Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
권호 표지
DOI QR코드

DOI QR Code

Novel Antibacterial, Cytotoxic and Catalytic Activities of Silver Nanoparticles Synthesized from Acidophilic Actinobacterial SL19 with Evidence for Protein as Coating Biomolecule

  • Wypij, Magdalena (Department of Microbiology, Nicolaus Copernicus University) ;
  • Ostrowski, Maciej (Department of Biochemistry, Nicolaus Copernicus University) ;
  • Piska, Kamil (Department of Pharmaceutical Biochemistry, Faculty of Pharmacy, Jagiellonian University Medical College) ;
  • Wojcik-Pszczola, Katarzyna (Department of Pharmaceutical Biochemistry, Faculty of Pharmacy, Jagiellonian University Medical College) ;
  • Pekala, Elzbieta (Department of Pharmaceutical Biochemistry, Faculty of Pharmacy, Jagiellonian University Medical College) ;
  • Rai, Mahendra (Department of Microbiology, Nicolaus Copernicus University) ;
  • Golinska, Patrycja (Department of Microbiology, Nicolaus Copernicus University)
  • Received : 2022.05.06
  • Accepted : 2022.08.18
  • Published : 2022.09.28
Download PDF
⟨ Previous Next ⟩

Abstract

Silver nanoparticles (AgNPs) have potential applications in medicine, photocatalysis, agriculture, and cosmetic fields due to their unique physicochemical properties and strong antimicrobial activity. Here, AgNPs were synthesized using actinobacterial SL19 strain, isolated from acidic forest soil in Poland, and confirmed by UV-vis and FTIR spectroscopy, TEM, and zeta potential analysis. The AgNPs were polydispersed, stable, spherical, and small, with an average size of 23 nm. The FTIR study revealed the presence of bonds characteristic of proteins that cover nanoparticles. These proteins were then studied by using liquid chromatography with tandem mass spectrometry (LC-MS/MS) and identified with the highest similarity to hypothetical protein and porin with molecular masses equal to 41 and 38 kDa, respectively. Our AgNPs exhibited remarkable antibacterial activity against Escherichia coli and Pseudomonas aeruginosa. The combined, synergistic action of these synthesized AgNPs with commercial antibiotics (ampicillin, kanamycin, streptomycin, and tetracycline) enabled dose reductions in both components and increased their antimicrobial efficacy, especially in the case of streptomycin and tetracycline. Furthermore, the in vitro activity of the AgNPs on human cancer cell lines (MCF-7, A375, A549, and HepG2) showed cancer-specific sensitivity, while the genotoxic activity was evaluated by Ames assay, which revealed a lack of mutagenicity on the part of nanoparticles in Salmonella Typhimurium TA98 strain. We also studied the impact of the AgNPs on the catalytic and photocatalytic degradation of methyl orange (MO). The decomposition of MO was observed by a decrease in intensity of absorbance within time. The results of our study proved the easy, fast, and efficient synthesis of AgNPs using acidophilic actinomycete SL19 strain and demonstrated the remarkable potential of these AgNPs as anticancer and antibacterial agents. However, the properties and activity of such particles can vary by biosynthesized batch.

Keywords

Acknowledgement

M.R. thankfully acknowledges the financial support of the Polish National Agency for Academic Exchange (NAWA; PPN/ULM/2019/1/00117/DEC/1 2019-10-02) and the Department of Microbiology, Nicolaus Copernicus University, Torun, Poland. This research and ACP was funded by the National Science Centre (NSC) grant Preludium (No. 2016/23/N/NZ9/00247).

