Skip to main content
SpringerLink
Log in

Lichen secondary metabolite evernic acid as potential quorum sensing inhibitor against Pseudomonas aeruginosa

  • Original Paper
  • Published:
World Journal of Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Cystic Fibrosis is a genetic disease and it affects the respiratory and digestive systems. Pseudomonas aeruginosa infections in Cystic Fibrosis are presented as the main cause for high mortality and morbidity rates. Pseudomonas aeruginosa populations can regulate their virulence gene expressions via the bacterial communication system: quorum sensing. Inhibition of quorum sensing by employing quorum sensing inhibitors can leave the bacteria vulnerable. Therefore, determining natural sources to obtain potential quorum sensing inhibitors is essential. Lichens have ethnobotanical value for their medicinal properties and it is possible that their secondary metabolites have quorum sensing inhibitor properties. This study aims to investigate an alternative treatment approach by utilizing lichen secondary metabolite evernic acid to reduce the expressions of Pseudomonas aeruginosa virulence factors by inhibiting quorum sensing. For this purpose, fluorescent monitor strains were utilized for quorum sensing inhibitor screens and quantitative reverse-transcriptase PCR analyses were conducted for comparison. Results indicate that evernic acid is capable of inhibiting Pseudomonas aeruginosa quorum sensing systems.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Acikgoz B, Karalti I, Ersoz M, Coskun ZM, Cobanoglu G, Sesal C (2013) Screening of antimicrobial activity and cytotoxic effects of two Cladonia species. Z Naturforsch C 68:191–197

    Article  CAS  Google Scholar 

  • Al-Ani I, Zimmermann S, Reichling J, Wink M (2015) Pharmacological synergism of bee venom and melittin with antibiotics and plant secondary metabolites against multi-drug resistant microbial pathogens. Phytomedicine 22:245–255. doi:10.1016/j.phymed.2014.11.019

    Article  CAS  Google Scholar 

  • Azimi H, Khakshur AA, Aghdasi I, Fallah-Tafti M, Abdollahi M (2012) A review of animal and human studies for management of benign prostatic hyperplasia with natural products: perspective of new pharmacological agents. Inflamm Allergy Drug Targets 11:207–221

    Article  CAS  Google Scholar 

  • Basile A et al (2015) Antiproliferative, antibacterial and antifungal activity of the lichen Xanthoria parietina and its secondary metabolite parietin. Int J Mol Sci 16:7861–7875

    Article  CAS  Google Scholar 

  • Bassler B (2015) Manipulating quorum sensing to control bacterial pathogenicity. FASEB J 29(Suppl 1):88-1

    Google Scholar 

  • Bhattarai HD, Paudel B, Hong SG, Lee HK, Yim JH (2008) Thin layer chromatography analysis of antioxidant constituents of lichens from Antarctica. J Nat Med 62:481–484

    Article  Google Scholar 

  • Bjarnsholt T, van Gennip M, Jakobsen TH, Christensen LD, Jensen PO, Givskov M (2010) In vitro screens for quorum sensing inhibitors and in vivo confirmation of their effect. Nat Protoc 5:282–293. doi:10.1038/nprot.2009.205

    Article  CAS  Google Scholar 

  • Boor KJ (2006) Bacterial stress responses: what doesn’t kill them can make them stronger. PLoS Biol 4:18–20. doi:10.1371/journal.pbio.0040023

    Article  CAS  Google Scholar 

  • Brackman G, Coenye T (2015) Quorum sensing ınhibitors as anti-biofilm agents. Curr Pharm Des 21:5–11

    Article  CAS  Google Scholar 

  • Caldas RR, Boisrame S (2015) Upper aero-digestive contamination by Pseudomonas aeruginosa and implications in Cystic Fibrosis. J Cystic Fibros 14:6–15. doi:10.1016/j.jcf.2014.04.008

    Article  Google Scholar 

  • De Kievit T (2009) Quorum sensing in Pseudomonas aeruginosa biofilms. Environ Microbiol 11:279–288

    Article  Google Scholar 

  • Deduke C, Timsina B, Piercey-Normore MD (2012) Effect of environmental change on secondary metabolite production in lichen-forming fungi. In: Young S (ed) International perspectives on global environmental change. InTech, Rejika, Croatia

