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Applied Microbiology and Biotechnology

, Volume 98, Issue 22, pp 9447–9457 | Cite as

Anti-biofilm, anti-hemolysis, and anti-virulence activities of black pepper, cananga, myrrh oils, and nerolidol against Staphylococcus aureus

  • Kayeon Lee
  • Jin-Hyung Lee
  • Soon-Il Kim
  • Moo Hwan Cho
  • Jintae Lee
Environmental biotechnology

Abstract

The long-term usage of antibiotics has resulted in the evolution of multidrug-resistant bacteria. Unlike antibiotics, anti-virulence approaches target bacterial virulence without affecting cell viability, which may be less prone to develop drug resistance. Staphylococcus aureus is a major human pathogen that produces diverse virulence factors, such as α-toxin, which is hemolytic. Also, biofilm formation of S. aureus is one of the mechanisms of its drug resistance. In this study, anti-biofilm screening of 83 essential oils showed that black pepper, cananga, and myrrh oils and their common constituent cis-nerolidol at 0.01 % markedly inhibited S. aureus biofilm formation. Furthermore, the three essential oils and cis-nerolidol at below 0.005 % almost abolished the hemolytic activity of S. aureus. Transcriptional analyses showed that black pepper oil down-regulated the expressions of the α-toxin gene (hla), the nuclease genes, and the regulatory genes. In addition, black pepper, cananga, and myrrh oils and cis-nerolidol attenuated S. aureus virulence in the nematode Caenorhabditis elegans. This study is one of the most extensive on anti-virulence screening using diverse essential oils and provides comprehensive data on the subject. This finding implies other beneficial effects of essential oils and suggests that black pepper, cananga, and myrrh oils have potential use as anti-virulence strategies against persistent S. aureus infections.

Keywords

Anti-virulence Biofilm Black pepper oil Essential oil Hemolysis Staphylococcus aureus 

Notes

Acknowledgments

The 83 essential oils used in this study were kindly provided by Prof. Young-Joon Ahn of Seoul National University. We thank Professor Sang Woo Joo of the World Class University Nano Research Center at Yeungnam University for the use of the scanning confocal laser microscope. This research was supported by the Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education, Science and Technology (Grant nos. 2012R1A1A3010534 and 2010-0021871 to J-H. Lee and J. Lee, respectively).

Supplementary material

253_2014_5903_MOESM1_ESM.pdf (156 kb)
ESM 1 (PDF 156 kb)