References

  1. Liu X, Chen JL, Yang WY, Qian YC, Pan JY, Zhu CN, et al. 2021. Biosynthesis of silver nanoparticles with antimicrobial and anticancer properties using two novel yeasts. Sci. Rep. 11: 15795. https://doi.org/10.1038/s41598-021-95262-6
  2. Singh BR, Singh BN, Singh A, Khan W, Naqvi AH, Singh HB. 2015. Mycofabricated biosilver nanoparticles interrupt Pseudomonas aeruginosa quorum sensing systems. Sci. Rep. 5: 13719. https://doi.org/10.1038/srep13719
  3. Roy R, Tiwari M, Donelli G, Tiwari V. 2019. Strategies for combating bacterial biofilms: a focus on anti-biofilm agents and their mechanisms of action. Virulence 9: 522-554. https://doi.org/10.1080/21505594.2017.1313372
  4. Monopoli MP, Aberg C, Salvati A, Dawson KA. 2012. Biomolecular coronas provide the biological identity of nanosized materials. Nat. Nanotechnol. 7: 779-786. https://doi.org/10.1038/nnano.2012.207
  5. Miclaus T, Beer C, Chevallier J, Scavenius C, Bochenkov VE, Enghild JJ, et al. 2016. Dynamic protein coronas revealed as a modulator of silver nanoparticle sulphidation in vitro. Nat. Commun. 7: 11770. https://doi.org/10.1038/ncomms11770
  6. VanOosten SK, Yuca E, Karaca BT, Boone K, Snead ML, Spencer P, et al. 2016. Biosilver nanoparticle interface offers improved cell viability. Surf. Innov. 4: 1. 121-132. https://doi.org/10.1680/jsuin.16.00010
  7. Wypij M, Jedrzejewski T, Trzcinska-Wencel J, Ostrowski M, Rai M, et al. 2021. Green synthesized silver nanoparticles: antibacterial and anticancer activities, biocompatibility, and analyses of surface-attached proteins. Front. Microbiol. 12: 17.
  8. Alqahtani MA, Othman MRA, Mohammed A. 2020. Biofabrication of silver nanoparticles with antibacterial and cytotoxic abilities using lichens. Sci. Rep. 10: 16781. https://doi.org/10.1038/s41598-020-73683-z
  9. Otari S, Patil R, Ghosh S, Thorat N, Pawar S. 2015. Intracellular synthesis of silver nanoparticle by actinobacteria and its antimicrobial activity. Spectrochim. Acta A Mol. Biomol. Spectrosc. 136: 1175-1180. https://doi.org/10.1016/j.saa.2014.10.003
  10. Wypij M, Czarnecka J, Swiecimska M, Dahm H, Rai M, Golinska P. 2018. Synthesis, characterization and evaluation of antimicrobial and cytotoxic activities of biogenic silver nanoparticles synthesized from Streptomyces xinghaiensis OF1 strain. World J. Microbiol. Biotechnol. 34: 23. https://doi.org/10.1007/s11274-017-2406-3
  11. Singh P, Pandit S, Jers Joshi AS, Garnaes J, Mijakovic I. 2021. Silver nanoparticles produced from Cedecea sp. exhibit antibiofilm activity and remarkable stability. Sci. Rep. 11: 12619. https://doi.org/10.1038/s41598-021-92006-4
  12. Sanad F, Nabih S, Goda MA. 2018. A lot of promise for ZnO-5FU nanoparticles cytotoxicity against breast cancer cell lines. J. Nanomed. Nanotechnol. 9: 1-8.
  13. Lin J, Huang Z, Wu H, Zhou W, Jin P, Wei P. 2014. Inhibition of autophagy enhances the anticancer activity of silver nanoparticles. Autophagy 10: 2006-2020. https://doi.org/10.4161/auto.36293
  14. Pei J, Fu B, Jiang L, Sun T. 2019. Biosynthesis, characterization, and anticancer effect of plant-mediated silver nanoparticles using Coptis chinensis. Int. J. Nanomed. 14: 1969-1978. https://doi.org/10.2147/IJN.S188235
  15. Wang ZX, Chen CY, Wang Y, Li FXZ, Huang J, Luo ZW. 2019. Angstrom scale silver particles as a promising agent for low toxicity broad spectrum potent anticancer therapy. Adv. Funct. Mater. 29: 1808556. https://doi.org/10.1002/adfm.201808556
  16. Xu L, Wang YY, Huang J, Chen CY, Wang ZX, Xie H. 2020. Silver nanoparticles: synthesis, medical applications and biosafety. Theranostics 10: 8996-9031. https://doi.org/10.7150/thno.45413
  17. Golinska P, Wypij M, Rathod S, Tikar S, Dahm H, Rai M. 2015. Synthesis of silver nanoparticles from two acidophilic strains of Pilimelia columellifera subsp. pallida and their antibacterial activities. J. Basic Microbiol. 56: 5.
