Effect of Rose (Rosa damascena Mill) Essential Oil on Biofilm Formation and Swarming Motility on Pseudomonas aeruginosa

Year 2023, , 367 - 374, 31.12.2023

Halime Çevikbaş , Seyhan Ulusoy

https://doi.org/10.24323/akademik-gida.1423448

Abstract

Pseudomonas aeruginosa is a Gram-negative, opportunistic pathogen that causes acute and chronic infections in immunocompromised patients. P. aeruginosa controls the production of virulence factors and biofilm formation properties with the Quorum sensing (QS) communication system, which is a kind of intercellular communication system. Studies have been carried out on the control of pathogenic bacteria by blocking or directing this communication system with different synthetic or natural molecules. Herbal essential oils, which have antibacterial, antifungal and antiviral activities because of their active molecules, have great potential in this sense. In this study, the inhibitory effects of rose essential oil, its major components (citronellol, geraniol, and nerol), and a combination of these three components (CGN) on the intercellular communication (QS) system of Pseudomonas aeruginosa PA01 strain were investigated. As a result of the study, it was determined that rose essential oil inhibited the swarming motility for the P. aeruginosa PA01 strain by 83%, and the inhibition by citronellol, geraniol, nerol, and a mixture CGN was in the range of 61-75%. For P. aeruginosa PA01 strain, biofilm formation was suppressed by rose essential oil by 54-68%, citronellol, geraniol, nerol, and mixture CGN by 10-15%. It was important that rose essential oil inhibited the swarming motility and biofilm formation of P. aeruginosa at a higher rate than the essential components of rose oil. The results of this study showed that citronellol, nerol, geraniol, and CGN had anti-QS activity for P. aeruginosa strain, but rose essential oil had a potential to be used in various applications.

Keywords

Quorum sensing, Rose essential oil, Biofilm, P. aeruginosa

Supporting Institution

Süleyman Demirel Üniversitesi, Bilimsel Araştırma Projeleri Koordinasyon Birimi

Project Number

2776-YL-11

Thanks

Bu çalışma, Süleyman Demirel Üniversitesi, Bilimsel Araştırma Projeleri Koordinasyon Birimi tarafından 2776-YL-11 No'lu Proje ile mali olarak desteklenmiştir.

Gül (Rosa damascena Mill.) Uçucu Yağının Pseudomonas aeruginosa’da Biyofilm Oluşumu ve Kayma Hareketi Üzerine Etkisi

Abstract

Pseudomonas aeruginosa, bağışıklığı baskılanmış hastalarda akut ve kronik enfeksiyonlara sebep olan Gram-negatif, fırsatçı bir patojendir. P. aeruginosa, virülens faktörlerinin üretimi ve biyofilm oluşturma özelliklerini bir çeşit hücreler arası iletişim sistemi olan çevreyi algılama (Quorum sensing, QS) haberleşme sistemi ile kontrol eder. Bu haberleşme sisteminin farklı sentetik veya doğal moleküller ile engellenmesi veya yönlendirilmesiyle patojen bakterilerin kontrolünü konu alan çalışmalar yapılmaktadır. İçerdiği aktif moleküller sayesinde antibakteriyel, antifungal ve antiviral aktivitelere sahip olan bitkisel uçucu yağlar bu anlamda büyük potansiyel taşımaktadır. Bu çalışmada gül uçucu yağının, gül uçucu yağının temel bileşenlerinin (sitronellol, geraniol ve nerol) ve bu üç bileşenin karışımının (CGN) Pseudomonas aeruginosa PA01 suşu için hücrelerarası iletişim (QS) sistemi üzerine engelleyici etkisi araştırılmıştır. Çalışma sonucunda P. aeruginosa PA01 suşu için kayma hareketini; gül uçucu yağının %83, sitronellol, geraniol, nerol ve karışım CGN’nin, %61-75 oranında engellediği belirlenmiştir. P. aeruginosa PA01 suşu için biyofilm oluşumunu, gül uçucu yağı %54-68, sitronellol, geraniol, nerol ve karışım CGN %10-15 oranında baskılamıştır. Gül uçucu yağının P. aeruginosa'nın kayma hareketini ve biyofilm oluşumunu gül yağının temel bileşenlerinden daha yüksek oranda inhibe etmesi önemlidir. Bu çalışmanın sonuçları, sitronellol, nerol, geraniol ve CGN'nin P. aeruginosa suşu için anti-QS aktivitesine sahip olduğunu, ancak gül uçucu yağının çeşitli uygulamalarda kullanılabilecek potansiyelinin bulunduğunu göstermektedir.

