Characterization and in vitro antitumor, antibacterial and antifungal activities of green synthesized silver nanoparticles using cell extract of Nostoc sp. strain HKAR-2

Authors Affiliation(s)

  • Laboratory of Photobiology and Molecular Microbiology, Centre of Advanced Study in Botany, Institute of Science, Banaras Hindu University, Varanasi 221005, INDIA

Can J Biotech, Volume 1, Issue 1, Pages 26-37, DOI: https://doi.org/10.24870/cjb.2017-000103

Received: Dec 26, 2016; Revised: Mar 04, 2017; Accepted: Mar 16, 2017

Abstract

In the present study we have made an attempt to develop an eco-friendly, cheap and convenient biological (green) method for the synthesis of silver nanoparticles (AgNPs) using the cell extract of the cyanobacterium Nostoc sp. strain HKAR-2. Their anticancerous, antifungal and antibacterial properties were also studied against MCF-7 cells, two fungal strains (Aspergillus niger and Trichoderma harzianum) and two plant bacterial strains (Ralstonia solanacearum and Xanthomonas campestris), respectively. The structural, morphological and optical properties of green synthesized AgNPs were determined by UV-VIS spectroscopy, Fourier transform infrared (FTIR) spectroscopy, X-ray diffraction, transmission electron microscopy selected area electron diffraction (TEM-SAED) and scanning electron microscopy (SEM). Spectroscopic analysis showed the peak at 419 nm due to the reduction of AgNO3 into silver ion by cyanobacterial extract indicating surface plasmon resonance (SPR) of the synthesized AgNPs. The XRD pattern of AgNPs showed the characteristic Bragg peaks at (111), (200), (220) and (311) facets of the face centre cubic (fcc) confirming their crystalline nature. FTIR analysis revealed that proteins and amino acids are responsible for the reduction of AgNO3 into Ag+ as well as for the stability of nanoparticles. Zeta potential confirmed that the charge on the nanoparticles is 1.80 mV which indicates the presence of stable nanoparticles. The results of SEM and TEM confirmed the large agglomerated shape of AgNPs with size ranging between 51-100 nm. The AgNPs showed a dose-dependent cytotoxic activity against human breast cancer MCF-7 cells with IC50 of 27.5 µg/ml. They also exhibited excellent antibacterial and antifungal activities.

