-N-acylhomoserine lactones. Proc Natl Acad Sci U S A 102:309–314

    Article  CAS  PubMed  Google Scholar 

  19. Qazi S, Middleton B, Muharram SH, Cockayne A, Hill P, O’Shea P, Chhabra SR, Camara M, Williams P (2006) N-acylhomoserine lactones antagonize virulence gene expression and quorum sensing in Staphylococcus aureus. Infect Immun 74:910–919

    Article  CAS  PubMed  Google Scholar 

  20. Shiner EK, Terentyev D, Bryan A, Sennoune S, Martinez-Zaguilan R, Li G, Gyorke S, Williams SC, Rumbaugh KP (2006) Pseudomonas aeruginosa autoinducer modulates host cell responses through calcium signalling. Cell Microbiol 8:1601–1610

    Article  CAS  PubMed  Google Scholar 

  21. Zhu H, Conibear TC, Thuruthyil SJ, Willcox MD (2008) Pseudomonas aeruginosa quorum-sensing signal molecules induce IL-8 production by human corneal epithelial cells. Eye Contact Lens 34:179–181

    Article  PubMed  Google Scholar 

  22. Williams P (2007) Quorum sensing, communication and cross-kingdom signalling in the bacterial world. Microbiology 153:3923–3938

    Article  CAS  PubMed  Google Scholar 

  23. Medina G, Juarez K, Valderrama B, Soberon-Chavez G (2003) Mechanism of Pseudomonas aeruginosa RhlR transcriptional regulation of the rhlAB promoter. J Bacteriol 185:5976–5983

    Article  CAS  PubMed  Google Scholar 

  24. Ledgham F, Ventre I, Soscia C, Foglino M, Sturgis JN, Lazdunski A (2003) Interactions of the quorum sensing regulator QscR: interaction with itself and the other regulators of Pseudomonas aeruginosa LasR and RhlR. Mol Microbiol 48:199–210

    Article  CAS  PubMed  Google Scholar 

  25. Lee JH, Lequette Y, Greenberg EP (2006) Activity of purified QscR, a Pseudomonas aeruginosa orphan quorum-sensing transcription factor. Mol Microbiol 59:602–609

    Article  CAS  PubMed  Google Scholar 

  26. Lequette Y, Lee JH, Ledgham F, Lazdunski A, Greenberg EP (2006) A distinct QscR regulon in the Pseudomonas aeruginosa quorum-sensing circuit. J Bacteriol 188:3365–3370

    Article  CAS  PubMed  Google Scholar 

  27. Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY

    Google Scholar 

  28. Heeb S, Blumer C, Haas D (2002) Regulatory RNA as mediator in GacA/RsmA-dependent global control of exoproduct formation in Pseudomonas fluorescens CHA0. J Bacteriol 184:1046–1056

    Article  CAS  PubMed  Google Scholar 

  29. Huang X, Zhang X, Xu Y (2008) Positive regulation of pyoluteorin biosynthesis in Pseudomonas sp. M18 by quorum-sensing regulator VqsR. J Microbiol Biotechnol 18:828–836

    CAS  PubMed  Google Scholar 

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Acknowledgments

This study was supported by the Hi-Tech Research and Development Program (863 Program) of China (No. 2007AA02Z215), the National Natural Science Foundation of China (No. 30800009), the National Key Basic Research Program (973 Program) of China (No. 2009CB118906), and the Key Project of the Shanghai Committee of Science and Technology (No. 08391911900). We are very grateful to the referees and editor for their helpful and valuable suggestions and revisions.

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  1. College of Life Science and Biotechnology, Shanghai Jiao Tong University, 800 Dongchuan Road, Shanghai, 200240, People’s Republic of China

    Jishun Lu, Xianqing Huang, Mingyue Zhang, Sainan Li, Haixia Jiang & Yuquan Xu

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  1. Jishun Lu
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  2. Xianqing Huang
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Correspondence to Xianqing Huang or Yuquan Xu.

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Lu, J., Huang, X., Zhang, M. et al. The Distinct Quorum Sensing Hierarchy of las and rhl in Pseudomonas sp. M18. Curr Microbiol 59, 621–627 (2009). https://doi.org/10.1007/s00284-009-9483-y

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  • DOI: https://doi.org/10.1007/s00284-009-9483-y

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