The Molecular Mechanisms of the Antibacterial Activity of Sumac (Rhus typhina L.) Tannin Against Pseudomonas aeruginosa
Source abstract
Abstract
Treatment of infections caused by Pseudomonas aeruginosa presents a challenge due to its ability to adapt and acquire drug resistance rapidly. Therefore, a key challenge is identifying and investigating new compounds with antibacterial and anti-virulence activity. Tannins, a group of plant polyphenolic compounds, can interact with bacterial cells and their virulence factors. The purpose of this study was to assess the antibacterial potential of using 3,6-bis-O-di-O-galloyl-1,2,4-tri-O-galloyl-β-D-glucose (C55H40O34) isolated from Rhus typhina against P. aeruginosa ATCC BAA-1744. The investigation involved viability analyses using the INT assay, fluorescence analyses of the tannins’ interaction with the cell membrane and membrane proteins of P. aeruginosa, and analysis of changes in the Zeta potential. The results obtained allowed us to conclude that C55H40O34 exhibits antimicrobial activity by inducing changes in the biophysical properties of P. aeruginosa’s cell membrane. The thermodynamic parameters indicated that C55H40O34 binds to bacterial membrane proteins through hydrophobic interactions. These interactions with proteins may impact their structure and disrupt their functions, such as disturbing or inhibiting the efflux pumps, which are part of P. aeruginosa’s resistance mechanisms. Therefore, C55H40O34 may be a new, natural agent and could potentially be used against P. aeruginosa.
Source: crossref · Quality: baseline
Research context
OpenAlex topics: Medicinal Plant Research · Essential Oils and Antimicrobial Activity · Natural product bioactivities and synthesis
SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.
Affiliations
Doctoral School, University of Bialystok, 15-254 Bialystok, Poland
Laboratory of Molecular Biophysics, Department of Microbiology and Biotechnology, Faculty of Biology, University of Bialystok, 15-254 Bialystok, Poland
Institute of Bioorganic Chemistry, Academy of Sciences of the Republic of Uzbekistan, Tashkent 100143, Uzbekistan
References (46)
Show source-provided references
1. Pseudomonas aeruginosa: Infections and Novel Approaches to Treatment “Knowing the Enemy” the Threat of Pseudomonas aeruginosa and Exploring Novel Approaches to Treatment10.1016/j.imj.2023.05.003 ↗
2. Giovagnorio, F., De Vito, A., Madeddu, G., Parisi, S.G., and Geremia, N. (2023). Resistance in Pseudomonas aeruginosa: A Narrative Review of Antibiogram Interpretation and Emerging Treatments. Antibiotics, 12.10.3390/antibiotics12111621 ↗
3. Thi, M.T.T., Wibowo, D., and Rehm, B.H.A. (2020). Pseudomonas aeruginosa Biofilms. Int. J. Mol. Sci., 21.10.3390/ijms21228671 ↗
4. Qin, S., Xiao, W., Zhou, C., Pu, Q., Deng, X., Lan, L., Liang, H., Song, X., and Wu, M. (2022). Pseudomonas aeruginosa: Pathogenesis, Virulence Factors, Antibiotic Resistance, Interaction with Host, Technology Advances and Emerging Therapeutics. Signal. Transduct. Target Ther., 7.10.1038/s41392-022-01056-1 ↗
5. Pseudomonas aeruginosa: All Roads Lead to Resistance10.1016/j.tim.2011.04.005 ↗
6. Antibiotic Resistance in Pseudomonas aeruginosa: Mechanisms and Alternative Therapeutic Strategies10.1016/j.biotechadv.2018.11.013 ↗
7. The Mortality Burden of Multidrug-Resistant Pathogens in India: A Retrospective, Observational Study10.1093/cid/ciy955 ↗
8. Chambers, J.R., Cherny, K.E., and Sauer, K. (2017). Susceptibility of Pseudomonas aeruginosa Dispersed Cells to Antimicrobial Agents Is Dependent on the Dispersion Cue and Class of the Antimicrobial Agent Used. Antimicrob. Agents Chemother., 61.10.1128/AAC.00846-17 ↗
