Natural bioactives versus synthetic antibiotics for the attenuation of quorum sensing-regulated virulence factors of Pseudomonas aeruginosa
Abstract
Aim: To study the influence of plant volatiles, bioactives and synthetic antibiotics on the attenuation of the quorum sensing (QS)-regulated virulence factors of Pseudomonas aeruginosa. Materials & methods: QS inhibition; the QS-regulated virulence factors pyocyanin, hemolysin, elastase, protease, alginate and pyochelin; and motility phenotypes were performed at sub-MIC to check the attenuation effect of 24 agents on the virulence of P. aeruginosa. Results: Eighteen out of 24 assayed compounds exhibited anti-QS activity and reduced the production of all virulence factors. Cinnamaldehyde, zingerone and lavender oil exhibited a significant reduction in motility phenotypes. Conclusion: Natural phytomolecules as a whole or their bioactives could be used to develop antivirulence drugs after in vivo evaluation.
Graphical abstract
References
- 1. Environment looming global-scale failures and missing institutions. Science 325, 1345–1346 (2009).
- 2. . Targeting the Pseudomonas quinolone signal quorum sensing system for the discovery of novel anti-infective pathoblockers. Beilstein. J. Org. Chem. 14, 2627–2645 (2018).
- 3. . Azithromycin inhibits quorum sensing in Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 45(6), 1930–1933 (2001).
- 4. Inhibition of quorum sensing in Pseudomonas aeruginosa biofilm bacteria by a halogenated furanone compound. Microbiology 148(1), 87–102 (2000).
- 5. Down regulation of virulence factors of Pseudomonas aeruginosa by salicylic acid attenuates its virulence on Arabidopsis thaliana and Caenorhabditis elegans. Infect. Immun. 73(9), 5319–5328 (2005).
- 6. . Quorum sensing inhibition in Pseudomonas aeruginosa biofilms: new insights through network mining. Biofouling 33(2), 128–142 (2017).
- 7. . Plant products as antimicrobial agents. Clin. Microbiol. Rev. 12(4), 564–582 (1999).
- 8. . Plant products as antimicrobial agents. Analele Ştiinţifice ale Universităţii „Alexandru Ioan Cuza”, Secţiunea Genetică şi Biologie Moleculară 8, 151–156 (2007).
- 9. . Plant-microbe interactions and secondary metabolites with antibacterial, antifungal and antiviral properties. In: Annual Plant Reviews Volume 39: Functions and Biotechnology of Plant Secondary Metabolites (2nd Edition). Wink M (Ed.). Wiley-Blackwell, Oxford, UK, 214–347 (2010).
- 10. . Plants secrete substances that mimic bacterial N-acyl homoserine lactone signal activities and affect population density-dependent behaviors in associated bacteria. Mol. Plant Microbe Interact. 13(6), 637–648 (2000).
- 11. . Inhibitory activity of yarrow essential oil on Listeria planktonic cells and biofilms. Food Control 29(1), 125–130 (2013).
- 12. . Expression of quorum sensing and virulence factors are interlinked in Pseudomonas aeruginosa: an in vitro approach. Am. J. Biomed. Sci. 3(2), 116–125 (2011).
- 13. . Dietary phytochemicals as quorum sensing inhibitors. Fitoterapia 78(4), 302–310 (2007).
- 14. . Herbs, spices and medicinal plants used in Hispanic traditional medicine can decrease quorum sensing dependent virulence in Pseudomonas aeruginosa. Int. J. Appl. Res. Nat. Prod. 1(2), 9–15 (2008).
- 15. . Direct haemolytic activity of phospholipase A. Biochim. Biophys. Acta 270(2), 241–247 (1972).
- 16. . Virulence determinants in Pseudomonas aeruginosa strains from urinary tract infections. Epidemiol. Infect. 108(2), 323–336 (1992).
- 17. . Mucoid conversion of Pseudomonas aeruginosa by hydrogen peroxide: a mechanism for virulence activation in the cystic fibrosis lung. Microbiol. Soc. 145(6), 1349–1357 (1999).
- 18. . Colorimetric determination of the components of 3,4-dihydroxyphenylalanine-tyrosine mixtures. J. Biol. Chem. 118(2), 531–537 (1937).
- 19. . Screening of some medicinal plants of Ethiopia for their anti-microbial properties and chemical profiles. J. Ethnopharmacol. 97, 421–427 (2005).
- 20. . Antimicrobial activities of some selected traditional Ethiopian medicinal plants used in the treatment of skin disorders. J. Ethnopharmacol. 100, 168–175 (2005).
- 21. . Antibacterial activities of selected medicinal plants in traditional treatment of human wounds in Ethiopia. Asian Pac. J. Trop. Biomed. 1(5), 370–375 (2011).
- 22. . Antimicrobial activity of traditional medicinal plants from Ankober District, North Shewa Zone, Amhara Region, Ethiopia. Pharm. Biol. 52(5), 614–620 (2014).
- 23. . Evaluation of antibacterial activity and phytochemical constituents of leaf extract of Lippia adoensis. Asia Pacific J. Energy Environ. 1(1), 45–53 (2014).