References

  1. Adukwu EC, Allen SC, Phillips CA (2012) The anti-biofilm activity of lemongrass (Cymbopogon flexuosus) and grapefruit (Citrus paradisi) essential oils against five strains of Staphylococcus aureus. J Appl Microbiol 113:1217–1227PubMedCrossRefGoogle Scholar
  2. Beenken KE, Mrak LN, Griffin LM, Zielinska AK, Shaw LN, Rice KC, Horswill AR, Bayles KW, Smeltzer MS (2010) Epistatic relationships between sarA and agr in Staphylococcus aureus biofilm formation. PLoS One 5:e10790PubMedCrossRefPubMedCentralGoogle Scholar
  3. Begun J, Gaiani JM, Rohde H, Mack D, Calderwood SB, Ausubel FM, Sifri CD (2007) Staphylococcal biofilm exopolysaccharide protects against Caenorhabditis elegans immune defenses. PLoS Pathog 3:e57PubMedCrossRefPubMedCentralGoogle Scholar
  4. Bhakdi S, Tranum-Jensen J (1991) Alpha-toxin of Staphylococcus aureus. Microbiol Rev 55:733–751PubMedPubMedCentralGoogle Scholar
  5. Boles BR, Horswill AR (2008) Agr-mediated dispersal of Staphylococcus aureus biofilms. PLoS Pathog 4:e1000052PubMedCrossRefPubMedCentralGoogle Scholar
  6. Boles BR, Horswill AR (2011) Staphylococcal biofilm disassembly. Trends Microbiol 19:449–455PubMedCrossRefPubMedCentralGoogle Scholar
  7. Caiazza NC, O'Toole GA (2003) Alpha-toxin is required for biofilm formation by Staphylococcus aureus. J Bacteriol 185:3214–3217PubMedCrossRefPubMedCentralGoogle Scholar
  8. Cegelski L, Marshall GR, Eldridge GR, Hultgren SJ (2008) The biology and future prospects of antivirulence therapies. Nat Rev Microbiol 6:17–27PubMedCrossRefPubMedCentralGoogle Scholar
  9. Costerton JW, Stewart PS, Greenberg EP (1999) Bacterial biofilms: a common cause of persistent infections. Science 284:1318–1322PubMedCrossRefGoogle Scholar
  10. Curvelo JA, Marques AM, Barreto AL, Romanos MT, Portela MB, Kaplan MA, Soares RM (2014) A novel nerolidol-rich essential oil from Piper claussenianum modulates Candida albicans biofilm. J Med Microbiol. doi: 10.1099/jmm.0.063834-0 PubMedGoogle Scholar
  11. Hammer KA, Carson CF, Riley TV (1999) Antimicrobial activity of essential oils and other plant extracts. J Appl Microbiol 86:985–990PubMedCrossRefGoogle Scholar
  12. Helander IM, Alakomi HL, Latva-Kala K, Mattila-Sandholm T, Pol I, Smid EJ, Gorris LGM, von Wright A (1998) Characterization of the action of selected essential oil components on gram-negative bacteria. J Agric Food Chem 46:3590–3595CrossRefGoogle Scholar
  13. Hentzer M, Riedel K, Rasmussen TB, Heydorn A, Andersen JB, Parsek MR, Rice SA, Eberl L, Molin S, Høiby N, Kjelleberg S, Givskov M (2002) Inhibition of quorum sensing in Pseudomonas aeruginosa biofilm bacteria by a halogenated furanone compound. Microbiology 148:87–102PubMedGoogle Scholar
  14. Isman MB (2000) Plant essential oils for pest and disease management. Crop Prot 19:603–608CrossRefGoogle Scholar
  15. Iwase T, Uehara Y, Shinji H, Tajima A, Seo H, Takada K, Agata T, Mizunoe Y (2010) Staphylococcus epidermidis Esp inhibits Staphylococcus aureus biofilm formation and nasal colonization. Nature 465:346–349PubMedCrossRefGoogle Scholar
  16. Izano EA, Amarante MA, Kher WB, Kaplan JB (2008) Differential roles of poly-N-acetylglucosamine surface polysaccharide and extracellular DNA in Staphylococcus aureus and Staphylococcus epidermidis biofilms. Appl Environ Microbiol 74:470–476PubMedCrossRefPubMedCentralGoogle Scholar
  17. Jabra-Rizk MA, Meiller TF, James CE, Shirtliff ME (2006) Effect of farnesol on Staphylococcus aureus biofilm formation and antimicrobial susceptibility. Antimicrob Agents Chemother 50:1463–1469PubMedCrossRefPubMedCentralGoogle Scholar
  18. Kapoor IP, Singh B, Singh G, De Heluani CS, De Lampasona MP, Catalan CA (2009) Chemistry and in vitro antioxidant activity of volatile oil and oleoresins of black pepper (Piper nigrum). J Agric Food Chem 57:5358–5364PubMedCrossRefGoogle Scholar
  19. Kristiawan M, Sobolik V, Al-Haddad A, Allaf K (2008) Effect of pressure-drop rate on the isolation of cananga oil using instantaneous controlled pressure-drop process. Chem Eng Process 47:66–75CrossRefGoogle Scholar
  20. Kwieciński J, Eick S, Wójcik K (2009) Effects of tea tree (Melaleuca alternifolia) oil on Staphylococcus aureus in biofilms and stationary growth phase. Int J Antimicrob Agents 33:343–347PubMedCrossRefGoogle Scholar
  21. Larzábal M, Mercado EC, Vilte DA, Salazar-González H, Cataldi A, Navarro-Garcia F (2010) Designed coiled-coil peptides inhibit the type three secretion system of enteropathogenic Escherichia coli. PLoS One 5:e9046PubMedCrossRefPubMedCentralGoogle Scholar
  22. Lee J-H, Cho MH, Lee J (2011) 3-Indolylacetonitrile decreases Escherichia coli O157:H7 biofilm formation and Pseudomonas aeruginosa virulence. Environ Microbiol 13:62–73PubMedCrossRefGoogle Scholar
  23. Lee J-H, Park J-H, Cho MH, Lee J (2012) Flavone reduces the production of virulence factors, staphyloxanthin and α-hemolysin, in Staphylococcus aureus. Curr Microbiol 65:726–732PubMedCrossRefGoogle Scholar
  24. Lee J-H, Cho HS, Kim Y, Kim J-A, Banskota S, Cho MH, Lee J (2013) Indole and 7-benzyloxyindole attenuate the virulence of Staphylococcus aureus. Appl Microbiol Biotechnol 97:4543–4552PubMedCrossRefGoogle Scholar
