Abstract
The use of silver nanoparticles obtained by the green synthesis approach in the field of nanomedicine is on the rise. Therefore, it is imperative to search for and develop simple, safe, and quick methods for mass production. Our previous study demonstrated a green synthesis approach that offers the possibility to reuse biomaterial to synthesise silver nanoparticles. Cyperus esculentus tubers were used as bio-reductant to synthesise silver nanoparticles (CpE-AgNPs) with sizes ranging from 50 to 80 nm. In the present study, the antimicrobial properties of the CpE-AgNPs were studied. The efficacy of the CpE-AgNPs was demonstrated against selected microorganisms, namely, Escherichia coli, Klebsiella pneumoniae, Salmonella typhi, Bacillus subtilis, Pseudomonas aeruginosa, methicillin-resistant Staphylococcus aureus (MRSA), Streptococcus mutans, and Candida albicans. The minimum inhibitory concentration of the CpE-AgNPs against the selected microorganisms ranged from 7.81 to 250 µg/mL, with B. subtilis being the most susceptible. The CpE-AgNPs were bacteri-/fungi-cidal against all the studied microorganisms. The efficacy of prepared CpE-AgNPs to enhance the potency of standard antibiotics was also demonstrated in combination with tetracycline and ciprofloxacin. The combinatory effect ranged from synergistic to antagonistic. The CpE-AgNPs were also efficacious in inhibiting microbial biofilm formation. Biofilm inhibition up to 100% was demonstrated against MRSA, S. mutans, P. aeruginosa, and C. albicans at a concentration of 250 µg/mL. The results from the study show that the CpE-AgNPs can serve as an effective drug candidate in the fight against the growing antimicrobial-resistant menace.
Similar content being viewed by others
Data Availability
The data supporting the findings of this study are available from the corresponding author upon request.
References
Elegbede, J. A., & Lateef, A. (2019). Green synthesis of silver (Ag), gold (Au), and silver–gold (Ag–Au) alloy nanoparticles: A review on recent advances, trends, and biomedical applications. In: Verma, D.K., Goyal, M.R., and Suleria, H.A.R. (Eds.). Nanotechnology and Nanomaterial Applications in Food, Health and Biomedical Sciences. Nanotechnology and Nanomaterial Applications in Food, Health, and Biomedical Sciences, Apple Academic Press Inc. /CRC Press, Taylor and Francis Group, Oakville, Ontario, Canada. https://doi.org/10.1201/9780429425660-1
Benyettou, F., Rezgui, R., Ravaux, F., Jaber, T., Blumer, K., Jouiad, M., … Trabolsi, A. (2015). Synthesis of silver nanoparticles for the dual delivery of doxorubicin and alendronate to cancer cells. Journal of Materials Chemistry B, 3(36), 7237–7245. https://doi.org/10.1039/C5TB00994D
Lee, S. H., & Jun, B. H. (2019). Silver nanoparticles: Synthesis and application for nanomedicine. International Journal of Molecular Sciences, 20(4), 865. https://doi.org/10.3390/IJMS20040865
Siddiqi, K. S., Husen, A., & Rao, R. A. K. (2018). A review on biosynthesis of silver nanoparticles and their biocidal properties. Journal of Nanobiotechnology, 16(1), 1–28. https://doi.org/10.1186/s12951-018-0334-5
Anees Ahmad, S., Sachi Das, S., Khatoon, A., Tahir Ansari, M., Afzal, M., Saquib Hasnain, M., & Kumar Nayak, A. (2020). Bactericidal activity of silver nanoparticles: A mechanistic review. Materials Science for Energy Technologies, 3(2020), 756–769. https://doi.org/10.1016/j.mset.2020.09.002
Sanyasi, S., Majhi, R. K., Kumar, S., Mishra, M., Ghosh, A., Suar, M., …, Goswami, L. (2016). Polysaccharide-capped silver Nanoparticles inhibit biofilm formation and eliminate multi-drug-resistant bacteria by disrupting bacterial cytoskeleton with reduced cytotoxicity towards mammalian cells. Scientific Reports, 6(October 2015), 1–16. https://doi.org/10.1038/srep24929