- 24. . Evaluation for in-vitro antibacterial activity of selected medicinal plants against food-borne pathogens. In. J. Pharmaceutical Sci. Rev. Res. 32(2), 45–50 (2015).
- 25. In vitro antimicrobial activity of plants used intraditional medicine in Gurage and Silti Zones, south central Ethiopia. BMC Complement. Altern. Med. 5, 286 (2015).
- 26. Anti-quorum sensing activity of 12 essential oils on Chromobacterium violaceum and specific action of cis-cis-p-menthenolide from corsican Mentha suaveolens ssp. insularis. Molecules 23, 1–11 (2018).
- 27. Buchbauer G Biological activities of essential oils. In: Handbook of Essential Oils: Science Technology, and Applications. Buchbauer GBaser KHC (Eds). CRC Press, FL, USA, 235–280 (2009).
- 28. . Anticancer activity of essential oils: a review. J. Sci. Food Agric. 93(15), 3643–3653 (2013).
- 29. . Antioxidant activity of Coriandrum sativum and protection against DNA damage and cancer cell migration. BMC Complement. Altern Med. 13(1), 1–13 (2013).
- 30. . Phytochemical screening and antidermatophytic activity of lavender essential oil from Saudi Arabia. Int. J. Pharmacol. 14(6), 802–810 (2018).
- 31. . Antimicrobial activity of spices. Int. J. Antimicrob. Agents 12(3), 257–262 (1999).
- 32. Effect of polyphenols on microbial cell-cell communications. In: Quorum Sensing: Molecular Mechanism and Biotechnological Application. Tommonaro G (Ed.). Academic Press, MA, USA, 195–223 (2019).
- 33. . Integrated regulation of acetoin fermentation by quorum sensing and pH in Serratia plymuthica RVH1. Appl. Environ. Microbiol. 77(10), 3422–3427 (2011).
- 34. . The impact of plant volatiles on bacterial quorum sensing. Lett. Appl. Microbiol. 60(1), 8–19 (2015).
- 35. . Influence of clove oil on certain quorum-sensing-regulated functions and biofilm of Pseudomonas aeruginosa and Aeromonas hydrophila. J. Biosci. 38(5), 835–844 (2013).
- 36. . Inhibition of quorum sensing-related biofilm of Pseudomonas fluorescens KM121 by Thymus vulgare essential oil and its major bioactive compounds. Int. Biodeterior. Biodegr. 114, 252–259 (2016).
- 37. . Initiation of biofilm formation by Pseudomonas aeruginosa 57RP correlates with emergence of hyperpiliated and highly adherent phenotypic variants deficient in swimming, swarming, and twitching motilities. J. Bacteriol. 183(4), 1195–1204 (2001).
- 38. . Analysis of quorum sensing inhibition and phytochemicals in different extracts of garlic. Int. J. Pharm. Bio. Sci. 5(3), 873–884 (2014).
- 39. . Terpinen-4-ol attenuates quorum sensing regulated virulence factors and biofilm formation in Pseudomonas aeruginosa. Future Microbiol. 15(2), 127–142 (2020).
- 40. Inhibition of quorum-sensing signals by essential oils. Phytother. Res. 24, 782–786 (2010).
- 41. Effect of cinnamon oil on quorum sensing-controlled virulence factors and biofilm formation in Pseudomonas aeruginosa. PLoS ONE 10(8), e0135495 (2015).
- 42. Pomegranate fruit extract impairs invasion and motility in human breast cancer. Integr. Cancer Ther. 8(3), 242–253 (2009).
- 43. . Pseudomonas aeruginosa biofilms: role of the alginate exopolysaccharide. J. Ind. Microbiol. Biotechnol. 15(3), 162–168 (1995).
- 44. . Antimicrobial resistance and putative virulence genes of Pseudomonas aeruginosa isolates from patients with respiratory tract infection. Germs 8(1), 31 (2018).
- 45. . Anti-quorum sensing activity of medicinal plants in southern Florida. J. Ethnopharmacol. 105(3), 427–435 (2006).
- 46. . Curcumin, a known phenolic from Curcuma longa, attenuates the virulence of Pseudomonas aeruginosa PAO1 in whole plant and animal pathogenicity models. J. Agric Food Chem. 56, 1955–1962 (2008).
- 47. . Anti-quorum sensing activity of essential oils from Colombian plants. Nat. Prod. Res. 26(12), 1075–1086 (2012).
- 48. . Natural quorum sensing inhibitors effectively downregulate gene expression of Pseudomonas aeruginosa virulence factors. Appl. Microbiol. Biotechnol. 103(8), 3521–3535 (2019).
- 49. . Zingerone silences quorum sensing and attenuates virulence of Pseudomonas aeruginosa. Fitoterapia 102, 84–95 (2015).
- 50. A cell-cell communication signal integrates quorum sensing and stress response. Nat. Chem. Biol. 9, 339–343 (2013).
- 51. . Pseudomonas aeruginosa adapts its iron uptake strategies in function of the type of infections. Front. Cell. Infect. Microbiol. 3, 75 (2013).