Advertisement

Environmental Science and Pollution Research

, Volume 25, Issue 11, pp 10250–10263 | Cite as

Exploiting fruit byproducts for eco-friendly nanosynthesis: Citrus × clementina peel extract mediated fabrication of silver nanoparticles with high efficacy against microbial pathogens and rat glial tumor C6 cells

  • Rijuta Ganesh Saratale
  • Han-Seung Shin
  • Gopalakrishnan Kumar
  • Giovanni Benelli
  • Gajanan S. Ghodake
  • Yuan Yuan Jiang
  • Dong Su Kim
  • Ganesh Dattatraya Saratale
Plant-borne compounds and nanoparticles: challenges for medicine, parasitology and entomology

Abstract

Process byproducts from the fruit industry may represent a cheap and reliable source of green reducing agents to be used in current bio-nanosynthesis. This study reports the use of orange (Citrus × clementina) peel aqueous extract (OPE) for one-pot green synthesis of silver nanoparticles (AgNPs) with high effectiveness against various microbial pathogens as well as rat glial tumor C6 cells. The effects of various operational parameters on the synthesis of AgNPs were systematically investigated. The morphology, particle size, and properties of synthesized AgNPs were characterized using UV–visible spectroscopy, x-ray diffraction, x-ray photoelectron spectroscopy, field emission scanning electron microscopy, energy-dispersive x-ray spectroscopy, and Fourier transform infrared spectroscopy. High-resolution transmission electron microscopy shows that the nanoparticles are mostly spherical in shape and monodispersed, with an average particle size of 15–20 nm. Notably, the OPE-synthesized AgNPs were stable up to 6 months without change in their properties. Low doses of OPE-AgNPs inhibited the growth of human pathogens Escherichia coli, Bacillus cereus, and Staphylococcus aureus. The minimum inhibitory concentration and minimum bactericidal concentration of AgNPs against selected pathogenic bacteria were determined. OPE-AgNPs exhibited strong antioxidant activity in terms of ABTS (2,2′-azino-bis (3-ethylbenzothiazoline-6-sulfonic acid)) radical scavenging (IC50 49.6 μg/mL) and DPPH (1,1-diphenyl-2-picrylhydrazyl) radical scavenging (IC50 63.4 μg/mL). OPE-AgNPs showed dose-dependent response against rat glial tumor C6 cells (LD50 60 μg/mL) showing a promising potential as anticancer agents. Overall, the current investigation highlighted a cheap green technology route to synthesize AgNPs using OPE byproducts and could potentially be utilized in biomedical, cosmetic, and pharmaceutical industry.

Keywords

Green synthesis Orange peel extract In vitro cytotoxicity ABTS and DPPH free radical scavenging activity Antimicrobial activity HR-TEM 

Notes

Acknowledgements

This research was supported by the Agricultural Research Center funded by the Ministry of Food, Forestry, and Fisheries, Korea. One of the author GK acknowledges Korea Research Fellowship Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Science, ICT and Future Planning (Grant No: 2016H1D3A1908953). The authors would like to thank Prof. Shrikrishna D. Sartale, Department of Physics, Savitribai Phule Pune University, India, for availing the HR-TEM facility. The authors are also thankful to Mr. Oh Sung-Taek, Dongguk University, for his technical help during anticancer studies.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.