    Google Scholar 

  • Diggle SP, Winzer K, Chhabra SR, Chhabra SR, Worrall KE, Camara M, Williams P (2003) The Pseudomonas aeruginosa quinolone signal molecule overcomes the cell density-dependency of the quorum sensing hierarchy, regulates rhl-dependent genes at the onset of stationary phase and can be produced in the absence of LasR. Mol Microbiol 50:29–43. doi:10.1046/j.1365-2958.2003.03672.x

    Article  CAS  Google Scholar 

  • Fernandez-Moriano C, Gomez-Serranillos MP, Crespo A (2016) Antioxidant potential of lichen species and their secondary metabolites. A systematic review. Pharm Biol 54:1–17. doi:10.3109/13880209.2014.1003354

    Article  CAS  Google Scholar 

  • Fux CA, Costerton JW, Stewart PS, Stoodley P (2005) Survival strategies of infectious biofilms. Trends Microbiol 13:34–40. doi:10.1016/j.tim.2004.11.010

    Article  CAS  Google Scholar 

  • Girard G, Bloemberg GV (2008) Central role of quorum sensing in regulating the production of pathogenicity factors in Pseudomonas aeruginosa. Future Microbiol 3:97–106. doi:10.2217/17460913.3.1.97

    Article  CAS  Google Scholar 

  • Hentzer M et al (2002) Inhibition of quorum sensing in Pseudomonas aeruginosa biofilm bacteria by a halogenated furanone compound. Microbiology-Sgm 148:87–102

    Article  CAS  Google Scholar 

  • Hentzer M, Eberl L, Nielsen J, Givskov M (2003a) Quorum sensing—a novel target for the treatment of biofilm infections. Biodrugs 17:241–250. doi:10.2165/00063030-200317040-00003

    Article  CAS  Google Scholar 

  • Hentzer M et al (2003b) Attenuation of Pseudomonas aeruginosa virulence by quorum sensing inhibitors. EMBO J 22:3803–3815. doi:10.1093/emboj/cdg366

    Article  CAS  Google Scholar 

  • Holloway BW, Morgan AF (1986) Genome organization in Pseudomonas. Annu Rev Microbiol 40:79–105. doi:10.1146/annurev.micro.40.1.79

    Article  CAS  Google Scholar 

  • Jakobsen TH et al (2012) Food as a source for quorum sensing inhibitors: iberin from horseradish revealed as a quorum sensing inhibitor of Pseudomonas aeruginosa. Appl Environ Microbiol 78:2410–2421. doi:10.1128/Aem.05992-11

    Article  CAS  Google Scholar 

  • Jakobsen TH, Bjarnsholt T, Jensen PO, Givskov M, Hoiby N (2013) Targeting quorum sensing in Pseudomonas aeruginosa biofilms: current and emerging inhibitors. Future Microbiol 8:901–921. doi:10.2217/fmb.13.57

    Article  CAS  Google Scholar 

  • Jones RN, Stilwell MG, Rhomberg PR, Sader HS (2009) Antipseudomonal activity of piperacillin/tazobactam: more than a decade of experience from the SENTRY Antimicrobial Surveillance Program (1997–2007). Diagn Microbiol Infect Dis 65:331–334. doi:10.1016/j.diagmicrobio.2009.06.022

    Article  CAS  Google Scholar 

  • Lambert ML et al (2011) Clinical outcomes of health-care-associated infections and antimicrobial resistance in patients admitted to European intensive-care units: a cohort study. Lancet Infect Dis 11:30–38. doi:10.1016/S1473-3099(10)70258-9

    Article  Google Scholar 

  • Lee J, Zhang L (2015) The hierarchy quorum sensing network in Pseudomonas aeruginosa. Protein Cell 6:26–41

    Article  CAS  Google Scholar 

  • Lee J et al (2013) A cell-cell communication signal integrates quorum sensing and stress response. Nat Chem Biol 9:339–343

    Article  CAS  Google Scholar 

  • Marijana K, Branislav R (2011) Antibacterial and antifungal activity of different lichens extracts and lichen acid. Res J Biotechnol 6:23–26

    Google Scholar 

  • McGrath S, Wade DS, Pesci EC (2004) Dueling quorum sensing systems in Pseudomonas aeruginosa control the production of the Pseudomonas quinolone signal (PQS). FEMS Microbiol Lett 230:27–34. doi:10.1016/S0378-1097(03)00849-8

    Article  CAS  Google Scholar 

  • Nash TH (ed) (2008) Lichen biology. Cambridge University Press, Cambridge

    Google Scholar 

  • Nguyen TT et al (2014) Lichen secondary metabolites in Flavocetraria cucullata exhibit anti-cancer effects on human cancer cells through the induction of apoptosis and suppression of tumorigenic potentials. PLoS ONE 9:e111575. doi:10.1371/journal.pone.0111575