References

  1. Wang, X., Yang, L., Chen, Z.G. and Shin, D.M. (2008) Application of nanotechnology in cancer therapy and imaging. CA Cancer J Clin 58: 97-110. Crossref
  2. Cuenya B.R. (2010) Synthesis and catalytic properties of metal nanoparticles: Size, shape, support, composition, and oxidation state effects. Thin Solid Films 518: 3127-3150. Crossref
  3. Kim, J.S., Kuk, E., Yu, K.N., Kim, J.H., Park, S.J., Lee, H.J., Kim, S.H., Park, Y.K., Park, Y.H., Hwang, C.Y., Kim, Y.K., Lee, Y.S., Jeong, D.H. and Cho, M.H. (2007) Antimicrobial effects of silver nanoparticles. Nanomed Nanotech Biol Med 3: 95-101. Crossref
  4. Kumar, V., Yadav, S.C. and Yadav, S.K. (2010) Syzygium cumini leaf and seed extract mediated biosynthesis of silver nanoparticles and their characterization. J Chem Technol Biotechnol 85: 1301-1309. Crossref
  5. Rajasekharreddy, P., Rani, P.U. and Sreedhar, B. (2010) Qualitative assessment of silver and gold nanoparticle synthesis in various plants: a photobiological approach. J Nanopart Res 12: 1711-1721. Crossref
  6. Tripathy, A., Raichur, A.M., Chandrasekaran, N., Prathna, T.C. and Mukherjee, A. (2010) Process variables in biomimetic synthesis of silver nanoparticles by aqueous extract of Azadirachta indica (Neem) leaves. J Nanopart Res 12: 237-246. Crossref
  7. Saravanan, M. and Nanda, A. (2010) Extracellular synthesis of silver bionanoparticles from Aspergillus clavatus and its antimicrobial activity against MRSA and MRSE. Colloids Surf B Biointerfaces 77: 214-218. Crossref
  8. Saravanan, M., Vemu, A.K. and Barik, S.K. (2011) Rapid biosynthesis of silver nanoparticles from Bacillus megaterium (NCIM 2326) and their antibacterial activity on multi drug resistant clinical pathogens. Colloids Surf B Biointerfaces 88: 325-331. Crossref
  9. Singh, G., Babele, P.K., Shahi, S.K., Sinha, R.P., Tyagi, M.B. and Kumar, A. (2014) Green synthesis of silver nanoparticles using cell extracts of Anabaena doliolum and screening of its antibacterial and antitumor activity. J Microbiol Biotechnol 24: 1354-1367.
  10. Shankar, S.S., Rai, A., Ahmad, A. and Sastry, M. (2004) Rapid synthesis of Au, Ag, and bimetallic Au core-Ag shell nanoparticles using Neem (Azadirachta indica) leaf broth. J Colloid Interface Sci 275: 496-502. Crossref
  11. Vilchis-Nestor, A.R., Sµnchez-Mendieta, V., Camacho-Lµpez, M.A., Gµmez-Espinosa, R.M., Camacho-Lµpez, M.A. and Arenas-Alatorre, J.A. (2008) Solventless synthesis and optical properties of Au and Ag nanoparticles using Camellia sinensis extract. Mater Lett 62: 3103-3105. Crossref
  12. Bhattacharya, D. and Gupta, R.K. (2005) Nanotechnology and potential of microorganisms. Crit Rev Biotechnol 25: 199-204. Crossref
  13. Mohanpuria, P., Rana, N.K. and Yadav, S.K. (2008) Biosynthesis of nanoparticles: technological concepts and future applications. J Nanopart Res 10: 507-517. Crossref
  14. Sastry, M., Ahmad, A., Khan, M.I., Kumar, R. (2004) ́Microbial nanoparticle productionµ. In Nanobiotechnology (Niemeyer CM, Mirkin CA, Eds). Wiley-VCH, Weinheim, Germany. 126-135.
  15. Klaus, T., Joerger, R., Olsson, E. and Granqvist, C.G. (1999) Silver-based crystalline nanoparticles, microbially fabricated. Proc Natl Acad Sci USA 96: 13611-13614. Crossref
  16. Konishi, Y., Ohno, K., Saitoh, N., Nomura, T., Nagamine, S., Hishida, H., Takahashi, Y. and Uruga, T. (2007) Bioreductive deposition of platinum nanoparticles on the bacterium Shewanella algae. J Biotechnol 128: 648-653. Crossref
  17. Nair, B. and Pradeep, T. (2002) Coalescence of nanoclusters and formation of submicron crystallites assisted by Lactobacillus strains. Cryst Growth Des 2: 293-298. Crossref
  18. Sudha, S.S., Rajamanickam, K. and Rengaramanujam, J. (2013) Microalgae mediated synthesis of silver nanoparticles and their antibacterial activity against pathogenic bacteria. Indian.J Exp Biol 52: 393-399.
  19. Singh, G., Babele, P.K., Kumar, A., Srivastava, A., Sinha, R.P. and Tyagi, M.B. (2014) Synthesis of ZnO nanoparticles using the cell extract of the cyanobacterium, Anabaena strain L31 and its conjugation with UV-B absorbing compound shinorine. J Photochem Photobiol B 138: 55-62. Crossref
  20. Willner, I., Baron, R. and Willner, B. (2006) Growing metal nanoparticles by enzymes. Adv Mater 18: 1109-1120. Crossref