References

  1. Ahmed S, Ahmad M, Swami BL, Ikram S (2016) A review on plants extract mediated synthesis of silver nanoparticles for antimicrobial applications: a green expertise. J Adv Res 7:17–28CrossRefGoogle Scholar
  2. Ajitha B, Reddy AKY, Reddy SP (2014) Biogenic nano-scale silver particles by Tephrosia purpurea leaf extract and their inborn antimicrobial activity. Spectrochim Acta Part A 121:164–172CrossRefGoogle Scholar
  3. Atiyeh BS, Costagliola M, Hayek SN, Dibo SA (2007) Effect of silver on burn wound infection control and healing: review of the literature. Burns 33:139–148Google Scholar
  4. Bae JT, Ko HJ, Kim GB, Pyo HB, Lee GS (2012) Protective effects of fermented Citrus unshiu peel extract against ultraviolet-A-induced photoageing in human dermal fibrobolasts. Phytother Res 26:1851–1856CrossRefGoogle Scholar
  5. Balan K, Qing W, Wang Y, Ma F, Zhang Y (2016) Antidiabetic activity of silver nanoparticles from green synthesis using Lonicera japonica leaf extract. RSC Adv 6:40162CrossRefGoogle Scholar
  6. Basavegowda N, Lee YR (2013) Synthesis of silver nanoparticles using Satsuma mandarin (Citrus unshiu) peel extract: a novel approach towards waste utilization. Mater Lett 109:31–33CrossRefGoogle Scholar
  7. Bauer AW, Kirby WMM, Sherris JC, Turck M (1966) Antibiotic susceptibility testing by standardized single disc method. Am J Clin Pathol 45:493–496CrossRefGoogle Scholar
  8. Benelli G (2016a) Plant-mediated biosynthesis of nanoparticles as an emerging tool against mosquitoes of medical and veterinary importance: a review. Parasitol Res 115:23–34CrossRefGoogle Scholar
  9. Benelli G (2016b) Green synthesized nanoparticles in the fight against mosquito-borne diseases and cancer—a brief review. Enzyme Microbial Technol. doi: 10.1016/j. enzmictec.2016.08.022 Google Scholar
  10. Bocco M, Cuvelier E, Richard H (1998) Antioxidant activity and phenolic composition of citrus peel and seed extracts. J Agric Food Chem 46:2123–2129CrossRefGoogle Scholar
  11. Devanesan S, AlSalhi MS, Vishnubalaji R, Alfuraydi AA, Alajez NM, Alfayez M, Murugan K, Sayed SRM, Nicoletti M, Benelli G (2016) Rapid biological synthesis of silver nanoparticles using plant seed extracts and their cytotoxicity on colorectal cancer cell lines. J Clust Sci. doi: 10.1007/s10876-016-1134-4 Google Scholar
  12. Ekar SU, Ganga S, Khollam YB, Wani PN, Jadkar SR, Chaskar MG, Jadhav SS, Fadel A, Jadhav VV, Shendkar JH, Mane RS (2016) Green synthesis and dye-sensitized solar cell application of rutile and anatase TiO2 nanorods. J Solid State Electrochem. doi: 10.1007/s10008-016-3376-3 Google Scholar
  13. Etxeberria U, De La Garza AL, Campin J, Martnez JA, Milagro FI (2012) Antidiabetic effects of natural plant extracts via inhibition of carbohydrate hydrolysis enzymes with emphasis on pancreatic alpha amylase. Expert Opin Ther Tar 16:269–297Google Scholar
  14. Ghaedi M, Yousefinejad M, Safarpoor M, Zare KH, Purkait MK (2015) Rosmarinus officinalis leaf extract mediated green synthesis of silver nanoparticles and investigation of its antimicrobial properties. J Ind Eng Chem 31:167–172CrossRefGoogle Scholar
  15. Gurunathan S, Han JW, Dayem AA, Eppakayala V, Park JH, Cho SG, Lee KJ, Kim JH (2013) Green synthesis of anisotropic silver nanoparticles and its potential cytotoxicity in human breast cancer cells (MCF-7). J Ind Eng Chem 19:1600–1605CrossRefGoogle Scholar