9. Liao, C., Huang, X., Wang, Q., Yao, D., and Lu, W. (2022). Virulence Factors of Pseudomonas aeruginosa and Antivirulence Strategies to Combat Its Drug Resistance. Front. Cell. Infect. Microbiol., 12.10.3389/fcimb.2022.926758 ↗
10. Ceftolozane–Tazobactam: A New-Generation Cephalosporin10.2146/ajhp150049 ↗
11. Olchowik-Grabarek, E., Sekowski, S., Bitiucki, M., Dobrzynska, I., Shlyonsky, V., Ionov, M., Burzynski, P., Roszkowska, A., Swiecicka, I., and Abdulladjanova, N. (2020). Inhibition of Interaction between Staphylococcus aureus α-Hemolysin and Erythrocytes Membrane by Hydrolysable Tannins: Structure-Related Activity Study. Sci. Rep., 10.10.1038/s41598-020-68030-1 ↗
12. Attenuation of Quorum Sensing Controlled Virulence Factors and Biofilm Formation in Pseudomonas aeruginosa by Pentacyclic Triterpenes, Betulin and Betulinic Acid10.1016/j.micpath.2018.03.012 ↗
13. Identification of Catechin as One of the Flavonoids from Combretum Albiflorum Bark Extract That Reduces the Production of Quorum-Sensing-Controlled Virulence Factors in Pseudomonas aeruginosa PAO110.1128/AEM.01059-09 ↗
14. Tea Polyphenols Inhibit Pseudomonas aeruginosa through Damage to the Cell Membrane10.1016/j.ijfoodmicro.2010.09.005 ↗
15. Antimicrobial and Antiviral Activity of Hydrolysable Tannins10.2174/138955708786140990 ↗
16. Czerkas, K., Olchowik-Grabarek, E., Łomanowska, M., Abdulladjanova, N., and Sękowski, S. (2024). Antibacterial Activity of Plant Polyphenols Belonging to the Tannins against Streptococcus Mutans—Potential against Dental Caries. Molecules, 29.10.3390/molecules29040879 ↗
17. Kaczmarek, B. (2020). Tannic Acid with Antiviral and Antibacterial Activity as A Promising Component of Biomaterials—A Minireview. Materials, 13.10.3390/ma13143224 ↗
18. Štumpf, S., Hostnik, G., Langerholc, T., Pintarič, M., Kolenc, Z., and Bren, U. (2023). The Influence of Chestnut Extract and Its Components on Antibacterial Activity against Staphylococcus aureus. Plants, 12.10.3390/plants12102043 ↗
19. Olchowik-Grabarek, E., Sękowski, S., Kwiatek, A., Płaczkiewicz, J., Abdulladjanova, N., Shlyonsky, V., Swiecicka, I., and Zamaraeva, M. (2022). The Structural Changes in the Membranes of Staphylococcus aureus Caused by Hydrolysable Tannins Witness Their Antibacterial Activity. Membranes, 12.10.3390/membranes12111124 ↗
20. Olchowik-Grabarek, E., Sekowski, S., Mies, F., Bitiucki, M., Swiecicka, I., Abdulladjanova, N., Shlyonsky, V., and Zamaraeva, M. (2023). Electrophysiological and Spectroscopic Investigation of Hydrolysable Tannins Interaction with α-Hemolysin of S. aureus. Bioelectrochemistry, 150.10.1016/j.bioelechem.2022.108318 ↗
21. (2024, November 06). Available online: https://www.invasive.org/browse/subinfo.cfm?sub=3950#references.
22. Specificity of Hy-drolysable Tannins from Rhus typhina L. to Oxidants in Cell and Cell-Free Models10.1007/s12010-016-2226-1 ↗
23. Sekowski, S., Naziris, N., Chountoulesi, M., Olchowik-Grabarek, E., Czerkas, K., Veiko, A., Abdulladjanova, N., Demetzos, C., and Zamaraeva, M. (2023). Interaction of Rhus typhina Tannin with Lipid Nanoparticles: Implication for the Formulation of a Tannin–Liposome Hybrid Biomaterial with Antibacterial Activity. J. Funct. Biomater., 14.10.3390/jfb14060296 ↗
24. Lakowicz, J.R., and Masters, B.R. (2008). Principles of Fluorescence Spectroscopy, Third Edition. J. Biomed. Opt., 13.10.1117/1.2904580 ↗
25. The Interaction of Sonochemically Synthesized Gold Nanoparticles with Serum albumins10.1016/j.jpba.2010.03.039 ↗
26. Spectroscopic Analysis on the Binding Interaction of Biologically Active Pyrimidine Derivative with Bovine Serum albumin10.1016/j.jpha.2015.07.001 ↗
27. Antioxidant and Antimicrobial Activity of Seed from Plants of the Mississippi River Basin