  18. Wypij M, Czarnecka J, Dahm H, Rai M, Golinska P. 2017. Silver nanoparticles from Pilimelia columellifera subsp. pallida SL19 strain demonstrated antifungal activity against fungi causing superficial mycoses. J. Basic Microbiol. 57: 9.
  19. Golinska P, Wypij M, Ingle A, Dahm H, Rai M. 2014. Biogenic synthesis of metal nanoparticles from actinomycetes: biomedical applications and cytotoxicity. Appl. Microbiol. Biotechnol. 98: 12344.
  20. Rai M, Golinska P. 2020. Microbial Nanotechnology, pp. 29-45. CRC Press Taylor and Francis Group.
  21. Swiecimska M, GolinskaP, WypijM, Goodfellow M. 2021. Genomic-based classification of Catenulispora pinisilvae sp. nov., novel actinobacteria isolated from a pine forest soil in Poland and emended description of Catenulispora rubra. Syst. Appl. Microbiol. 44: 126-164.
  22. El Sayed MT, El-Sayed ASA. 2020. Biocidal activity of metalnanoparticles synthesized by Fusarium solani against multi-resistant bacteria and mycotoxigenic fungi. J. Microbiol. Biotechnol. 30: 226-236. https://doi.org/10.4014/jmb.1906.06070
  23. Kumari S, Tehri N, Gahlaut A, Hooda V. 2021. Actinomycetes mediated synthesis, characterization, and applications of metallic nanoparticles. Inorg. Nano-Metal Chem. 51: 1386-1395. https://doi.org/10.1080/24701556.2020.1835978
  24. Gad El-Rab SMF, Basha S, Ashour AA, Enan ET, Alyamani AA, Felemban NH. 2021. Green synthesis of cooper nano-drug and its dental application upon periodontal disease-causing microorganisms. J. Microbiol. Biotechnol. 31: 1656-1666. https://doi.org/10.4014/jmb.2106.06008
  25. Shirling EB, Gottlieb D. 1966. Methods for characterization of Streptomyces sp. Int. J. Syst. Bacteriol. 16: 313-340. https://doi.org/10.1099/00207713-16-3-313
  26. Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72: 248-254. https://doi.org/10.1006/abio.1976.9999
  27. Ogita ZI, Markert CL. 1979. A miniaturized system for electrophoresis on polyacrylamide gels. Anal. Biochem. 99: 233-241. https://doi.org/10.1016/S0003-2697(79)80001-9
  28. Harlow E, Lane D. 1988. Antibodies: A laboratory manual, pp. 83. In Greenfield EA (ed.), Antibodies. Cold Spring Harbour Laboratory Press, New York, NY, USA.
  29. Kassim A, Omuse GO, Premji Z, Revathi G. 2016. Comparison of Clinical Laboratory Standards Institute and European Committee on Antimicrobial Susceptibility Testing. Annals Clin. Microbiol. Antimicrobiol. 15: 21. https://doi.org/10.1186/s12941-016-0135-3
  30. May J, Shannon K, King A, French G. 1998. Glycopeptide tolerance in Staphylococcus aureus. J. Antimicrob. Chemother. 42: 189-197. https://doi.org/10.1093/jac/42.2.189
  31. Mohammed AE, Al-Qahtani A, Al-Mutairi A, Al-Shamri B, Aabed KF. 2018. Antibacterial and cytotoxic potential of biosynthesized silver nanoparticles by some plant extracts. Nanomat. (Basel) 8: 6. https://doi.org/10.3390/nano8010006
  32. Odds FC. 2003. Synergy, antagonism, and what the chequerboard puts between them. J. Antimicrob. Chemother. 52: 1. https://doi.org/10.1093/jac/dkg301
  33. Oparka M, Walczak J, Malinska D, van Oppen LMPE, Szczepanowska J, Koopman WJH, Wieckowski MR. 2016. Quantifying ROS levels using CM-H2DCFDA and HyPer. Methods 15: 109.
