Antimicrobial, Antibiofilm and Antiurease Activities of Microbially Synthesized Silver Nanoparticles against Proteus mirabilis

Yıl 2023, Cilt: 28 Sayı: 2, 359 - 369, 31.08.2023

Sümeyra Gürkök , Murat Özdal

https://doi.org/10.53433/yyufbed.1194875

Cited By: 1

Öz

Nanoparticles (NPs) are tiny materials ranging in size from 1 to 100 nm and have unique magnetic, electrical, and optical characteristics differing from bulk materials. They have a broad spectrum of applications in different industries. Several physical and chemical techniques have been applied to produce metal NPs. Alternatively, green synthesis offers an environmentally friendly and simple means for NP preparation. In the present study, silver NPs were produced by the Pseudomonas aeruginosa OG1 strain. Characterization of NPs was performed by TEM, SEM, and XRD. These NPs were used against pathogenic Proteus mirabilis, which shows high-level urease activity and forms clear biofilms. Silver NPs obtained in the present study were applied to inhibit the growth, urease production, and biofilm formation of P. mirabilis. Growth inhibition zones of 9 mm and 11 mm and, 60 % and 85% antibiofilm effects were obtained by 100 µg mL-1 and 200 µg mL-1 NPs, respectively. The urease activity of P. mirabilis was completely inhibited in both concentrations. These results show that AgNPs can be used as effective antimicrobial, antibiofilm, and antiurease agents in the fight against pathogens.

Anahtar Kelimeler

Antibiofilm, Antimicrobial, Antiurease, Nanoparticles, P. aeruginosa Proteus mirabilis, Silver

Destekleyen Kurum

Atatürk University

Proje Numarası

No grant number

Teşekkür

This research was supported by Ataturk University (No grant number).

Mikrobiyal Olarak Sentezlenen Gümüş Nanopartiküllerin Proteus mirabilis'e Karşı Antimikrobiyal, Antibiyofilm ve Antiüreaz Aktiviteleri

Öz

Nanopartiküller (NP), 1 ila 100 nm arasında değişen küçük malzemelerdir ve bulk malzemelerden farklı benzersiz manyetik, elektriksel, optik özelliklere sahiptir. Farklı endüstrilerde geniş bir uygulama alanlarına sahiptirler. Metal NP'leri üretmek için çeşitli fiziksel ve kimyasal teknikler uygulanmıştır. Alternatif olarak, yeşil sentez, NP hazırlama için çevre dostu ve basit bir yol sunar. Bu çalışmada, gümüş NP'ler Pseudomonas aeruginosa OG1 suşu tarafından üretilmiştir. NP'lerin karakterizasyonu TEM, SEM ve XRD ile yapılmıştır. Bu NP'ler, yüksek düzeyde üreaz aktivitesi gösteren ve berrak biyofilmler oluşturan patojenik Proteus mirabilis'e karşı kullanılmıştır. Bu çalışmada elde edilen gümüş NP'ler P. mirabilis'in büyümesini, üreaz üretimini ve biyofilm oluşumunu engellemek için uygulanmıştır. Sırasıyla 100 µg mL-1 ve 200 µg mL-1 konsantrasyonlardaki NP'lerle 9 mm ve 11 mm'lik büyüme inhibisyon bölgeleri ve %60 ve %85 antibiyofilm etkileri elde edildi. P. mirabilis'in üreaz aktivitesi her iki konsantrasyonda da tamamen inhibe edilmiştir. Bu sonuçlar, AgNP'lerin patojenlerle mücadelede etkili antimikrobiyal, antibiyofilm ve antiüreaz ajanları olarak kullanılabileceğini göstermektedir.