Keywords

Gül uçucu yağı, Biyofilm, P. aeruginosa, Kayma hareketi

Project Number

2776-YL-11

References

• [1] Willcox, M.D. (2007). Pseudomonas aeruginosa infection and inflammation during contact lens wear: A review. Optometry and Vision Science, 84(4), 273-278.
• [2] Church, D., Elsayed, S., Reid, O., Winston, B., Lindsay, R. (2006). Burn wound infections. Clinical Microbiology Reviews, 19(2), 403-434.
• [3] Klockgether, J., Tummler, B. (2017). Recent advances in understanding Pseudomonas aeruginosa as a pathogen. F1000Research, 6, 1261.
• [4] Hilliam, Y., Kaye, S., Winstanley, C. (2020). Pseudomonas aeruginosa and microbial keratitis. Journal of Medical Microbiology, 69(1), 3-13.
• [5] Aldawsari, M.F., Khafagy, E.S., Saqr, A.A., Alalaiwe, A., Abbas, H.A., Shaldam, M.A., Hegazy, W.A.H., Goda, R.M. (2021). Tackling virulence of Pseudomonas aeruginosa by the natural furanone sotolon. Antibiotics, 10(7), 871.
• [6] Hegazy, W.A.H., Khayat, M.T., Ibrahim, T.S., Nassar, M.S., Bakhrebah, M.A., Abdulaal, W.H., Alhakamy, N.A., Bendary, M.M. (2020). Repurposing anti-diabetic drugs to cripple quorum sensing in Pseudomonas aeruginosa. Microorganisms 8(9), 1285.
• [7] Valentini, M., Gonzalez, D., Mavridou, D.A., Filloux, A. (2018). Lifestyle transitions and adaptive pathogenesis of Pseudomonas aeruginosa. Current Opinion in Microbiology, 41, 15-20.
• [8] Pesci, E.C., Pearson, J.P., Seed, P.C., Iglewski, B.H. (1997). Regulation of las and rhl quorum sensing in Pseudomonas aeruginosa. Journal of bacteriology. 179(10), 3127-3132.
• [9] Déziel, E., Gopalan, S., Tampakaki, A.P., Lépine, F., Padfield, K.E., Saucier, M., Rahme, L.G. (2005). The contribution of MvfR to Pseudomonas aeruginosa pathogenesis and quorum sensing circuitry regulation: multiple quorum sensing‐regulated genes are modulated without affecting lasRI, rhlRI or the production of N‐acyl‐l‐homoserine lactones. Molecular Microbiology, 55(4), 998-1014.
• [10] Dubern, J.F., Diggle, S.P. (2008). Quorum sensing by 2-alkyl-4-quinolones in Pseudomonas aeruginosa and other bacterial species. Molecular Biosystems, 4(9), 882-888.
• [11] Lee, J., Zhang, L. (2015). The hierarchy quorum sensing network in Pseudomonas aeruginosa. Protein & Cell, 6(1), 26-41.
• [12] Rampioni, G., Falcone, M., Heeb, S., Frangipani, E., Fletcher, M.P., Dubern, J.F., Williams, P. (2016). Unravelling the genome-wide contributions of specific 2-alkyl-4-quinolones and PqsE to quorum sensing in Pseudomonas aeruginosa. PLoS pathogens, 12(11), e1006029.
• [13] Parsek, M.R., Greenberg, E.P. (2000). Acyl-homoserine lactone quorum sensing in gram-negative bacteria: a signaling mechanism involved in associations with higher organisms. Proceedings of the National Academy of Sciences, 97(16), 8789-8793.
• [14] Tuon, F.F., Dantas, L.R., Suss, P.H.,Tasca Ribeiro, V.S. (2022). Pathogenesis of the Pseudomonas aeruginosa biofilm: A review. Pathogens, 11(3), 300.
• [15] Mühlen, S., Dersch, P. (2016). Anti-virulence strategies to target bacterial infections. Curr Top Microbiol Immunol. 398, 147-183.
• [16] Kamal, A.A., Maurer, C.K., Allegretta, G., Haupenthal, J., Empting, M., Hartmann, R.W. (2018). Quorum sensing inhibitors as pathoblockers for Pseudomonas aeruginosa infections: a new concept in anti-infective drug discovery. Antibacterials, 2,185-210.
• [17] Bakkali, F., Averbeck, S., Averbeck, D., Idaomar, M. (2008). Biological effects of essential oils–a review. Food and Chemical Toxicology, 46(2), 446-475.