  34. Wypij M, Jedrzejewski T, Ostrowski M, Trzcinska J, Rai M, Golinska P. 2020. Biogenic silver nanoparticles: assessment of their cytotoxicity, genotoxicity and study of capping proteins. Molecules 25: 3022. https://doi.org/10.3390/molecules25133022
  35. OCDE. 2018. Stemming the Superbug Tide. OECD Health Policy Studies. OECD. Available from https://www.oecd.org/health/stemming-the-superbug-tide9789264307599-en.htm. Accessed Nov. 07, 2018.
  36. Siegel RL, Miller KD, Jemal A. 2020. Cancer statistics. Cancer J. Clin. 70: 7-30. https://doi.org/10.3322/caac.21590
  37. Gomes F, Lorigan P, Woolley S,Foden P, BurnsK, Yorke J, Blackhall F. 2021. A prospective cohort study on the safety of checkpoint inhibitors in older cancer patients -the ELDERS study. ESMO Open 6: 100042. https://doi.org/10.1016/j.esmoop.2020.100042
  38. Khan MS, Alomari A, Tabrez S, Hassan I, Wahab R, Bhat SA, et al. 2021. Anticancer potential of biogenic silver nanoparticles: a mechanistic study. Pharmaceutics 13: 707. https://doi.org/10.3390/pharmaceutics13050707
  39. Yang Y, Guo L, Wang Z, Liu P, Liu X, Ding J, et al. 2021. Targeted silver nanoparticles for rheumatoid arthritis therapy via macrophage apoptosis and Re-polarization. Biomaterials 264: 120390. https://doi.org/10.1016/j.biomaterials.2020.120390
  40. Burdusel AC, Gherasim O, Grumezescu AM, Mogoanta L, Ficai A, Andronescu E. 2018. Biomedical applications of silver nanoparticles: an up-to-date overview. Nanomat. 8: 681. https://doi.org/10.3390/nano8090681
  41. Khan MZH, Tarek FK, Nuzat M, Momin MA, Hasan MR. 2017. Rapid biological synthesis of silver nanoparticles from Ocimum sanctum and their characterization. J. Nanosci. 6: 6-9.
  42. Azmath P, Baker S, Rakshith D, Satish S. 2016. Mycosynthesis of silver nanoparticles bearing antibacterial activity. Saudi Pharm. J. 24: 140-146. https://doi.org/10.1016/j.jsps.2015.01.008
  43. Hamouda RA, Hussein MH, Abo-elmagd RA, Bawazir SS. 2019. Synthesis and biological characterization of silver nanoparticles derived from the cyanobacterium Oscillatoria limnetica. Sci. Rep. 9: 13071. https://doi.org/10.1038/s41598-019-49444-y
  44. Ahmad N, Sharma S. 2012. Green synthesis of silver nanoparticles using extracts of Ananas comosus. Green Sustain. Chem. 2: 26832.
  45. Gemishev O, Panayotova M, Gicheva G, Mintcheva N. 2022. Green synthesis of stable spherical monodisperse silver nanoparticles using a cell-free extract of Trichoderma reesei. Materials 15: 481. https://doi.org/10.3390/ma15020481
  46. Rezvani Amin Z, Khashyarmanesh Z, Fazly Bazzaz BS, Sabeti Noghabi Z. 2019. Does biosynthetic silver nanoparticles are more stable with lower toxicity than their synthetic counterparts? Iranian J. Pharm. Res. 18: 210-221.