Anahtar Kelimeler

Antibiyofilm, Antimikrobiyal, Antiüreaz, Gümüş, Nanopartiküller, P. aeruginosa Proteus mirabilis

Proje Numarası

No grant number

Kaynakça

• Abdo, A. M., Fouda, A., Eid, A. M., Fahmy, N. M., Elsayed, A. M., Khalil, A. M. A., ... & Soliman, A. M. (2021). Green synthesis of Zinc Oxide Nanoparticles (ZnO-NPs) by Pseudomonas aeruginosa and their activity against pathogenic microbes and common house mosquito, Culex pipiens. Materials, 14(22), 6983. doi:10.3390/ma14226983
• Abdulkareem, M. A., Joudi, M. S., & Ali, A. H. (2022). Eco-friendly synthesis of low-cost antibacterial agent (brown attapulgite-Ag nanocomposite) for environmental application. Chemical Data Collections, 37, 100814. doi:10.1016/j.cdc.2021.100814
• Abeer Mohammed, A. B., Abd Elhamid, M. M., Khalil, M. K. M., Ali, A. S., & Abbas, R. N. (2022). The potential activity of biosynthesized silver nanoparticles of Pseudomonas aeruginosa as an antibacterial agent against multidrug-resistant isolates from intensive care unit and anticancer agent. Environmental Sciences Europe, 34(1), 109. doi:10.1186/s12302-022-00684-2
• Ahmad, F., Ashraf, N., Ashraf, T., Zhou, R.-B., & Yin, D.-C. (2019). Biological synthesis of metallic nanoparticles (MNPs) by plants and microbes: their cellular uptake, biocompatibility, and biomedical applications. Applied Microbiology and Biotechnology, 103(7), 2913-2935. doi:10.1007/s00253-019-09675-5
• Alavi, M., & Varma, R. S. (2021). Phytosynthesis and modification of metal and metal oxide nanoparticles/nanocomposites for antibacterial and anticancer activities: Recent advances. Sustainable Chemistry and Pharmacy, 21, 100412. doi:10.1016/j.scp.2021.100412
• Ali, S., Bacha, M., Shah, M. R., Shah, W., Kubra, K., Khan, A., Ahmad, M., Latif, A., Ali, M. (2021). Green synthesis of silver and gold nanoparticles using Crataegus oxyacantha extract and their urease inhibitory activities. Biotechnology and Applied Biochemistry, 68(5), 992-1002. doi:10.1002/bab.2018
• Ashraf, H., Meer, B., Iqbal, J., Ali, J. S., Andleeb, A., Butt, H., … & Abbasi, B. H. (2023). Comparative evaluation of chemically and green synthesized zinc oxide nanoparticles: their in vitro antioxidant, antimicrobial, cytotoxic and anticancer potential towards HepG2 cell line. Journal of Nanostructure in Chemistry, 13, 243-261. doi:10.1007/s40097-021-00460-3
• Bai, J-R., Zhong, K., Wu, Y-P., Elena, G., & Gao, H. (2019). Antibiofilm activity of shikimic acid against Staphylococcus aureus. Food Control, 95, 327-333. doi:10.1016/j.foodcont.2018.08.020
• Bauer, A. W., Kirby, W. M., Sherris, J. C., & Turck, M. (1966). Antibiotic susceptibility testing by a standardized single disk method. Technical Bulletin of the Registry of Medical Technologists, 36(3), 49-52. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/5908210
• Bharathi, D., Vasantharaj, S., & Bhuvaneshwari, V. (2018). Green synthesis of silver nanoparticles using Cordia dichotoma fruit extract and its enhanced antibacterial, anti-biofilm and photo catalytic activity. Materials Research Express, 5(5), 055404. doi:10.1088/2053-1591/aac2ef
• Çakıcı, T., Özdal, M., Kundakcı, M., & Kayalı, R. (2019). ZnSe and CuSe NP’s by microbial green synthesis method and comparison of I-V characteristics of Au/ZnSe/p-Si/Al and Au/CuSe/p-Si/Al structures. Materials Science in Semiconductor Processing, 103, 104610. doi:10.1016/j.mssp.2019.104610
