Aim: To investigate the hypothesis that zeolites interfere with quorum-sensing (QS) systems of Chromobacterium violaceum and Pseudomonas aeruginosa by adsorbing N-acyl homoserine lactone (AHL) signal molecules. Methods: QS inhibition by zeolite 4A was investigated using an AHL-based bioreporter assay. The adsorption of the AHLs was evaluated by performing inductively coupled plasma–optical emission spectroscopy and confirmed by Monte Carlo and molecular dynamic simulations. Results: Zeolite 4A reduced the violacein production in C. violaceum by over 90% and the biofilm formation, elastase and pyocyanin production in P. aeruginosa by 87, 68 and 98%, respectively. Conclusion: Zeolite 4A disrupts the QS systems of C. violaceum and P. aeruginosa by means of adsorbing 3-oxo-C6-AHL and 3-oxo-C12-AHL signaling molecules and can be developed as a novel QS jammer to combat P. aeruginosa-related infections.

Keywords:

References

1. Rutherford ST, Bassler BL. Bacterial quorum sensing: its role in virulence and possibilities for its control. Cold Spring Harb. Perspect. Med. 2(11), a012427 (2012).
MedlineGoogle Scholar
2. Schauder S, Bassler BL. The languages of bacteria. Genes Devel. 15(12), 1468–1480 (2001).
Medline CASGoogle Scholar
3. De Kievit TR, Gillis R, Marx S, Brown C, Iglewski BH. Quorum-sensing genes in Pseudomonas aeruginosa biofilms: their role and expression patterns. Appl. Environ. Microbiol. 67(4), 1865–1873 (2001).
MedlineGoogle Scholar
4. Ikeno T, Fukuda K, Ogawa M, Honda M, Tanabe T, Taniguchi H. Small and rough colony Pseudomonas aeruginosa with elevated biofilm formation ability isolated in hospitalized patients. Microbiol. Immunol. 51(10), 929–938 (2007).
Medline CASGoogle Scholar
5. Van Delden C, Iglewski BH. Cell-to-cell signaling and Pseudomonas aeruginosa infections. Emerg. Infect. Dis. 4(4), 551 (1998).
Medline CASGoogle Scholar
6. Pearson JP, Gray KM, Passador L et al. Structure of the autoinducer required for expression of Pseudomonas aeruginosa virulence genes. Proc. Natl Acad. Sci. USA 91(1), 197–201 (1994).
Medline CASGoogle Scholar
7. Pearson JP, Passador L, Iglewski BH, Greenberg E. A second N-acylhomoserine lactone signal produced by Pseudomonas aeruginosa. Proc. Natl Acad. Sci. USA 92(5), 1490–1494 (1995).
Medline CASGoogle Scholar
8. Heeb S, Fletcher MP, Chhabra SR, Diggle SP, Williams P, Cámara M. Quinolones: from antibiotics to autoinducers. FEMS Microbiol. Rev. 35(2), 247–274 (2011).
Medline CASGoogle Scholar
9. Costerton J, Stewart PS, Greenberg E. Bacterial biofilms: a common cause of persistent infections. Science 284(5418), 1318–1322 (1999).
Medline CASGoogle Scholar
10. Bjarnsholt T, Jensen PØ, Rasmussen TB et al. Garlic blocks quorum sensing and promotes rapid clearing of pulmonary Pseudomonas aeruginosa infections. Microbiology 151(12), 3873–3880 (2005).
Medline CASGoogle Scholar
11. Lee SJ, Park SY, Lee JJ, Yum DY, Koo BT, Lee JK. Genes encoding the N-acyl homoserine lactone-degrading enzyme are widespread in many subspecies of Bacillus thuringiensis. Appl. Environ. Microbiol. 68(8), 3919–3924 (2002).
Medline CASGoogle Scholar
12. Uroz S, Oger PM, Chapelle E, Adeline MT, Faure D, Dessaux Y. A Rhodococcus qsdA-encoded enzyme defines a novel class of large-spectrum quorum-quenching lactonases. Appl. Environ. Microbiol. 74(5), 1357–1366 (2008).
Medline CASGoogle Scholar
13. Bjarnsholt T, Van Gennip M, Jakobsen TH, Christensen LD, Jensen PO, Givskov M. In vitro screens for quorum sensing inhibitors and in vivo confirmation of their effect. Nat. Protoc. 5(2), 282–293 (2010).
Medline CASGoogle Scholar
14. Rasamiravaka T, Jedrzejowski A, Kiendrebeogo M et al. Endemic Malagasy Dalbergia species inhibit quorum sensing in Pseudomonas aeruginosa PAO1. Microbiology 159(Pt 5), 924–938 (2013).