  47. Bakhtiari-Sardari A, Mashreghi M, Eshghi H, Behnam-Rasouli F, Lashani E, Shahnavaz B. 2020. Comparative evaluation of silver nanoparticles biosynthesis by two cold-tolerant Streptomyces strains and their biological activities. Biotechnol. Lett. 42: 1985-1999. https://doi.org/10.1007/s10529-020-02921-1
  48. Jeevan P, Rena RK, Edith A. 2012. Extracellular biosynthesis of silver nanoparticles by culture supernatant of Pseudomonas aeruginosa. IJBT 11: 72-76.
  49. Monowar T, Rahman M, Bhore SJ, Raju G, Sathasivam KV. 2018. Silver nanoparticles synthesized by using the endophytic bacterium Pantoea ananatis are promising antimicrobial agents against multidrug resistant bacteria. Molecules 23: 3220. https://doi.org/10.3390/molecules23123220
  50. Ren Y, Yang H, Wang T, Wang C. 2019. Bio-synthesis of silver nanoparticles with antibacterial activity. Mat. Chem. Physics 235: 1.
  51. Rasheed T, Bilal M, Li C, Nabeel F, Khalid M, Iqbal HMN. 2018. Catalytic potential of biosynthesized silver nanoparticles using Convolvulus arvensis extract for the degradation of environmental pollutants. J. Photochem. Photobiol. B Biol. 181: 44-52. https://doi.org/10.1016/j.jphotobiol.2018.02.024
  52. Dusane DH, Pawar VS, Nancharaiah Y, Venugopalan VP, Kumar AR, Zinjarde SS. 2011. Anti-biofilm potential of a glycolipid surfactant produced by a tropical marine strain of Serratia marcescens. Biofouling 27: 645-654. https://doi.org/10.1080/08927014.2011.594883
  53. Choudhary MK, Kataria J, Cameotra SS, Singh J. 2016. A facile biomimetic preparation of highly stabilized silver nanoparticles derived from seed extract of Vigna radiata and evaluation of their antibacterial activity. Appl. Nanosci. 6: 105-111. https://doi.org/10.1007/s13204-015-0418-6
  54. Narasimha G, Janardhan K, Alzohairy M, Khadri H, Mallikarjuna K. 2013. Extracellular synthesis, characterization and antibacterial activity of silver nanoparticles by actinomycetes isolative. Int. J. Nano Dimens. 4: 77-83.
  55. Rodrigues AG, Ping LY, Marcato PD, Alves OL, Silva MCP, Ruiz RC, et al. 2013. Biogenic antimicrobial silver nanoparticles produced by fungi. Appl. Microbiol. Biotechnol. 97: 775-782. https://doi.org/10.1007/s00253-012-4209-7
  56. Jain N, Bhargava A, Majumdar S, Tarafdar JC, Panwar J. 2011. Extracellular biosynthesis and characterization of silver nanoparticles using Aspergillus flavus NJP08: a mechanism perspective. Nanoscale 3: 635-641. https://doi.org/10.1039/C0NR00656D
  57. Guilger-Casagrande M, Germano-Costa T, Bilesky-Jose N, Pasquoto-Stigliani T, Carvalho L, Fraceto LF, et al. 2021. Influence of the capping of biogenic silver nanoparticles on their toxicity and mechanism of action towards Sclerotinia sclerotiorum. J. Nanobiotechnol. 19: 53. https://doi.org/10.1186/s12951-021-00797-5
  58. Singh HJD, Singh P, HooYi T. 2018. Extracellular synthesis of silver nanoparticles by Pseudomonas sp. THG-LS1.4 and their antimicrobial application. J. Pharma. Anal. 8: 258-264. https://doi.org/10.1016/j.jpha.2018.04.004
  59. Al-Dhabi NA, Ghilan AKM, Arasu MV, Duraipandiyan V. 2018. Green biosynthesis of silver nanoparticles produced from marine Streptomyces sp. Al-Dhabi-89 and their potential applications against wound infection and drug resistant clinical pathogens. J. Photochem. Photobiol. B Biol. 189: 176-184. https://doi.org/10.1016/j.jphotobiol.2018.09.012
  60. Mondejar-Lopez M, Lopez-Jimenez AJ, Abad-Jorda M, Rubio-Moraga A, Ahrazem O, Gomez-Gomez L, Niza E. 2021. Biogenic silver nanoparticles from Iris tuberosa as potential preservative in cosmetic products. Molecules 26: 4696. https://doi.org/10.3390/molecules26154696