• Chandrakar, V., Tapadia, K., & Gupta, S. K. (2021). Greener production of silver nanoparticles: a sensitive nanodrop spectrophotometric determination of biothiols. Chemical Papers, 75(7), 3327-3336. doi:10.1007/s11696-021-01565-3
• Chandrasekharan, S., Chinnasamy, G., & Bhatnagar, S. (2022). Sustainable phyto-fabrication of silver nanoparticles using Gmelina arborea exhibit antimicrobial and biofilm inhibition activity. Scientific Reports, 12(1), 156. doi:10.1038/s41598-021-04025-w
• Dong, Z. Y., Narsing Rao, M. P., Xiao, M., Wang, H. F., Hozzein, W. N., Chen, W., & Li, W. J. (2017). Antibacterial activity of silver nanoparticles against Staphylococcus warneri synthesized using endophytic bacteria by photo-irradiation. Frontiers in Microbiology, 8, 1090. doi:10.3389/fmicb.2017.01090
• Doriya, K., & Kumar, D. S. (2016). Isolation and screening of L-asparaginase free of glutaminase and urease from fungal sp. 3 Biotech, 6(2), 239. doi:10.1007/s13205-016-0544-1
• Elbahnasawy, M. A., Shehabeldine, A. M., Khattab, A. M., Amin, B. H., & Hashem, A. H. (2021). Green biosynthesis of silver nanoparticles using novel endophytic Rothia endophytica: Characterization and anticandidal activity. Journal of Drug Delivery Science and Technology, 62, 102401. doi:10.1016/j.jddst.2021.102401
• Elnady, A., Sorour, N. M., & Abbas, R. N. (2022). Characterization, cytotoxicity, and genotoxicity properties of novel biomediated nanosized-silver by Egyptian Streptomyces roseolus for safe antimicrobial applications. World Journal of Microbiology and Biotechnology, 38(3), 47. doi:10.1007/s11274-022-03231-6
• Hu, X., Wu, L., Du, M., & Wang, L. (2022). Eco-friendly synthesis of size-controlled silver nanoparticles by using Areca catechu nut aqueous extract and investigation of their potent antioxidant and anti-bacterial activities. Arabian Journal of Chemistry, 15(5), 103763. doi:10.1016/j.arabjc.2022.103763
• Hussein, A. A., & Alsharifi, M. R. (2021). Antimicrobial activity of silver nanoparticles against Proteus mirabilis isolated from patients with food diabetes ulcer. Caspian Journal of Environmental Sciences, 19(5), 853-860. doi:10.22124/cjes.2021.5243
• Husseiny, M. I., Abd El-Aziz, M., Badr, Y., & Mahmoud, M. A. (2007). Biosynthesis of gold nanoparticles using Pseudomonas aeruginosa. Spectrochimica Acta Part A: Molecular and Biomolecular Spectroscopy, 67(3-4), 1003-1006. doi:10.1016/j.saa.2006.09.028
• John, M. S., Nagoth, J. A., Ramasamy, K. P., Mancini, A., Giuli, G., Natalello, A., … & Pucciarelli, S. (2020). Synthesis of bioactive silver nanoparticles by a Pseudomonas strain associated with the antarctic psychrophilic protozoon Euplotes focardii. Marine Drugs, 18(1), 38. doi:10.3390/md18010038
• Kapoor, R. T., Salvadori, M. R., Rafatullah, M., Siddiqui, M. R., Khan, M. A., & Alshareef, S. A. (2021). Exploration of microbial factories for synthesis of nanoparticles – A sustainable approach for bioremediation of environmental contaminants. Frontiers in Microbiology, 12, 658294. doi:10.3389/fmicb.2021.658294
• Khan, S. T., Malik, A., Wahab, R., Abd-Elkader, O. H., Ahamed, M., Ahmad, J., … & Al-Khedhairy, A. A. (2017). Synthesis and characterization of some abundant nanoparticles, their antimicrobial and enzyme inhibition activity. Acta Microbiologica et Immunologica Hungarica, 64(2), 203-216. doi:10.1556/030.64.2017.004