Goswami, S. R., Sahareen, T., Singh, M., & Kumar, S. (2015). Role of biogenic silver nanoparticles in disruption of cell-cell adhesion in Staphylococcus aureus and Escherichia coli biofilm. Journal of Industrial and Engineering Chemistry, 26, 73–80. https://doi.org/10.1016/j.jiec.2014.11.017
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(June), 1–15.https://doi.org/10.3389/fmicb.2020.01143
Prasad Yadav, T., Manohar Yadav, R., & Pratap Singh, D. (2012). Mechanical milling: A top down approach for the synthesis of nanomaterials and nanocomposites. Nanoscience and Nanotechnology, 2(3), 22–48. https://doi.org/10.5923/J.NN.20120203.01
Corbierre, M. K., Beerens, J., & Lennox, R. B. (2005). Gold nanoparticles generated by electron beam lithography of gold(I)-thiolate thin films. Chemistry of Materials, 17(23), 5774–5779. https://doi.org/10.1021/CM051085B
Grammatikopoulos, P., Steinhauer, S., Vernieres, J., Singh, V., & Sowwan, M. (2016). Nanoparticle design by gas-phase synthesis. Advances in Physics, 1(1), 81–100. https://doi.org/10.1080/23746149.2016.1142829
Asanithi, P., Chaiyakun, S., & Limsuwan, P. (2012). Growth of silver nanoparticles by DC magnetron sputtering. Journal of Nanomaterials, 2012, 1–8. https://doi.org/10.1155/2012/963609
Galembeck, A., Brito-Silva, A. M., Gmez, L. A., & De Arajo, C. B. (2010). Laser ablated silver nanoparticles with nearly the same size in different carrier media. Journal of Nanomaterials, 2010, 1–7. https://doi.org/10.1155/2010/142897
Bokov, D., Turki Jalil, A., Chupradit, S., Suksatan, W., Javed Ansari, M., Shewael, I. H., Valiev, G. H., Kianfar, E. (2021). Nanomaterial by sol-gel method: Synthesis and application. Advances in Materials Science and Engineering, 2021, 1–7. https://doi.org/10.1155/2021/5102014
Singh, J., Dutta, T., Kim, K. H., Rawat, M., Samddar, P., & Kumar, P. (2018). “Green” synthesis of metals and their oxide nanoparticles: Applications for environmental remediation. Journal of Nanobiotechnology, 16(1), 1–24. https://doi.org/10.1186/s12951-018-0408-4
Mare, A. D., Ciurea, C. N., Man, A., Mareș, M., Toma, F., Berța, L., & Tanase, C. (2021). In vitro antifungal activity of silver nanoparticles biosynthesized with beech bark extract. Plants, 10(10), 1–15. https://doi.org/10.3390/plants10102153
Gajbhiye, M., Kesharwani, J., Ingle, A., Gade, A., & Rai, M. (2009). Fungus-mediated synthesis of silver nanoparticles and their activity against pathogenic fungi in combination with fluconazole. Nanomedicine: Nanotechnology, Biology and Medicine, 5(4), 382–386. https://doi.org/10.1016/J.NANO.2009.06.005
Shu, M., He, F., Li, Z., Zhu, X., Ma, Y., Zhou, Z., …, Zeng, M. (2020). Biosynthesis and antibacterial activity of silver nanoparticles using yeast extract as reducing and capping agents. Nanoscale Research Letters, 15(1), 1–9. https://doi.org/10.1186/S11671-019-3244-Z/FIGURES/7
Gloria Martin, K. D., & Vergara Padilla, K. G. (2020). Sunlight mediated synthesis of silver nanoparticles by Bacillus sp and its antibacterial property. Oriental Journal of Chemistry, 36(03), 419–424. https://doi.org/10.13005/ojc/360309
Khanna, P., Kaur, A., & Goyal, D. (2019). Algae-based metallic nanoparticles: Synthesis, characterization and applications. Journal of Microbiological Methods, 163, 105656. https://doi.org/10.1016/J.MIMET.2019.105656