  61. Rautela A, Rani J, Debnath (Das) M. 2019. Green synthesis of silver nanoparticles from Tectona grandis seeds extract: characterization and mechanism of antimicrobial action on different microorganisms. J. Analytic. Sci. Technol. 10: 5. https://doi.org/10.1186/s40543-018-0163-z
  62. Barros CHL. 2018. Biogenic nanosilver against multidrug-resistant bacteria (MRDB). Tasic Antibiotics 7: 69. https://doi.org/10.3390/antibiotics7030069
  63. Bapat RA, Chaubal TV, Joshi CP, Bapat PR, Choudhury H, Pandey M, Gorain B, Kesharwani P. 2018. An overview of application of silver nanoparticles for biomaterials in dentistry. Mater. Sci. Eng. C 91: 881-898. https://doi.org/10.1016/j.msec.2018.05.069
  64. Khorrami S, Zarrabi A, Khaleghi M, Danaei M, Mozafari M. 2018. Selective cytotoxicity of green synthesized silver nanoparticles against the MCF-7 tumor cell line and their enhanced antioxidant and antimicrobial properties. Int. J. Nanomed. 13: 8013-8024. https://doi.org/10.2147/IJN.S189295
  65. Liu X, Ma L, Chen F, Liu J, Lu Z. 2019. Synergistic antibacterial mechanism of nanoparticles combined with the ineffective β-lactam antibiotic cefotaxime against methicillin-resistant Staphylococcus aureus. J. Inorg. Biochem. 196: 110687. https://doi.org/10.1016/j.jinorgbio.2019.04.001
  66. Hwang IS, Hwang JH, Choi H, Kim KJ, Lee DG. 2012. Synergistic effects between silver nanoparticles and antibiotics and the mechanisms involved. J. Med. Microbiol. 61: 1719-1726. https://doi.org/10.1099/jmm.0.047100-0
  67. Marr KA, Boeckh M, Carter RA, Kim HW, Corey L. 2004. Combination antifungal therapy for invasive aspergillosis. Clin. Infect. Dis. 39: 797-802. https://doi.org/10.1086/423380
  68. Abdel-HaqR, SchlachetzkiJCM, GlassCK, Mazmanian SK. 2019. Microbiome-microglia connections via the gut-brain axis. J. Exp. Med. 7: 41-59.
  69. FayazAM, Balaji K, Girilal M, Yadav R, Kalaichelvan PT, Venketesan R. 2010. Biogenic synthesis of silver nanoparticles and their synergistic effect with antibiotics: a study against gram-positive and gram-negative bacteria. Nanomed. 6: 103-109. https://doi.org/10.1016/j.nano.2009.04.006
  70. Fulaz S, Vitale S, Quinn L, Casey E. 2019. Nanoparticle-biofilm interactions: the role of the EPS matrix. Trends Microbiol. 27: 915-926. https://doi.org/10.1016/j.tim.2019.07.004
  71. Mikhailova EO. 2020. Silver nanoparticles: mechanism of action and probable bio-application. J. Funct. Biomater. 11: 84. https://doi.org/10.3390/jfb11040084
  72. Berne C, Ellison CK, Ducret A, Brun YV. 2018. Bacterial adhesion at the single-cell level. Nat. Rev. Genet. 16: 616-627. https://doi.org/10.1038/s41579-018-0057-5
  73. Rizzello L, Cingolani R, Pompa PP. 2013. Nanotechnology tools for antibacterial materials. Nanomed. 8: 807-821. https://doi.org/10.2217/nnm.13.63
  74. Buerki-Thurnherr T,Xiao L,Diener L, Arslan O, Hirsch C,Maeder-Althaus X, et al. 2013. In vitro mechanistic study towards a better understanding of ZnO nanoparticle toxicity. Nanotoxicol. 7: 402-426. https://doi.org/10.3109/17435390.2012.666575
  75. Gaiser BK, Hirn S, Kermanizadeh A, Kanase N, Fytianos K, Wenk A, et al. 2013. Effects of silver nanoparticles on the liver and hepatocytes in vitro. Toxicol. Sci. 131: 537-547. https://doi.org/10.1093/toxsci/kfs306
  76. Sahu SC, Zheng J. Graham L, Chen L, Ihrie J, Yourick JJ, et al. 2014. Comparative cytotoxicity of nanosilver in human liver HepG2 and colon Caco2 cells in culture. J. Appl. Toxicol. 34: 1155-1166. https://doi.org/10.1002/jat.2994
  77. Supraja N, Prasad T, Soundariya M, Babujanarthanam R. 2016. Synthesis, characterization and dose dependent antimicrobial and anti-cancerous activity of phycogenic silver nanoparticles against human hepatic carcinoma (HepG2) cell line. AIMS Bioeng. 4: 425-440.