• [18] Luciardi, M.C., Blázquez, M.A., Alberto, M.R., Cartagena, E., Arena, M.E. (2021). Lemon oils attenuate the pathogenicity of Pseudomonas aeruginosa by quorum sensing inhibition. Molecules, 26(10), 2863.
• [19] Sobieszczańska, N., Myszka, K., Szwengiel, A., Majcher, M., Grygier, A., Wolko, Ł. (2020). Tarragon essential oil as a source of bioactive compounds with anti-quorum sensing and anti-proteolytic activity against Pseudomonas spp. isolated from fish–in vitro, in silico and in situ approaches. International Journal of Food Microbiology, 331, 108732.
• [20] Tomaś, N., Myszka, K., Wolko, Ł., Nuc, K., Szwengiel, A., Grygier, A., Majcher, M. (2021). Effect of black pepper essential oil on quorum sensing and efflux pump systems in the fish-borne spoiler Pseudomonas psychrophila KM02 identified by RNA-seq, RT-qPCR and molecular docking analyses. Food Control, 130, 108284.
• [21] Luciardi, M.C., Blázquez, M.A., Alberto, M.R., Cartagena, E., Arena, M.E. (2021). Lemon oils attenuate the pathogenicity of pseudomonas aeruginosa by quorum sensing inhibition. Molecules, 26(10), 2863.
• [22] D'Almeida, R.E., Sued, N., Arena, M.E. (2022). Citrus paradisi and Citrus reticulata essential oils interfere with Pseudomonas aeruginosa quorum sensing in vivo on Caenorhabditis elegans. Phytomedicine Plus, 2(1), 100160.
• [23] Mahmood, N., Piacente, S., Pizza, C., Burke, A., Khan, A. I., Hay, A.J. (1996). The anti-HIV activity and mechanisms of action of pure compounds isolated fromrosa damascena. Biochemical and Biophysical Research Communications, 229(1), 73-79.
• [24] Arıdoğan, B.C., Baydar, H., Kaya, S., Demirci, M., Ozbaşar, D., Mumcu, E., (2002). Antimicrobial activity and chemical composition of some essential oils. Archives of Pharmacal Resarch, 25(6), 860-864.
• [25] Ozkan, G., Sağdıc, O., Baydar, H., (2004). Antioxidant and antibacterial activities of Rosa damascena flower extracts. Food Science and Technology, 10(4), 277- 281.
• [26] Ulusoy, S., Boşgelmez-Tınaz, G., Secilmiş-Canbay, H., (2009). Tocopherol, carotene, phenolic contents and antibacterial properties rose essential oil, hydrosol and absolute. Current Microbiology, 59, 554-558.
• [27] Abdel-Hameed, M., Bertrand, R.L., Piercey-Normore, M.D., Sorensen, J.L. (2016). Putative identification of the usnic acid biosynthetic gene cluster by de novo whole-genome sequencing of a lichen-forming fungus. Fungal Biology, 120(3), 306-316.
• [28] Zu Y, Yu H, Liang L, Fu Y, Efferth T, Liu X, Wu N. (2010). Activities of ten essential oils towards Propionibacterium acnes and PC-3, A-549 and MCF-7 cancer cells. Molecules, 15(5), 3200-10.
• [29] Achuthan, C.R., Babu, B.H., Padikkala, J. (2003). Antioxidant and hepatoprotective effects of Rosa damascena. Pharmaceutical Biology, 41(5), 357-361.
• [30] Kumar, N., Bhandari, P., Singh, B., Bari, S. S. (2009). Antioxidant activity and ultra-performance LC-electrospray ionization-quadrupole time-of-flight mass spectrometry for phenolics-based fingerprinting of Rose species: Rosa damascena, Rosa bourboniana and Rosa brunonii. Food and Chemical Toxicology, 47(2), 361-367.
• [31] Adonizio, A., Kong, K.F., Mathee, K. (2008). Inhibition of quorum sensing-controlled virulence factor production in Pseudomonas aeruginosa by South Florida plant extracts. Antimicrobial Agents and Chemotherapy, 52(1), 198-203.