Akintayo, G. O., Lateef, A., Azeez, M. A., Asafa, T. B., Oladipo, I. C., Badmus, J. A., …, Yekeen, T. A. (2020). Synthesis, bioactivities and cytogenotoxicity of animal fur-mediated silver nanoparticles. IOP Conference Series: Materials Science and Engineering, 805(1), 012041. https://doi.org/10.1088/1757-899X/805/1/012041
Jamdagni, P., Khatri, P., & Rana, J. S. (2018). Green synthesis of zinc oxide nanoparticles using flower extract of Nyctanthes arbor-tristis and their antifungal activity. Journal of King Saud University - Science, 30(2), 168–175. https://doi.org/10.1016/J.JKSUS.2016.10.002
Chauhan, N., Tyagi, A. K., Kumar, P., & Malik, A. (2016). Antibacterial potential of Jatropha curcas synthesized silver nanoparticles against food borne pathogens. Frontiers in Microbiology, 7(NOV), 1748. https://doi.org/10.3389/FMICB.2016.01748/BIBTEX
Król, A., Railean-Plugaru, V., Pomastowski, P., & Buszewski, B. (2019). Phytochemical investigation of Medicago sativa L. extract and its potential as a safe source for the synthesis of ZnO nanoparticles: The proposed mechanism of formation and antimicrobial activity. Phytochemistry Letters, 31, 170–180. https://doi.org/10.1016/J.PHYTOL.2019.04.009
Singhal, G., Bhavesh, R., Kasariya, K., Sharma, A. R., & Singh, R. P. (2011). Biosynthesis of silver nanoparticles using Ocimum sanctum (Tulsi) leaf extract and screening its antimicrobial activity. Journal of Nanoparticle Research, 13(7), 2981–2988. https://doi.org/10.1007/S11051-010-0193-Y
Mo, Y. Y., Tang, Y. K., Wang, S. Y., Lin, J. M., Zhang, H. B., & Luo, D. Y. (2015). Green synthesis of silver nanoparticles using eucalyptus leaf extract. Materials Letters, 144, 165–167. https://doi.org/10.1016/J.MATLET.2015.01.004
Ashraf, A., Zafar, S., Zahid, K., Salahuddin Shah, M., Al-Ghanim, K. A., Al-Misned, F., & Mahboob, S. (2019). Synthesis, characterization, and antibacterial potential of silver nanoparticles synthesized from Coriandrum sativum L. Journal of Infection and Public Health, 12(2), 275–281. https://doi.org/10.1016/J.JIPH.2018.11.002
Krishnaraj, C., Jagan, E. G., Rajasekar, S., Selvakumar, P., Kalaichelvan, P. T., & Mohan, N. (2010). Synthesis of silver nanoparticles using Acalypha indica leaf extracts and its antibacterial activity against water borne pathogens. Colloids and surfaces. B, Biointerfaces, 76(1), 50–56. https://doi.org/10.1016/J.COLSURFB.2009.10.008
Lateef, A., Azeez, M. A., Asafa, T. B., Yekeen, T. A., Akinboro, A., Oladipo, I. C., …, Beukes, L. S. (2016). Cocoa pod husk extract-mediated biosynthesis of silver nanoparticles: its antimicrobial, antioxidant and larvicidal activities. Journal of Nanostructure in Chemistry, 6(2), 159–169. https://doi.org/10.1007/S40097-016-0191-4/FIGURES/9
Azeez, M. A., Lateef, A., Asafa, T. B., Yekeen, T. A., Akinboro, A., Oladipo, I. C., …, Beukes, L. S. (2017). Biomedical applications of cocoa bean extract-mediated silver nanoparticles as antimicrobial, larvicidal and anticoagulant agents. Journal of Cluster Science, 28(1), 149–164. https://doi.org/10.1007/S10876-016-1055-2/METRICS
Ajayi, I. A., Raji, A. A., & Ogunkunle, E. O. (2015). Green synthesis of silver nanoparticles from seed extracts of Cyperus esculentus and Butyrospermum paradoxum. IOSR Journal of Pharmacy and Biological Sciences Ver. I, 10(4), 2319–7676. https://doi.org/10.9790/3008-10417690
Gambo, A., & Da’u, A. (2014). Tiger nut (Cyperus Esculentus): Composition, products, uses and health benefits - A review. Bayero Journal of Pure and Applied Sciences, 7(1), 56.https://doi.org/10.4314/bajopas.v7i1.11
Ankudze, B., & Samlafo, V. B. (2022). Repeated use of Cyperus esculentus tubers, towards sustainable green synthesis of silver nanoparticles. BioNanoScience, 2022, 1–8. https://doi.org/10.1007/S12668-022-01032-7