  21. Vigneshwaran, N., Ashtaputre, N.M., Varadarajan, P.V., Nachane, R.P., Paralikar, K.M. and Balasubramanya, R.H. (2007) Biological synthesis of silver nanoparticles using the fungus Aspergillus flavus. Mater Lett 61: 1413-1418. Crossref
  22. Chandran, S.P., Chaudhary, M., Pasricha, R., Ahmad, A. and Sastry, M. (2006) Synthesis of gold nanotriangles and silver nanoparticles using Aloe vera plant extract. Biotechnol Prog 22: 577-583. Crossref
  23. Song, J.Y. and Kim, B.S. (2009) Rapid biological synthesis of silver nanoparticles using plant leaf extracts. Bioprocess Biosyst Eng 32: 79-84. Crossref
  24. Shankar, S.S., Rai, A., Ankamwar, B., Singh, A., Ahmad, A. and Sastry, M. (2004) Biological synthesis of triangular gold nanoprisms. Nat Mater 3: 482-488. Crossref
  25. Ghani, A (1998) Medicinal Plants of Bangladesh, Asiatic Society Dhaka, 1st edition, pp: 13.
  26. Kubyshkin, A., Chegodar, D., Katsev, A., Petrosyan, A., Krivorutchenko, Y. and Postnikova, O. (2016) Antimicrobial effects of silver nanoparticles stabilized in solution by sodium alginate. Biochem Mol Biol J 2: 13. Crossref
  27. Shah, M.S.A.S., Nag, M., Kalagara, T., Singh, S. and Manorama, S.V. (2008) Silver on PEG-PU-TiO2 polymer nanocomposite films: An excellent system for antibacterial applications. Chem Mater 20: 2455-2460. Crossref
  28. Ali, D.M., Sasikala, M., Gunasekaran, M. and Thajuddin, N. (2011) Biosynthesis and characterization of silver nanoparticles using marine cyanobacterium, Oscillatoria willei NTDM01. Dig J Nanomater Biostruct 6: 385-390.
  29. Liu, L., Shao, Z., Ang, H.M., Tadµ, M.O. and Liu, S. (2014) Are microorganisms indispensable in green microbial nanomaterial synthesis? RSC Adv 4: 14564-14568. Crossref
  30. Otari, S.V., Patil, R.M., Nadaf, N.H., Ghosh, S.J. and Pawar, S.H. (2014) Green synthesis of silver nanoparticles by microorganism using organic pollutant: its antimicrobial and catalytic application. Environ Sci Pollut Res Int 21: 1503-1513. Crossref
  31. Prasad, T.N., Kambala, V.S.R. and Naidu, R. (2013) Phyconanotechnology: synthesis of silver nanoparticles using brown marine algae Cystophora moniliformis and their characterization. J Appl Phycol 25: 177-182. Crossref
  32. Sharma, V.K., Yngard, R.A. and Lin, Y. (2009) Silver nanoparticles: green synthesis and their antimicrobial activities. Adv Colloid Interface Sci 145: 83-96. Crossref
  33. MubarakAli, D., Gopinath, V., Rameshbabu, N. and Thajuddin, N (2012) Synthesis and characterization of CdS nanoparticles using C-phycoerythrin from the marine cyanobacteria. Mater Lett 74: 8-11. Crossref
  34. Shahverdi, A.R., Minaeian, S., Shahverdi, H.R., Jamalifar, H. and Nohi, A.A. (2007) Rapid synthesis of silver nanoparticles using culture supernatants of Enterobacteria: a novel biological approach. Process Biochem 42: 919-923. Crossref
  35. Rippka, R., Deruelles, J., Waterbury, J.B., Herdman, M. and Stanier, R.Y. (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. Microbiology 111: 1-61. Crossref
  36. Soni, B., Visavadiya, N.P., Dalwadi, N., Madamwar, D., Winder, C. and Khalil, C. (2010) Purified C‐phycoerythrin: safety studies in rats and protective role against permanganate‐mediated fibroblast‐DNA damage. J Appl Toxicol 30: 542-550. Crossref
  37. Lengke, M.F., Fleet, M.E. and Southam, G. (2007) Biosynthesis of silver nanoparticles by filamentous cyanobacteria from a silver (I) nitrate complex. Langmuir 23: 2694-2699. Crossref
  38. Brayner, R., Barberousse, H., Hernadi, M., Djedjat, C., Yepremian, C., Coradin, T., Livage, J., Fievet, F. and Coute, A. (2007) Cyanobacteria as bioreactors for the synthesis of Au, Ag, Pd, and Pt nanoparticles via an enzyme-mediated route. J Nanosci Nanotechnol 7: 2696-2708.
  39. Mahdieha, M., Zolanvari A., Azimeea, A.S. and Mahdiehc M. (2012) Green biosynthesis of silver nanoparticles by Spirulina platensis. Sci Iran 19: 926-929. Crossref
  40. Ardelean, I.I. (2015) Metallic nanoparticle synthesis by cyanobacteria: fundamentals and applications. In: The Algae World. Springer, Netherlands, pp. 429-448.
  41. Husain, S., Sardar, M. and Fatma, T. (2015) Screening of cyanobacterial extracts for synthesis of silver nanoparticles. World J Microbiol Biotechnol 31: 1279-1283. Crossref
  42. Lakshmi, P.T.V., Priyanka, D. and Annamalai, A. (2015) Reduction of silver ions by cell free extracts of Westiellopsis sp. Int J Biomater 539494. Crossref