  78. Noorbazargan H, Amintehrani S, Dolatabadi A, Mashayekhi A, Khayam N, Moulavi P, et al. 2021. Anti-cancer & anti-metastasis properties of bioorganic-capped silver nanoparticles fabricated from Juniperus chinensis extract against lung cancer cells. AMB Express 11: 61. https://doi.org/10.1186/s13568-021-01216-6
  79. El-HusseinA, Hamblin MR. 2017. ROS generation and DNA damage with photo-inactivation mediated by silver nanoparticles in lung cancer cell line. IET Nanobiotechnol. 11: 173-178. https://doi.org/10.1049/iet-nbt.2015.0083
  80. Butler KS, Peeler DJ, Casey BJ, Dair BJ, Elespuru RK. 2015. Silver nanoparticles: correlating nanoparticle size and cellular uptake with genotoxicity. Mutagenesis 30: 577-591. https://doi.org/10.1093/mutage/gev020
  81. Donaldson K, Poland CA, Schins RP. 2010. Possible genotoxic mechanisms of nanoparticles: criteria for improved test strategies. Nanotoxicol. 4: 414-420. https://doi.org/10.3109/17435390.2010.482751
  82. Cyril N, George JB, Laigi J, Sylas VP. 2019. Catalytic degradation of methyl orange and selective sensing of mercury ion in aqueous solutions using green synthesized silver nanoparticles from the seeds of Derris trifoliata. J. Clust. Scien. 30: 459-468. https://doi.org/10.1007/s10876-019-01508-9
  83. Kumar P, Govindaraju M, Senthamilselvi S, Premkumar K. 2013. Photocatalytic degradation of methyl orange dye using silver (Ag) nanoparticles synthesized from Ulva lactuca. Colloids Surf. B Biointerfaces 103: 658-661. https://doi.org/10.1016/j.colsurfb.2012.11.022
  84. Wang P, Huang B, Qin X, Zhang X, Dai Y, Wei J, et al. 2008. Ag@AgCl: a highly efficient and stable photocatalyst active under visible light. J. German Chem. Soc. 47: 7931-7933.
  85. Bhakya S, Muthukrishnan S, Sukumaran M, Muthukumar M, Senthil Kumar T, Rao MV. 2015. Catalytic degradation of organic dyes using synthesized silver nanoparticles: a green approach. J. Bioremed. Biodeg. 6: 312.
  86. Latha D, Arulvasu CD, Prabu PD, Narayanan VD. 2017. Photocatalytic activity of biosynthesized silver nanoparticle from leaf extract of Justicia adhatoda. Mechan. Mat. Sci. Engin. 16: 3243.
  87. Christopher P, Xin H, Linic S. 2011. Visible-light-enhanced catalytic oxidation reactions on plasmonic silver nanostructures. Nat. Chem. 3: 467-472. https://doi.org/10.1038/nchem.1032