Nester, E. W., Anderson, D. ., Roberts Jr, C. E., Pearsall, N. N., Nester, T., & Hurley, D. (2004). Microbiology: A human perspective (4th Editio.). New York, USA: McGraw-Hill, Boston. Retrieved from https://www.scirp.org/(S(lz5mqp453edsnp55rrgjct55))/reference/ReferencesPapers.aspx?ReferenceID=1856478. Accessed 28 April 2022
Khodavandi, A., Alizadeh, F., Aala, F., Sekawi, Z., & Chong, P. P. (2010). In vitro investigation of antifungal activity of allicin alone and in combination with azoles against Candida species. Mycopathologia, 169(4), 287–295. https://doi.org/10.1007/S11046-009-9251-3
Nascimento Da Silva, L. C., Messias Sandes, J., De Paiva, M. M., De Araú Jo, J. M., De Figueiredo, R. C. B. Q., Da Silva, M. V., & Correia, M. T. D. S. (2013). Anti-Staphylococcus aureus action of three Caatinga fruits evaluated by electron microscopy. Natural Product Research, 27(16), 1492–1496. https://doi.org/10.1080/14786419.2012.722090
Pierce, C. G., Uppuluri, P., Tristan, A. R., Wormley, F. L., Mowat, E., Ramage, G., & Lopez-Ribot, J. L. (2008). A simple and reproducible 96-well plate-based method for the formation of fungal biofilms and its application to antifungal susceptibility testing. Nature Protocols, 3(9), 1494–1500. https://doi.org/10.1038/NPORT.2008.141
Krithiga, N., Rajalakshmi, A., & Jayachitra, A. (2015). Green synthesis of silver nanoparticles using leaf extracts of Clitoria ternatea and Solanum nigrum and study of its antibacterial effect against common nosocomial pathogens. Journal of Nanoscience, 2015, 1–8. https://doi.org/10.1155/2015/928204
Vanaja, M., & Annadurai, G. (2013). Coleus aromaticus leaf extract mediated synthesis of silver nanoparticles and its bactericidal activity. Applied Nanoscience (Switzerland), 3(3), 217–223. https://doi.org/10.1007/s13204-012-0121-9
Shankar, S. S., Ahmad, A., & Sastry, M. (2003). Geranium leaf assisted biosynthesis of silver nanoparticles. Biotechnology Progress, 19(6), 1627–1631. https://doi.org/10.1021/bp034070w
Joo, H. S., & Otto, M. (2012). Molecular basis of in vivo biofilm formation by bacterial pathogens. Chemistry and Biology, 19(12), 1503–1513. https://doi.org/10.1016/j.chembiol.2012.10.022
Siddique, M. H., Aslam, B., Imran, M., Ashraf, A., Nadeem, H., Hayat, S., … Muzammil, S. (2020). Effect of silver nanoparticles on biofilm formation and eps production of multidrug-resistant Klebsiella pneumoniae. BioMed Research International, 2020, 1–9. https://doi.org/10.1155/2020/6398165
Hsueh, Y. H., Lin, K. S., Ke, W. J., Hsieh, C. T., Chiang, C. L., Tzou, D. Y., & Liu, S. T. (2015). The antimicrobial properties of silver nanoparticles in Bacillus subtilis are mediated by released Ag+ ions. PLoS ONE, 10(12), 1–17. https://doi.org/10.1371/journal.pone.0144306
Helmlinger, J., Sengstock, C., Groß-Heitfeld, C., Mayer, C., Schildhauer, T. A., Köller, M., & Epple, M. (2016). Silver nanoparticles with different size and shape: Equal cytotoxicity, but different antibacterial effects. RSC Advances, 6(22), 18490–18501. https://doi.org/10.1039/c5ra27836h
Aguda, O. N., & Lateef, A. (2021). Novel biosynthesis of silver nanoparticles through valorization of Parkia biglobosa fermented-seed wastewater: Antimicrobial properties and nanotextile application. Environmental Technology & Innovation, 24, 102077. https://doi.org/10.1016/J.ETI.2021.102077
Masoud Hussein, E. A., Mohammad, A. A. H., Harraz, F. A., & Ahsan, M. F. (2019). Biologically synthesized silver nanoparticles for enhancing tetracycline activity against Staphylococcus aureus and Klebsiella pneumoniae. Brazilian Archives of Biology and Technology, 62, 1–14. https://doi.org/10.1590/1678-4324-2019180266