  25. Levy SB, Marshall B (2004) Antibacterial resistance worldwide: causes, challenges and responses. Nat Med 10:S122–S129PubMedCrossRefGoogle Scholar
  26. Liu CI, Liu GY, Song Y, Yin F, Hensler ME, Jeng WY, Nizet V, Wang AH, Oldfield E (2008) A cholesterol biosynthesis inhibitor blocks Staphylococcus aureus virulence. Science 319:1391–1394PubMedCrossRefPubMedCentralGoogle Scholar
  27. Lowy FD (1998) Staphylococcus aureus infections. N Engl J Med 339:520–532PubMedCrossRefGoogle Scholar
  28. Mann EE, Rice KC, Boles BR, Endres JL, Ranjit D, Chandramohan L, Tsang LH, Smeltzer MS, Horswill AR, Bayles KW (2009) Modulation of eDNA release and degradation affects Staphylococcus aureus biofilm maturation. PLoS One 4:e5822PubMedCrossRefPubMedCentralGoogle Scholar
  29. Marongiu B, Piras A, Porcedda S, Scorciapino A (2005) Chemical composition of the essential oil and supercritical CO2 extract of Commiphora myrrha (Nees) Engl. and of Acorus calamus L. J Agric Food Chem 53:7939–7943PubMedCrossRefGoogle Scholar
  30. Murphy CT, McCarroll SA, Bargmann CI, Fraser A, Kamath RS, Ahringer J, Li H, Kenyon C (2003) Genes that act downstream of DAF-16 to influence the lifespan of Caenorhabditis elegans. Nature 424:277–283PubMedCrossRefGoogle Scholar
  31. Nostro A, Sudano Roccaro A, Bisignano G, Marino A, Cannatelli MA, Pizzimenti FC, Cioni PL, Procopio F, Blanco AR (2007) Effects of oregano, carvacrol and thymol on Staphylococcus aureus and Staphylococcus epidermidis biofilms. J Med Microbiol 56:519–523PubMedCrossRefGoogle Scholar
  32. Nuryastuti T, van der Mei HC, Busscher HJ, Iravati S, Aman AT, Krom BP (2009) Effect of cinnamon oil on icaA expression and biofilm formation by Staphylococcus epidermidis. Appl Environ Microbiol 75:6850–6855PubMedCrossRefPubMedCentralGoogle Scholar
  33. Ohlsen K, Koller KP, Hacker J (1997) Analysis of expression of the alpha-toxin gene (hla) of Staphylococcus aureus by using a chromosomally encoded hla::lacZ gene fusion. Infect Immun 65:3606–3614PubMedPubMedCentralGoogle Scholar
  34. Olivero J, Gracia T, Payares P, Vivas R, Díaz D, Daza E, Geerlings P (1997) Molecular structure and gas chromatographic retention behavior of the components of Ylang-Ylang oil. J Pharm Sci 86:625–630PubMedCrossRefGoogle Scholar
  35. Oscarsson J, Kanth A, Tegmark-Wisell K, Arvidson S (2006) SarA is a repressor of hla (α-hemolysin) transcription in Staphylococcus aureus: its apparent role as an activator of hla in the prototype strain NCTC 8325 depends on reduced expression of sarS. J Bacteriol 188:8526–8533PubMedCrossRefPubMedCentralGoogle Scholar
  36. Park J, Jagasia R, Kaufmann GF, Mathison JC, Ruiz DI, Moss JA, Meijler MM, Ulevitch RJ, Janda KD (2007) Infection control by antibody disruption of bacterial quorum sensing signaling. Chem Biol 14:1119–1127PubMedCrossRefPubMedCentralGoogle Scholar
  37. Reddy SV, Srinivas PV, Praveen B, Kishore KH, Raju BC, Murthy US, Rao JM (2004) Antibacterial constituents from the berries of Piper nigrum. Phytomedicine 11:697–700PubMedCrossRefGoogle Scholar
  38. Schillaci D, Arizza V, Dayton T, Camarda L, Di Stefano V (2008) In vitro anti-biofilm activity of Boswellia spp. oleogum resin essential oils. Lett Appl Microbiol 47:433–438PubMedCrossRefGoogle Scholar
  39. Sifri CD, Begun J, Ausubel FM, Calderwood SB (2003) Caenorhabditis elegans as a model host for Staphylococcus aureus pathogenesis. Infect Immun 71:2208–2217PubMedCrossRefPubMedCentralGoogle Scholar
  40. Song L, Hobaugh MR, Shustak C, Cheley S, Bayley H, Gouaux JE (1996) Structure of staphylococcal α-hemolysin, a heptameric transmembrane pore. Science 274:1859–1866PubMedCrossRefGoogle Scholar
  41. Stewart PS, Costerton JW (2001) Antibiotic resistance of bacteria in biofilms. Lancet 358:135–138PubMedCrossRefGoogle Scholar
  42. Tipton DA, Lyle B, Babich H, Dabbous MK (2003) In vitro cytotoxic and anti-inflammatory effects of myrrh oil on human gingival fibroblasts and epithelial cells. Toxicol In Vitro 17:301–310PubMedCrossRefGoogle Scholar
  43. Weston SA, Parish CR (1990) New fluorescent dyes for lymphocyte migration studies. Analysis by flow cytometry and fluorescence microscopy. J Immunol Methods 133:87–97PubMedCrossRefGoogle Scholar
  44. Wilke GA, Bubeck Wardenburg J (2010) Role of a disintegrin and metalloprotease 10 in Staphylococcus aureus α-hemolysin-mediated cellular injury. Proc Natl Acad Sci U S A 107:13473–13478PubMedCrossRefPubMedCentralGoogle Scholar
  45. Wyatt MA, Wang W, Roux CM, Beasley FC, Heinrichs DE, Dunman PM, Magarvey NA (2010) Staphylococcus aureus nonribosomal peptide secondary metabolites regulate virulence. Science 329:294–296PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Kayeon Lee
    • 1
  • Jin-Hyung Lee
    • 1
  • Soon-Il Kim
    • 2
  • Moo Hwan Cho
    • 1
  • Jintae Lee
    • 1
  1. 1.School of Chemical EngineeringYeungnam UniversityGyeongsanRepublic of Korea
  2. 2.Nareso Research CenterSuwonRepublic of Korea

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