    Article  Google Scholar 

  • Pesci EC, Milbank JB, Pearson JP, McKnight S, Kende AS, Greenberg EP, Iglewski BH (1999) Quinolone signaling in the cell-to-cell communication system of Pseudomonas aeruginosa. Proc Natl Acad Sci 96:11229–11234

    Article  CAS  Google Scholar 

  • Pompilio A et al (2013) Antimicrobial and antibiofilm activity of secondary metabolites of lichens against methicillin-resistant Staphylococcus aureus strains from cystic fibrosis patients. Future Microbiol 8:281–292. doi:10.2217/Fmb.12.142

    Article  CAS  Google Scholar 

  • Proesmans M, Vermeulen F, Boulanger L, Verhaegen J, De Boeck K (2013) Comparison of two treatment regimens for eradication of Pseudomonas aeruginosa infection in children with cystic fibrosis. J Cystic Fibros 12:29–34. doi:10.1016/j.jcf.2012.06.001

    Article  CAS  Google Scholar 

  • Savo V, Joy R, Caneva G, McClatchey WC (2015) Plant selection for ethnobotanical uses on the Amalfi Coast (Southern Italy). J Ethnobiol Ethnomed 11:58. doi:10.1186/s13002-015-0038-y

    Article  CAS  Google Scholar 

  • Shannon KP, French GL (2004) Increasing resistance to antimicrobial agents of Gram-negative organisms isolated at a London teaching hospital, 1995–2000. J Antimicrob Chemother 53:818–825. doi:10.1093/jac/dkh135

    Article  CAS  Google Scholar 

  • Shukla V, Joshi GP, Rawat M (2010) Lichens as a potential natural source of bioactive compounds: a review. Phytochem Rev 9:303–314

    Article  CAS  Google Scholar 

  • Truchado P, Tomas-Barberan FA, Larrosa M, Allende A (2012) Food phytochemicals act as quorum sensing inhibitors reducing production and/or degrading autoinducers of Yersinia enterocolitica and Erwinia carotovora. Food Control 24:78–85. doi:10.1016/j.foodcont.2011.09.006

    Article  CAS  Google Scholar 

  • Yang L, Rybtke MT, Jakobsen TH, Hentzer M, Bjarnsholt T, Givskov M, Tolker-Nielsen T (2009) Computer-aided identification of recognized drugs as Pseudomonas aeruginosa quorum-sensing inhibitors. Antimicrob Agents Chemother 53:2432–2443. doi:10.1128/Aac.01283-08

    Article  CAS  Google Scholar 

  • Zeng Z et al (2008) Virtual screening for novel quorum sensing inhibitors to eradicate biofilm formation of Pseudomonas aeruginosa. Appl Microbiol Biotechnol 79:119–126. doi:10.1007/s00253-008-1406-5

    Article  CAS  Google Scholar 

  • Zhanel GG, Hoban DJ, Schurek K, Karlowsky JA (2004) Role of efflux mechanisms on fluoroquinolone resistance in Streptococcus pneumoniae and Pseudomonas aeruginosa. Int J Antimicrob Agents 24:529–535. doi:10.1016/j.ijantimicag.2004.08.003

    Article  CAS  Google Scholar 

  • Zhang RG et al (2002) Structure of a bacterial quorum-sensing transcription factor complexed with pheromone and DNA. Nature 417:971–974. doi:10.1038/nature00833

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank Tim Holm Jakobsen and Michael Givskov for providing us the monitor strains. This study was funded by the projects: TUBITAK 113S306 (COST FA1202) and BAPKO FEN-A-130515-0177.

Author information

Authors and Affiliations

  1. Department of Biology, Faculty of Arts and Sciences, Marmara University, Göztepe Campus, 34722, Istanbul, Turkey

    Barış Gökalsın & Nüzhet Cenk Sesal

Authors
  1. Barış Gökalsın
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nüzhet Cenk Sesal
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Nüzhet Cenk Sesal.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gökalsın, B., Sesal, N.C. Lichen secondary metabolite evernic acid as potential quorum sensing inhibitor against Pseudomonas aeruginosa . World J Microbiol Biotechnol 32, 150 (2016). https://doi.org/10.1007/s11274-016-2105-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11274-016-2105-5

Keywords

Search

Navigation