28. Antimicrobial Activity of Natural Products from the Flora of Northern Ontario, Canada10.3109/13880209.2014.942867 ↗
29. Alsamri, H., Athamneh, K., Pintus, G., Eid, A.H., and Iratni, R. (2021). Pharmacological and Antioxidant Activities of Rhus coriaria L. (Sumac). Antioxidants, 10.10.3390/antiox10010073 ↗
30. Trentin, D.S., Silva, D.B., Amaral, M.W., Zimmer, K.R., Silva, M.V., Lopes, N.P., Giordani, R.B., and Macedo, A.J. (2013). Tannins Possessing Bacteriostatic Effect Impair Pseudomonas aeruginosa Adhesion and Biofilm Formation. PLoS ONE, 8.10.1371/journal.pone.0066257 ↗
31. Virtanen, V., Green, R.J., and Karonen, M. (2022). Interactions between Hydrolysable Tannins and Lipid Vesicles from Escherichia coli with Isothermal Titration Calorimetry. Molecules, 27.10.3390/molecules27103204 ↗
32. Biomolecular Interactions of Tannin Isolated from Oenothera gigas with Liposomes10.1007/s00232-015-9858-x ↗
33. Ivanov, M., Novović, K., Malešević, M., Dinić, M., Stojković, D., Jovčić, B., and Soković, M. (2022). Polyphenols as Inhibitors of Antibiotic Resistant Bacteria—Mechanisms Underlying Rutin Interference with Bacterial Virulence. Pharmaceuticals, 15.10.3390/ph15030385 ↗
34. Getting Across the Cell Membrane: An Overview for Small Molecules, Peptides, and Proteins10.1007/978-1-4939-2272-7_3 ↗
35. Sekowski, S., Veiko, A., Olchowik-Grabarek, E., Dubis, A., Wilczewska, A.Z., Markiewicz, K.H., Zavodnik, I.B., Lapshina, E., Dobrzynska, I., and Abdulladjanova, N. (2022). Hydrolysable Tannins Change Physicochemical Parameters of Lipid Nano-Vesicles and Reduce DPPH Radical—Experimental Studies and Quantum Chemical Analysis. Biochim. Biophys. Acta (BBA) Biomembr., 1864.10.1016/j.bbamem.2021.183778 ↗
36. Action of Tannin on Cellular Membranes: Novel Insights from Concerted Studies on Lipid Bilayers and Native Cells10.1016/j.bbamem.2019.03.017 ↗
37. Mattio, L.M., Dallavalle, S., Musso, L., Filardi, R., Franzetti, L., Pellegrino, L., D’Incecco, P., Mora, D., Pinto, A., and Arioli, S. (2019). Antimicrobial Activity of Resveratrol-Derived Monomers and Dimers against Foodborne Pathogens. Sci. Rep., 9.10.1038/s41598-019-55975-1 ↗
38. Cholesterol Lipids and Cholesterol-Containing Lipid Rafts in Bacteria10.1016/j.chemphyslip.2016.03.002 ↗
39. Flavonoid–Serum Albumin Complexation: Determination of Binding Constants and Binding Sites by Fluorescence Spectroscopy10.1016/j.bbagen.2004.10.013 ↗
40. Surfactants: Physicochemical Interactions with Biological Macromolecules10.1007/s10529-020-03054-1 ↗
41. The Role of Interactions in Defining the Structure of Mixed Protein–Surfactant Interfaces10.1016/j.cis.2005.04.002 ↗
42. Staring at Protein-Surfactant Interactions: Fundamental Approaches and Comparative Evaluation of Their Combinations—A Review10.1016/j.aca.2019.02.024 ↗
43. Feng, Y., Jin, C., Lv, S., Zhang, H., Ren, F., and Wang, J. (2023). Molecular Mechanisms and Applications of Polyphenol-Protein Complexes with Antioxidant Properties: A Review. Antioxidants, 12.10.3390/antiox12081577 ↗
44. Zhang, L., Wang, P., Yang, Z., Du, F., Li, Z., Wu, C., Fang, A., Xu, X., and Zhou, G. (2020). Molecular Dynamics Simulation Exploration of the Interaction between Curcumin and Myosin Combined with the Results of Spectroscopy Techniques. Food Hydrocoll., 101.10.1016/j.foodhyd.2019.105455 ↗
45. Ferreyra Maillard, A.P.V., Espeche, J.C., Maturana, P., Cutro, A.C., and Hollmann, A. (2021). Zeta Potential beyond Materials Science: Applications to Bacterial Systems and to the Development of Novel Antimicrobials. Biochim. Biophys. Acta (BBA) Biomembr., 1863.10.1016/j.bbamem.2021.183597 ↗
46. Effects of Natural Antimicrobials on Bacterial Cell Hydrophobicity, Adhesion, and Zeta Potential/Vpliv Naravnih Protimikrobnih Snovi Na Bakterijsko Hidrofobnost, Adhezijo in Zeta Potencial