Medline CASGoogle Scholar
15. Majik MS, Gawas UB, Mandrekar VK. Next generation quorum sensing inhibitors: accounts on structure activity relationship studies and biological activities. Bioorg. Med. Chem. 28(21), 115728 (2020).
Medline CASGoogle Scholar
16. Beus M, Savijoki K, Patel JZ, Yli-Kauhaluoma J, Fallarero A, Zorc B. Chloroquine fumardiamides as novel quorum sensing inhibitors. Bioorg. Med. Chem. Lett. 30(16), 127336 (2020).
Medline CASGoogle Scholar
17. Bosgelmez-Tinaz G, Ulusoy S, Ugur A, Ceylan O. Inhibition of quorum sensing-regulated behaviors by Scorzonera sandrasica. Curr. Microbiol. 55(2), 114–118 (2007).
Medline CASGoogle Scholar
18. Eris R, Ulusoy S. Rose, clove, chamomile essential oils and pine turpentine inhibit quorum sensing in Chromobacterium violaceum and Pseudomonas aeruginosa. J. Essent. Oil Bearing Plants 16(2), 126–135 (2013).
CASGoogle Scholar
19. Miandji A, Ulusoy S, Dündar Y et al. Synthesis and biological activities of some 1,3-benzoxazol-2 (3H)-one derivatives as anti-quorum sensing agents. Arzneimittel-Forschung 62(7), 330–334 (2012).
Medline CASGoogle Scholar
20. Ulusoy S, Senkardes S, Coskun I et al. Quorum sensing inhibitor activities of celecoxib derivatives in Pseudomonas aeruginosa. Lett. Drug Des. Discov. 14(5), 613–618 (2017).
CASGoogle Scholar
21. Jiang K, Yan X, Yu J et al. Design, synthesis, and biological evaluation of 3-amino-2-oxazolidinone derivatives as potent quorum-sensing inhibitors of Pseudomonas aeruginosa PAO1. Eur. J. Med. Chem. 194, 112252 (2020).
Medline CASGoogle Scholar
22. Hançer Aydemir D, Cifci G, Aviyente V, Boşgelmez-Tinaz G. Quorum-sensing inhibitor potential of trans-anethole aganist Pseudomonas aeruginosa. J. Appl. Microbiol. 125(3), 731–739 (2018).
MedlineGoogle Scholar
23. Petrus R, Warchoł J. Ion exchange equilibria between clinoptilolite and aqueous solutions of Na⁺/Cu 2⁺, Na⁺/Cd 2⁺ and Na⁺/Pb 2⁺. Micropor. Mesopor. Mater. 61(1), 137–146 (2003).
CASGoogle Scholar
24. Wang S, Peng Y. Natural zeolites as effective adsorbents in water and wastewater treatment. Chem. Eng. J. 156(1), 11–24 (2010).
CASGoogle Scholar
25. Morris RE. Microporous materials in antibacterial applications. In: Antimicrobial Coatings and Modifications on Medical Devices. Springer Nature, Cham, Switzerland, 171–188 (2017).
Google Scholar
26. Servatan M, Zarrintaj P, Mahmodi G et al. Zeolites in drug delivery: progress, challenges and opportunities. Drug Discov. Today 25(4), 642–656 (2020).
Medline CASGoogle Scholar
27. Choo J, Rukayadi Y, Hwang JK. Inhibition of bacterial quorum sensing by vanilla extract. Lett. Appl. Microbiol. 42(6), 637–641 (2006).
Medline CASGoogle Scholar
28. McClean KH, Winson MK, Fish L et al. Quorum sensing and Chromobacterium violaceum: exploitation of violacein production and inhibition for the detection of N-acylhomoserine lactones. Microbiology 143(12), 3703–3711 (1997).
Medline CASGoogle Scholar
29. Morohoshi T, Kato M, Fukamachi K, Kato N, Ikeda T. N-acylhomoserine lactone regulates violacein production in Chromobacterium violaceum type strain ATCC 12472. FEMS Microbiol. Lett. 279(1), 124–130 (2008).
Medline CASGoogle Scholar
30. Im H, Choi SY, Son S, Mitchell RJ. Combined application of bacterial predation and violacein to kill polymicrobial pathogenic communities. Sci. Rep. 7(1), 1–10 (2017).
MedlineGoogle Scholar
31. O’Toole GA, Kolter R. Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis. Mol. Microbiol. 28(3), 449–461 (1998).
MedlineGoogle Scholar
32. Li H, Li X, Wang Z et al. Autoinducer-2 regulates Pseudomonas aeruginosa PAO1 biofilm formation and virulence production in a dose-dependent manner. BMC Microbiol. 15(1), 1–8 (2015).
MedlineGoogle Scholar