• Khan, F., Kang, M.-G., Jo, D.-M., Chandika, P., Jung, W.-K., Kang, H. W., & Kim, Y.-M. (2021). Phloroglucinol-gold and -zinc oxide nanoparticles: Antibiofilm and antivirulence activities towards Pseudomonas aeruginosa PAO1. Marine Drugs, 19(11), 601. doi:10.3390/md19110601
• Khan, U., Arshad, N., Sultana, R., Hashim, J., Sheikh, H., Zaidi, W., & Khan, S. (2022). Synthesis of dihydropyrimidine stabilized silver nanoparticles with significant anti urease and catalytic applications. Pakistan Journal of Pharmaceutical Sciences, 35(3 (Special)), 923-930.
• Khandel, P., & Shahi, S. K. (2018). Mycogenic nanoparticles and their bio-prospective applications: Current status and future challenges. Journal of Nanostructure in Chemistry, 8(4), 369-391. doi:10.1007/s40097-018-0285-2
• Koul, B., Poonia, A. K., Yadav, D., & Jin, J. O. (2021). Microbe-mediated biosynthesis of nanoparticles: Applications and future prospects. Biomolecules, 11(6), 886. doi:10.3390/biom11060886
• Lange, A., Grzenia, A., Wierzbicki, M., Strojny-Cieslak, B., Kalińska, A., Gołębiewski, M., ... & Jaworski, S. (2021). Silver and copper nanoparticles inhibit biofilm formation by mastitis pathogens. Animals, 11(7), 1884. doi:10.3390/ani11071884
• Lashin, I., Fouda, A., Gobouri, A. A., Azab, E., Mohammedsaleh, Z. M., & Makharita, R. R. (2021). Antimicrobial and in vitro cytotoxic efficacy of biogenic silver nanoparticles (Ag-NPs) fabricated by callus extract of Solanum incanum L. Biomolecules, 11(3), 341. doi:10.3390/biom11030341
• Lee, N. Y., Ko, W. C., & Hsueh, P. R. (2019). Nanoparticles in the treatment of infections caused by multidrug-resistant organisms. Frontiers in Pharmacology, 10, 1-10. doi:10.3389/fphar.2019.01153
• Loharch, S., & Berlicki, Ł. (2022). Rational development of bacterial ureases inhibitors. The Chemical Record, 22(8), e202200026. doi:10.1002/tcr.202200026
• Loo, Y. Y., Rukayadi, Y., Nor-Khaizura, M. A. R., Kuan, C. H., Chieng, B. W., Nishibuchi, M., & Radu, S. (2018). In vitro antimicrobial activity of green synthesized silver nanoparticles against selected gram-negative foodborne pathogens. Frontiers in Microbiology, 9, 1555. doi:10.3389/fmicb.2018.01555
• Maniraj, A., Kannan, M., Rajarathinam, K., Vivekanandhan, S., & Muthuramkumar, S. (2019). Green synthesis of silver nanoparticles and their effective utilization in fabricating functional surface for antibacterial activity against multi-drug resistant Proteus mirabilis. Journal of Cluster Science, 30, 1403-1414. doi:10.1007/s10876-019-01582-z
• Mohamed, A. A., Abu-Elghait, M., Ahmed, N. E., & Salem, S. S. (2021). Eco-friendly mycogenic synthesis of ZnO and CuO nanoparticles for in vitro antibacterial, antibiofilm, and antifungal applications. Biological Trace Element Research, 199(7), 2788-2799. doi:10.1007/s12011-020-02369-4
• Mohanta, Y. K., Biswas, K., Jena, S. K., Hashem, A., Abd_Allah, E. F., & Mohanta, T. K. (2020). Anti-biofilm and antibacterial activities of silver nanoparticles synthesized by the reducing activity of phytoconstituents present in the Indian medicinal plants. Frontiers in Microbiology, 11, 1143. doi:10.3389/fmicb.2020.01143
• Morou-Bermudez, E., Rodriguez, S., Bello, A. S., & Dominguez-Bello, M. G. (2015). Urease and dental plaque microbial profiles in children. PLOS One, 10(9), e0139315. doi:10.1371/journal.pone.0139315