  16. Jang SJ, Yang IJ, Tettey CO, Kim KM, Shin HM (2016) In-vitro anticancer activity of green synthesized silver nanoparticles on MCF-7 human breast cancer cells. Mater Sci Eng C 68:430–435CrossRefGoogle Scholar
  17. Kanchi S, Kumar G, Lo AY, Tseng CM, Chen SK, Lin CY, Chin TS (2014) Exploitation of de-oiled jatropha waste for gold nanoparticles synthesis: a green approach. Arab J Chem. doi: 10.1016/j.arabjc.2014.08.006 Google Scholar
  18. Kaviya S, Santhanalakshmi J, Viswanathan B, Muthumar J, Srinivasan K (2011) Biosynthesis of silver nanoparticles using Citrus sinensis peel extract and its antibacterial activity. Spectrochim Acta A 79:594–598CrossRefGoogle Scholar
  19. Kim JS, Kuk E, Yu KN, Kim JH, Park SJ, Lee HJ, Kim SH, Park YK, Park YH, Hwang CY, Kim YK, Lee YS, Jeong DH, Cho MH (2007) Antimicrobial effects of silver nanoparticles. Nanomed Nanotechnol 3:95–101CrossRefGoogle Scholar
  20. Kora AJ, Sashidhar RB, Arunachalam J (2010) Gum kondagogu (Cochlospermum gossypium): a template for the green synthesis and stabilization of silver nanoparticles with antibacterial application. Carbohydr Polym 82:670–679CrossRefGoogle Scholar
  21. Krishnan P, Yan KJ, Windler D, Tubbs J, Grand R, Li BDL, Aldaz CM, McLarty J, Kleiner-Hancock HE (2009) Citrus auraptene suppresses cyclin D1 and significantly delays N-methyl nitrosourea induced mammary carcinogenesis in female Sprague–Dawley rats. BMC Cancer 9:259CrossRefGoogle Scholar
  22. Kumar B, Smita K, Cumbal L, Camacho J, Hernández-Gallegos E, Chávez MG, López Grijalva M, Andrade K (2016) One pot phytosynthesis of gold nanoparticles using Genipa americana fruit extract and its biological applications. Mater Sci Eng C 62C:725–731CrossRefGoogle Scholar
  23. Lee KJ, Park SH, Govarthanan M, Hwang PH, Seo YS (2013) Synthesis of silver nanoparticles using cow milk and their antifungal activity against phytopathogens. Mater Lett 105:128–131CrossRefGoogle Scholar
  24. Lee KD, Nagajyothi PC, Sreekanth TVM, Park SH (2015) Eco-friendly synthesis of gold nanoparticles (AuNPs) using Inonotus obliquus and their antibacterial, antioxidant and cytotoxic activities. J Ind Eng Chem 26:67–72CrossRefGoogle Scholar
  25. Logeswari P, Silambarasan S, Abraham J (2015) Synthesis of silver nanoparticles using plants extract and analysis of their antimicrobial property. J Saudi Chem Soc 19:311–317CrossRefGoogle Scholar
  26. Makarov VV, Love AJ, Sinitsyna OV, Makarova SS, Yaminsky IV, Taliansky ME, Kalinina NO (2014) Green nanotechnologies: synthesis of metal nanoparticles using plants. Acta Nat 6:35–44Google Scholar
  27. Martins D, Frungillo L, Anazzetti MC, Melo PS, Duran N (2010) Antitumoral activity of L-ascorbic acid-poly-D,L-(lactide-co-glycolide) nanoparticles containing violacein. Int J Nanomedicine 5:77–85CrossRefGoogle Scholar
  28. Mata R, Nakkala JR, Sadras SR (2015) Biogenic silver nanoparticles from Abutilon indicum: Their antioxidant, antibacterial and cytotoxic effects in vitro. Colloid Surface B 128:276–286Google Scholar
  29. Mittal K, Chisti Y, Banerjee UC (2013) Synthesis of metallic nanoparticles using plant extracts. Biotechnol Adv 31:346–356CrossRefGoogle Scholar