33. Essar D, Eberly L, Hadero A, Crawford I. Identification and characterization of genes for a second anthranilate synthase in Pseudomonas aeruginosa: interchangeability of the two anthranilate synthases and evolutionary implications. J. Bacteriol. 172(2), 884–900 (1990).
Medline CASGoogle Scholar
34. Ohman D, Cryz S, Iglewski B. Isolation and characterization of Pseudomonas aeruginosa PAO mutant that produces altered elastase. J. Bacteriol. 142(3), 836–842 (1980).
Medline CASGoogle Scholar
35. Hsissou R, Benhiba F, Abbout S et al. Trifunctional epoxy polymer as corrosion inhibition material for carbon steel in 1.0 M HCl: MD simulations, DFT and complexation computations. Inorg. Chem. Commun. 115, 107858 (2020).
CASGoogle Scholar
36. Hsissou R, Abbout S, Seghiri R et al. Evaluation of corrosion inhibition performance of phosphorus polymer for carbon steel in [1 M] HCl: computational studies (DFT, MC and MD simulations). J. Mater. Res. Technol. 9(3), 2691–2703 (2020).
CASGoogle Scholar
37. Hsissou R, Dagdag O, Abbout S et al. Novel derivative epoxy resin TGETET as a corrosion inhibition of E24 carbon steel in 1.0 M HCl solution. Experimental and computational (DFT and MD simulations) methods. J. Mol. Liq. 284, 182–192 (2019).
CASGoogle Scholar
38. Dagdag O, Hsissou R, El Harfi A et al. Fabrication of polymer based epoxy resin as effective anti-corrosive coating for steel: computational modeling reinforced experimental studies. Surf. Interfaces 18, 100454 (2020).
CASGoogle Scholar
39. Dagdag O, Berisha A, Safi Z et al. DGEBA-polyaminoamide as effective anti-corrosive material for 15CDV6 steel in NaCl medium: computational and experimental studies. J. Appl. Polym. Sci. 137(8), 48402 (2020).
CASGoogle Scholar
40. Sun H, Jin Z, Yang C et al. COMPASS II: extended coverage for polymer and drug-like molecule databases. J. Mol. Model. 22(2), 47 (2016).
MedlineGoogle Scholar
41. Abbout S, Zouarhi M, Chebabe D, Damej M, Berisha A, Hajjaji N. Galactomannan as a new bio-sourced corrosion inhibitor for iron in acidic media. Heliyon 6(3), e03574 (2020).
MedlineGoogle Scholar
42. Dagdag O, Berisha A, Safi Z et al. Highly durable macromolecular epoxy resin as anticorrosive coating material for carbon steel in 3% NaCl: computational supported experimental studies. J. Appl. Polym. Sci. 137(34), 49003 (2020).
CASGoogle Scholar
43. Berisha A. The influence of the grafted aryl groups on the solvation properties of the graphyne and graphdiyne-a MD study. Open Chemistry 17(1), 703–710 (2019).
CASGoogle Scholar
44. Hsissou R, Benzidia B, Rehioui M et al. Anticorrosive property of hexafunctional epoxy polymer HGTMDAE for E24 carbon steel corrosion in 1.0 M HCl: gravimetric, electrochemical, surface morphology and molecular dynamic simulations. Polym. Bull. 77, 3577–3601 (2019).
Google Scholar
45. Guo L, Zhang S, Li W, Hu G, Li X. Experimental and computational studies of two antibacterial drugs as corrosion inhibitors for mild steel in acid media. Mater. Corros. 65(9), 935–942 (2014).
CASGoogle Scholar
46. Dagdag O, Hsissou R, Berisha A et al. Polymeric-based epoxy cured with a polyaminoamide as an anticorrosive coating for aluminum 2024-T3 surface: experimental studies supported by computational modeling. J. Bio- Tribo-Corros. 5(3), 58 (2019).
Google Scholar
47. Kalia VC. Quorum sensing inhibitors: an overview. Biotechnol. Adv. 31(2), 224–245 (2013).
Medline CASGoogle Scholar
48. Kim HS, Lee SH, Byun Y, Park HD. 6-Gingerol reduces Pseudomonas aeruginosa biofilm formation and virulence via quorum sensing inhibition. Sci. Rep. 5, 8656 (2015).
Medline CASGoogle Scholar
49. Imperi F, Tiburzi F, Fimia GM, Visca P. Transcriptional control of the pvdS iron starvation sigma factor gene by the master regulator of sulfur metabolism CysB in Pseudomonas aeruginosa. Environ. Microbiol. 12(6), 1630–1642 (2010).