• [32] Pereira, L.A.S., Oliveira, M.M.M.D., Martins, H.H.D.A., Vale, L.A.D., Isidoro, S.R., Botrel, D.A., Piccoli, R.H. (2019). Sanitizing cinnamaldehyde solutions against Pseudomonas aeruginosa biofilms formed on stainless steel surfaces. Brazilian Journal of Food Technology, 22.
• [33] Mohammed, M.H., Farghaly, R.M., Abdel-Aziz, N.M. (2023). The effect of some essential oils against biofilm producing Pseudomonas aeruginosa of meat sources. SVU-International Journal of Veterinary Sciences, 6(1), 100-115.
• [34] Zhang, X.S., García-Contreras, R., Wood, T.K. (2008). Escherichia coli transcription factor YncC (McbR) regulates colanic acid and biofilm formation by repressing expression of periplasmic protein YbiM (McbA). The ISME Journal, 2(6), 615-631.
• [35] Rashid, M.H., Kornberg, A. (2000). Inorganic polyphosphate is needed for swimming, swarming, and twitching motilities of Pseudomonas aeruginosa. Proceedings of the National Academy of Sciences. 97(9), 4885-4890.
• [36] Wagner, V.E., Li, L.L., Isabella, V.M., Iglewski, B.H. (2007). Analysis of the hierarchy of quorum-sensing regulation in Pseudomonas aeruginosa. Analytical and Bioanalytical Chemistry. 387(2), 469-479.
• [37] Boucher, H.W., Talbot, G.H., Bradley, J.S., Edwards, J.E., Gilbert, D., Rice, L.B. (2009). bad bugs, no drugs: no ESKAPE! An update from the Infectious Diseases Society of America. Clin Infect Dis. 48(1), 1-12.
• [38] Vijayakumar, K., Ramanathan, T. (2020). Musa acuminata and its bioactive metabolite 5-Hydroxymethylfurfural mitigates quorum sensing (las and rhl) mediated biofilm and virulence production of nosocomial pathogen Pseudomonas aeruginosa in vitro. Journal of Ethnopharmacology, 246, 112242.
• [39] Casciaro, B., Lin, Q., Afonin, S., Loffredo, M.R., de Turris, V., Middel, V., Mangoni, M.L. (2019). Inhibition of Pseudomonas aeruginosa biofilm formation and expression of virulence genes by selective epimerization in the peptide Esculentin‐1a (1‐21) NH 2. The FEBS Journal, 286(19), 3874-3891.
• [40] Darzins, A. (1994). Characterization of a Pseudomonas aeruginosa gene cluster involved in pilus biosynthesis and twitching motility: sequence similarity to the chemotaxis proteins of enterics and the gliding bacterium Myxococcus xanthus. Molecular Microbiology, 11(1), 137-153.
• [41] Norizan, S., Yin, W.F. (2013). Chan, K.G., Caffeine as a potential quorum sensing inhibitor. Sensors, 13(4), 5117-5129.
• [42] Gupta, R.K., Setia, S., Harjai, K. (2011). Expression of quorum sensing and virulence factors are interlinked in Pseudomonas aeruginosa: an in vitro approach. Am J Biomed Sci., 3(2), 116-125.
• [43] Zhang, Y., Kong, J., Xie, Y., Guo, Y., Cheng, Y., Qian, H., Yao, W. (2018). Essential oil components inhibit biofilm formation in Erwinia carotovora and Pseudomonas fluorescens via anti-quorum sensing activity. LWT, 92,133-139.
• [44] Heydorn, A., Ersbøll,. B, Kato, J., Hentzer, M., Parsek, M.R., Tolker-Nielsen, T., Molin, S. (2002). Statistical analysis of Pseudomonas aeruginosa biofilm development: impact of mutations in genes involved in twitching motility, cell-to-cell signaling, and stationary-phase sigma factor expression. Applied and Environmental Microbiology, 68(4), 2008-2017.
• [45] Sivri, E.D., Ulusoy, S. (2018). Reduction of tissue maceration in potatoes by rose essential oil. Akademik Gıda, 16(2), 127-134.
• [46] Soković, M., Glamočlija, J., Marin, P.D., Brkić, D., van Griensven, L.J. (2010). Antibacterial effects of the essential oils of commonly consumed medicinal herbs using an in vitro model. Molecules, 15(11), 7532-7546.