  30. Moldovan B, David L, Achim M, Clichici S, Filip GA (2016) A green approach to phytomediated synthesis of silver nanoparticles using Sambucus nigra L. fruits extract and their antioxidant activity. J Mol Liq 221:271–278Google Scholar
  31. Moharram FA, Marzouk MSA, Ibrahim MT, Marby TJ (2006) Antioxidant galloylated flavonol glycosides from Calliandra haematocephala. Nat Prod Res 20:927–934CrossRefGoogle Scholar
  32. Morones JR, Elechiguerra JL, Camacho A, Holt K, Kouri JB, Ramírez JT, Yacaman MJ (2005) The bactericidal effect of silver nanoparticles. Nanotechnol 16:2346–2353CrossRefGoogle Scholar
  33. Nazeruddin GM, Prasad NR, Waghmare SR, Garadkar KM, Mulla IS (2014) Extracellular biosynthesis of silver nanoparticle using Azadirachta indica leaf extract and its anti-microbial activity. J Alloys Compd 583:272–277CrossRefGoogle Scholar
  34. Niraimathi KL, Sudha V, Lavanya R, Brindha P (2013) Biosynthesis of silver nanoparticles using Alternanthera sessilis (Linn.) extract and their antimicrobial, antioxidant activities. Colloids Surf B: Biointerfaces 102:288–291CrossRefGoogle Scholar
  35. Nirmala JG, Akila S, Nadar MSAM, Narendhirakannan RT, Chatterjee S (2016) Biosynthesized Vitis vinifera seed gold nanoparticles induce apoptotic cell death in A431 skin cancer cells. RSC Adv 6:82205CrossRefGoogle Scholar
  36. Otari SV, Patil RM, Ghosh SJ, Pawar SH (2014) Green phytosynthesis of silver nanoparticles using aqueous extract of Manilkara zapota (L.) seeds and its inhibitory action against Candida species. Mater Lett 116:367–369CrossRefGoogle Scholar
  37. Pal S, Tak YK, Song JM (2007) Does the antibacterial activity of silver nanoparticles depend on the shape of the nanoparticle? A study of the Gram-negative bacterium Escherichia coli? Appl Environ Microbiol 73:1712–1720CrossRefGoogle Scholar
  38. Pavela R, Murugan K, Canale A, Benelli G (2017) Saponaria officinalis-synthesized silver nanocrystals as effective biopesticides and oviposition inhibitors against Tetranychus urticae Koch. Ind Crop Prod 97:338–344CrossRefGoogle Scholar
  39. Peer D, Karp JM, Hong S, Farokhzad OC, Margalit R, Langer R (2007) Nanocarriers as an emerging platform for cancer therapy. Nat Nanotechnol 2:751–760Google Scholar
  40. Pugazhendhi S, Sathya P, Palanisamy PK, Gopalakrishnan R (2016) Synthesis of silver nanoparticles through green approach using Dioscorea alata and their characterization on antibacterial activities and optical limiting behavior. J Photochem Photobiol B 159:155–160CrossRefGoogle Scholar
  41. Rajan R, Chandranb K, Harper SL, Yun S-I, Kalaichelvan PT (2015) Plant extract synthesized silver nanoparticles: an ongoing source of novel biocompatible materials. Ind Crop Prod 70:356–373CrossRefGoogle Scholar
  42. Ravichandran V, Vasanthi S, Shalini S, Ali Shah SA, Harish R (2016) Green synthesis of silver nanoparticles using Atrocarpus altilis leaf extract and the study of their antimicrobial and antioxidant activity. Mater Lett 180:264–267CrossRefGoogle Scholar
  43. Ruparelia JP, Chatterjee AK, Duttagupta SP, Mukherji S (2008) Strain specificity in antimicrobial activity of silver and copper nanoparticles. Acta Biomater 4:707–716CrossRefGoogle Scholar
  44. Sankar R, Karthik A, Prabu A, Karthik S, Shivashangari KS, Ravikumar V (2013) Origanum vulgare mediated biosynthesis of silver nanoparticles for its antibacterial and anticancer activity. Colloid Surface B: Biointerfaces 108:80–84CrossRefGoogle Scholar