Medline CASGoogle Scholar
50. Galloway WR, Hodgkinson JT, Bowden S, Welch M, Spring DR. Applications of small molecule activators and inhibitors of quorum sensing in Gram-negative bacteria. Trends Microbiol. 20(9), 449–458 (2012).
Medline CASGoogle Scholar
51. Khan MSA, Zahin M, Hasan S, Husain FM, Ahmad I. Inhibition of quorum sensing regulated bacterial functions by plant essential oils with special reference to clove oil. Lett. Appl. Microbiol. 49(3), 354–360 (2009).
Medline CASGoogle Scholar
52. Yu L, Gong J, Zeng C, Zhang L. Preparation of zeolite-A/chitosan hybrid composites and their bioactivities and antimicrobial activities. Mater. Sci. Eng. C 33(7), 3652–3660 (2013).
Medline CASGoogle Scholar
53. Ames L Jr. The cation sieve properties of clinoptilolite. Am. Mineral. 45(5–6), 689–700 (1960).
CASGoogle Scholar
54. Ackley MW, Yang RT. Diffusion in ion-exchanged clinoptilolites. AIChE J. 37(11), 1645–1656 (1991).
CASGoogle Scholar
55. Jiang N, Yuan S, Wang J, Jiao H, Qin Z, Li YW. A theoretical study of amines adsorption in HMOR by using ONIOM2 method. J. Mol. Catal. A Chem. 220(2), 221–228 (2004).
CASGoogle Scholar
56. Wingenfelder U, Nowack B, Furrer G, Schulin R. Adsorption of Pb and Cd by amine-modified zeolite. Water Res. 39(14), 3287–3297 (2005).
Medline CASGoogle Scholar
57. Derouane EG, Chang CD. Confinement effects in the adsorption of simple bases by zeolites. Micropor. Mesopor. Mater. 35, 425–433 (2000).
Google Scholar
58. Guo X, Yun H, Zhang M et al. Adsorption of low-molecular-weight amines in aqueous solutions to zeolites: an approach to impeding low-molecular-weight amines from regenerating N-nitrosamines. Ind. Eng. Chem. Res. 56(42), 12024–12031 (2017).
CASGoogle Scholar
59. Hentzer M, Wu H, Andersen JB et al. Attenuation of Pseudomonas aeruginosa virulence by quorum sensing inhibitors. EMBO J. 22(15), 3803–3815 (2003).
Medline CASGoogle Scholar
60. Jakobsen TH, Bragason SK, Phipps RK et al. Food as a source for QS inhibitors: iberin from horseradish revealed as a quorum sensing inhibitor of Pseudomonas aeruginosa. Appl. Environ. Microbiol. 78(7), 2410–2421 (2012).
Medline CASGoogle Scholar
61. Naik SP, Scholin J, Ching S, Chi F, Herpfer M. Quorum sensing disruption in Vibrio harveyi bacteria by clay materials. J. Agric. Food Chem. 66(1), 40–44 (2018).
Medline CASGoogle Scholar
62. Fruijtier-Pölloth C. The safety of synthetic zeolites used in detergents. Arch. Toxicol. 83(1), 23–35 (2009).
MedlineGoogle Scholar
63. Für Risikobewertung B. Introduction to the problems surrounding garment textiles. Report no.: BfR Information no. 018/2007. German Federal Institute for Risk Assessment (BfR), Berlin (DE) (2007).
Google Scholar

Vol. 17, No. 11

Supplemental Materials

Metrics

Downloaded 37 times

History

Received 5 July 2021

Accepted 4 May 2022

Published online 6 June 2022

Published in print July 2022

Information

Keywords

Supplementary data

To view the supplementary data that accompany this paper please visit the journal website at: www.futuremedicine.com/doi/suppl/10.2217/fmb-2021-0174

Author contributions

S Ulusoy designed and supervised this research. All authors contributed to the construction and writing of this article.

Financial & competing interests disclosure

The authors have no relevant affiliations or financial involvement with any organization or entity with a financial interest in or financial conflict with the subject matter or materials discussed in the manuscript. This includes employment, consultancies, honoraria, stock ownership or options, expert testimony, grants or patents received or pending, or royalties.

No writing assistance was utilized in the production of this manuscript.

PDF download