Ipe, D. S., Kumar, P. T. S., Love, R. M., & Hamlet, S. M. (2020). Silver nanoparticles at biocompatible dosage synergistically increases bacterial susceptibility to antibiotics. Frontiers in Microbiology, 11(May), 1–11. https://doi.org/10.3389/fmicb.2020.01074
Fayaz, A. M., Balaji, K., Girilal, M., Yadav, R., Kalaichelvan, P. T., & Venketesan, R. (2010). Biogenic synthesis of silver nanoparticles and their synergistic effect with antibiotics: a study against gram-positive and gram-negative bacteria. Nanomedicine: Nanotechnology, Biology and Medicine, 6(1), 103–109. https://doi.org/10.1016/J.NANO.2009.04.006
Ayala-Núñez, N. V., Lara Villegas, H. H., Del Carmen Ixtepan Turrent, L., & Rodríguez Padilla, C. (2009). Silver nanoparticles toxicity and bactericidal effect against methicillin-resistant staphylococcus aureus: Nanoscale does matter. Nanobiotechnology, 5(1–4), 2–9. https://doi.org/10.1007/s12030-009-9029-1
Moteriya, P., & Chanda, S. (2018). Biosynthesis of silver nanoparticles formation from Caesalpinia pulcherrima stem metabolites and their broad spectrum biological activities. Journal of Genetic Engineering and Biotechnology, 16(1), 105–113. https://doi.org/10.1016/j.jgeb.2017.12.003
Balakrishnan, S., Ibrahim, K. S., Duraisamy, S., Sivaji, I., Kandasamy, S., Kumarasamy, A., & Kumar, N. S. (2020). Antiquorum sensing and antibiofilm potential of biosynthesized silver nanoparticles of Myristica fragrans seed extract against MDR Salmonella enterica serovar Typhi isolates from asymptomatic typhoid carriers and typhoid patients. Environmental Science and Pollution Research, 27(3), 2844–2856. https://doi.org/10.1007/s11356-019-07169-5
Palanisamy, N. K., Ferina, N., Amirulhusni, A. N., Mohd-Zain, Z., Hussaini, J., Ping, L. J., & Durairaj, R. (2014). Antibiofilm properties of chemically synthesized silver nanoparticles found against Pseudomonas aeruginosa. Journal of Nanobiotechnology, 12(1), 1–7. https://doi.org/10.1186/1477-3155-12-2
Vijayan, S., Divya, K., Varghese, S., & Jisha, M. S. (2020). Antifungal efficacy of chitosan-stabilized biogenic silver nanoparticles against pathogenic Candida spp. isolated from human. BioNanoScience, 10(4), 974–982. https://doi.org/10.1007/s12668-020-00781-7
Right, C., Alotaibi, G. F., & Bukhari, M. A. (2021). Factors influencing bacterial biofilm formation and development. American Journal of Biomedical Science & Research, 12(6), 617–626. https://doi.org/10.34297/AJBSR.2021.12.001820
Acknowledgements
Christopher K. Dawari and the University of Eastern Finland are acknowledged for their immense help in the acquisition of the Scanning electron microscopy image and EDS spectrum.
Funding
No funding was received for conducting this study.
Author information
Authors and Affiliations
Contributions
A.B synthesised the silver nanoparticle solution and characterised it. D.N and B.K.H carried out the antimicrobial studies of the silver nanoparticles. All the authors contributed to the writing of the manuscript.
Corresponding author
Ethics declarations
Conflict of Interests
The authors declare no competing interests.
Research Involving Humans and Animals Statement
This research does not involve humans and animals.
Informed Consent
All authors authorise the publication of this manuscript.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Ankudze, B., Neglo, D. & Harley, B.K. Antimicrobial and Biofilm Formation Inhibition Properties of Biogenic Silver Nanoparticles Synthesised Using Tuber Extract of Cyperus esculentus. BioNanoSci. 13, 103–113 (2023). https://doi.org/10.1007/s12668-023-01061-w
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12668-023-01061-w