  45. Saratale GD, Saratale RG, Benelli G, Kumar G, Pugazhendhi A, Kim DS, Shin HS (2017) Anti-diabetic potential of silver nanoparticles synthesized with Argyreia nervosa leaf extract high synergistic antibacterial activity with standard antibiotics against foodborne bacteria. J Clust Sci. doi: 10.1007/s10876-017-1179-z Google Scholar
  46. Sathiya CK, Akilandeswari S (2014) Fabrication and characterization of silver nanoparticles using Delonix elata leaf broth. Spectrochim Acta Part A Mol Biomol Spectrosc 128:337–341CrossRefGoogle Scholar
  47. Sriranjani R, Srinithya B, Vellingiri V, Brindha P, Anthony SP, Sivasubramanian A, Muthuraman MS (2016) Silver nanoparticle synthesis using Clerodendrum phlomidis leaf extract and preliminary investigation of its antioxidant and anticancer activities. J Mol Liq 220:926–930CrossRefGoogle Scholar
  48. Syed A, Ahmad A (2012) Extracellular biosynthesis of platinum nanoparticles using the fungus Fusarium oxysporum. Coll Surf B Biointerfaces 97:27–31CrossRefGoogle Scholar
  49. Thatoi P, Kerry RG, Gouda S, Das G, Pramanik K, Thatoi H, Patra JK (2016) Photo-mediated green synthesis of silver and zinc oxide nanoparticles using aqueous extracts of two mangrove plant species, Heritiera fomes and Sonneratia apetala and investigation of their biomedical applications. J Photochem Photobiol B 163:311–318CrossRefGoogle Scholar
  50. Velmurugan P, Lee SM, Cho M, Park JH, Seo SK, Myung H, Bang KS, Oh BT (2014) Antibacterial activity of silver nanoparticle-coated fabric and leather against odor and skin infection causing bacteria. Appl Microbiol Biotechnol 98:8179–8189CrossRefGoogle Scholar
  51. Velmurugan P, Cho M, Lim SS, Seo SK, Myung H, Bang KS, Sivakumar S, Cho KM, Oh BT (2015) Phytosynthesis of silver nanoparticles by Prunus yedoensis leaf extract and their antimicrobial activity. Mater Lett 138:272–275CrossRefGoogle Scholar
  52. Venkatpurwar V, Pokharkar V (2011) Green synthesis of silver nanoparticles using marine polysaccharide: study of in-vitro antibacterial activity. Mater Lett 65:999–1002CrossRefGoogle Scholar
  53. Vijayaraghavan K, Nalini SPK, Prakash NU, Madhankumar D (2012) Biomimetic synthesis of silver nanoparticles by aqueous extract of Syzygium aromaticum. Mater Lett 75:33–35CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Rijuta Ganesh Saratale
    • 1
  • Han-Seung Shin
    • 2
  • Gopalakrishnan Kumar
    • 3
  • Giovanni Benelli
    • 4
  • Gajanan S. Ghodake
    • 5
  • Yuan Yuan Jiang
    • 6
  • Dong Su Kim
    • 7
  • Ganesh Dattatraya Saratale
    • 2
  1. 1.Research Institute of Biotechnology and Medical Converged ScienceDongguk University–SeoulGoyang-siRepublic of Korea
  2. 2.Department of Food Science and BiotechnologyDongguk University–SeoulGoyang-siRepublic of Korea
  3. 3.Department of Environmental EngineeringDaegu UniversityGyeongsanRepublic of Korea
  4. 4.Department of Agriculture, Food and EnvironmentUniversity of PisaPisaItaly
  5. 5.Department of Biological and Environmental ScienceDongguk UniversityGoyang-siRepublic of Korea
  6. 6.Department of Medical BiotechnologyDongguk UniversityGoyang-siRepublic of Korea
  7. 7.Department of Environmental Science and EngineeringEwha Womans UniversitySeoulRepublic of Korea

Personalised recommendations