• Ozdal, M., Ozdal, O. G., & Algur, O. F. (2016). Isolation and characterization of α-Endosulfan degrading bacteria from the microflora of cockroaches. Polish Journal of Microbiology, 65(1), 63-68. doi:10.5604/17331331.1197325
• Ozdal, M., & Gurkok, S. (2022a). Recent advances in nanoparticles as antibacterial agent. ADMET and DMPK. 10(2), 115-129. doi:10.5599/admet.1172
• Ozdal, M., & Gurkok, S. (2022b). Mechanisms of Nanoparticles Biosynthesis by Microorganisms. In T. Çakıcı (Ed.), The Trends in Nano Materials Synthesis and Applications (pp. 81-98). İstanbul, Türkiye: Efe Academy.
• Pernas-Pleite, C., Conejo-Martínez, A. M., Marín, I., & Abad, J. P. (2022). Green extracellular synthesis of silver nanoparticles by Pseudomonas alloputida, their growth and biofilm-formation inhibitory activities and synergic behavior with three classical antibiotics. Molecules, 27(21), 7589. doi:10.3390/molecules27217589
• Ponnuvel, S., Subramanian, B., & Ponnuraj, K. (2015). Conformational change results in loss of enzymatic activity of jack bean urease on its interaction with silver nanoparticle. The Protein Journal, 34(5), 329-337. doi:10.1007/s10930-015-9627-9
• Sajjad, A., Bhatti, S. H., Ali, Z., Jaffari, G. H., Khan, N. A., Rizvi, Z. F., & Zia, M. (2021). Photoinduced fabrication of zinc oxide nanoparticles: Transformation of morphological and biological response on light irradiance. ACS Omega, 6(17), 11783-11793. doi:10.1021/acsomega.1c01512
• Salem, S. S., Badawy, M. S. E. M., Al-Askar, A. A., Arishi, A. A., Elkady, F. M., & Hashem, A. H. (2022). Green biosynthesis of selenium nanoparticles using orange peel waste: Characterization, antibacterial and antibiofilm activities against multidrug-resistant bacteria. Life, 12(6), 893. doi:10.3390/life12060893
• Seo, M., Oh, T., & Bae, S. (2021). Antibiofilm activity of silver nanoparticles against biofilm forming Staphylococcus pseudintermedius isolated from dogs with otitis externa. Veterinary Medicine and Science, 7(5), 1551-1557. doi:10.1002/vms3.554
• Shah, M., Fawcett, D., Sharma, S., Tripathy, S. K., & Poinern, G. E. J. (2015). Green synthesis of metallic nanoparticles via biological entities. Materials, 8(11), 7278-7308. doi:10.3390/ma8115377
• Sharifi-Rad, M., Pohl, P., & Epifano, F. (2021). Phytofabrication of silver nanoparticles (AgNPs) with pharmaceutical capabilities using Otostegia persica (Burm.) Boiss. leaf extract. Nanomaterials, 11(4), 1045. doi:10.3390/nano11041045
• Singh, P., Kim, Y.-J., Zhang, D., & Yang, D.-C. (2016). Biological synthesis of nanoparticles from plants and microorganisms. Trends in Biotechnology, 34(7), 588-599. doi:10.1016/j.tibtech.2016.02.006
• Ullah, R., Azam, A., Aziz, T., Farhan, Rehman, H. U., Qiao, S., & Hameed, A. (2022). Peacock feathers extract use as template for synthesis of Ag and Au nanoparticles and their biological applications. Waste and Biomass Valorization, 13(1), 659-666. doi:10.1007/s12649-021-01537-4
• Wasfi, R., Hamed, S. M., Amer, M. A., & Fahmy, L. I. (2020). Proteus mirabilis Biofilm: Development and therapeutic strategies. Frontiers in Cellular and Infection Microbiology, 10, 414. doi:10.3389/fcimb.2020.00414
• Yang, J., Wang, Q., Wang, C., Yang, R., Ahmed, M., Kumaran, S., Velu, P., & Li, B. (2020). Pseudomonas aeruginosa synthesized silver nanoparticles inhibit cell proliferation and induce ROS mediated apoptosis in thyroid cancer cell line (TPC1). Artificial Cells, Nanomedicine, and Biotechnology, 48(1), 800-809. doi:10.1080/21691401.2019.1687495