  43. Kaliamurthi, S., Selvaraj, G., µakmak, Z.E. and µakmak, T. (2016) Production and characterization of spherical thermostable silver nanoparticles from Spirulina platensis (Cyanophyceae). Phycologia 55: 568-576. Crossref
  44. Keskin, N.O.S., Kiliµ, N.K., Dµnmez, G. and Tekinay, T. (2016) Green synthesis of silver nanoparticles using cyanobacteria and evaluation of their photocatalytic and antimicrobial activity. J Nano Res 40: 120-127. Crossref
  45. Roychoudhury, P., Ghosh, S. and Pal, R. (2016). Cyanobacteria mediated green synthesis of gold-silver nanoalloy. J Plant Biochem Biotechnol 25: 73-78. Crossref
  46. Sharma, A., Sharma, S., Sharma, K., Chetri, S.P.K., Vashishtha, A., Singh, P., Kumar, R., Rathi, B. and Agrawal, V. (2016) Algae as crucial organisms in advancing nanotechnology: a systematic review. J Appl Phycol 28: 1759-1774. Crossref
  47. Rastogi, R.P., Kumari, S., Han, T. and Sinha, R.P. (2012) Molecular characterization of hot spring cyanobacteria and evaluation of their photoprotective compounds. Can J Microbiol 58: 719-727. Crossref
  48. Kedia, A., Prakash, B., Mishra, P.K. and Dubey, N.K. (2014) Antifungal and antiaflatoxigenic properties of Cuminum cyminum (L.) seed essential oil and its efficacy as a preservative in stored commodities. Int J Food Microbiol 168: 1-7. Crossref
  49. Parashar, U.K., Kumar, V., Bera, T., Saxena, P.S., Nath, G., Srivastava, S.K., Giri, R. and Srivastava, A. (2011) Study of mechanism of enhanced antibacterial activity by green synthesis of silver nanoparticles. Nanotechnology 22: 415104-415117. Crossref
  50. Von White, G., Kerscher, P., Brown, R.M., Morella, J.D., McAllister, W., Dean, D. and Kitchens, C.L. (2012) Green synthesis of robust, biocompatible silver nanoparticles using garlic extract. J Nanomater 730746. Crossref
  51. Choi, H.S., Liu, W., Misra, P., Tanaka, E., Zimmer, J.P., Ipe, B.I., Bawendi, M.G. and Frangioni, J.V. (2007) Renal clearance of quantum dots. Nat Biotechnol 25: 1165-1170. Crossref
  52. Shrivastava, S., Bera, T., Roy, A., Singh, G., Ramachandrarao, P. and Dash, D. (2007) Characterization of enhanced antibacterial effects of novel silver nanoparticles. Nanotechnology 18: 225103. Crossref
  53. Muller, R. and Akkar, A. (2004) Drug nanocrystals of poorly soluble drugs. In Encyclopedia of nanoscience and nanotechnology (H.S. Nalwa, Ed). American Scientific Publishers, Stevenson Ranch, 627-638.
  54. Vivek, R., Thangam, R., Muthuchelian, K., Gunasekaran, P., Kaveri, K. and Kannan, S. (2012) Green biosynthesis of silver nanoparticles from Annona squamosa leaf extract and its in vitro cytotoxic effect on MCF-7 cells. Process Biochem 47: 2405-2410. Crossref
  55. Sanpui, P., Chattopadhyay, A. and Ghosh, S.S. (2011) Induction of apoptosis in cancer cells at low silver nanoparticle concentrations using chitosan nanocarrier. ACS Appl Mater Interfaces 3: 218-228. Crossref
  56. Hsueh, Y.H., Lin, K.S., Ke, W.J., Hsieh, C.T., Chiang, C.L., Tzou, D.Y. and Liu. S.T. (2015) The antimicrobial properties of silver nanoparticles in Bacillus subtilis are mediated by released Ag+ ions. PLoS ONE 10: e0144306. Crossref
  57. Li, P., Li, J., Wu, C., Wu, Q. and Li, J. (2005) Synergistic antibacterial effects of β-lactam antibiotic combined with silver nanoparticles. Nanotechnology 16: 1912-1917.
  58. Nowack, B., Krug, H.F. and Height, M. (2011) 120 years of nanosilver history: implications for policy makers. Environ Sci Technol 45: 1177-1183. Crossref
  59. Duran, N., Marcato, P.D., De Souza, G.I., Alves, O.L. and Esposito, E. (2007) Antibacterial effect of silver nanoparticles produced by fungal process on textile fabrics and their effluent treatment. J Biomed Nanotechnol 3: 203-208. Crossref
  60. Saha, S., Sarkar, J., Chattopadhyay, D., Patra, S., Chakraborty, A. and Acharya, K. (2010) Production of silver nanoparticles by a phytopathogenic fungus Bipolaris nodulosa and its antimicrobial activity. Dig J Nanomater Biostruct 5: 887-895.
  61. Nel, A., Xia, T., Mµdler, L. and Li, N. (2006) Toxic potential of materials at the nanolevel. Science 311: 622-627. Crossref
  62. E Lin. Y.S., Vidic, R.D., Stout, J.E., McCartney, C.A. and Yu, V.L. (1998) Inactivation of Mycobacterium avium by copper and silver ions. Water Res 32: 1997-2000. Crossref
  63. Sondi, I. and Salopek-Sondi, B. (2004) Silver nanoparticles as antimicrobial agent: a case study on E. coli as a model for Gram-negative bacteria. J Colloid Interface Sci 275: 177-182. Crossref