Extracellular biosynthesis of silver nanoparticles from Penicillium italicum and its antioxidant, antimicrobial and cytotoxicity activities

  • Zainab K. Taha
  • Sumaiya N. Hawar
  • Ghassan M. SulaimanEmail author
Original Research Paper



The synthesis of silver nanoparticles and its antioxidant, antimicrobial and cytotoxic activities was investigated and extracellularly biosynthesized using Penicillium italicum isolated from Iraqi lemon fruits.


The formation of synthesized nanoparticles was observed after 72 h of incubation. Color changing, ultraviolet and visible spectrum, X-ray diffraction, Fourier transform infrared spectroscopy, scanning electron microscopy, transmission electron microscopy and energy dispersive analysis X- ray confirmed the biosynthesis and characterization of silver nanoparticles. Ultraviolet and visible spectroscopy showed silver surface plasmon resonance band at 415 nm. X- ray diffraction showed that the particles were crystalline with face-centered cubic lattice phase and a size of 39.5 nm. Fourier transform infrared analysis shows the possible interactions between silver and bioactive molecules, which may be responsible for synthesis and stabilization of silver nanoparticles. Scanning electron microscopy imaging revealed different morphologies of the AgNPs, some of nanoparticles were close to spherical in shape, while others had platelet like structure, in size range between 32 and 100 nm. The transmission electron microscopy image demonstrated that AgNPs were spherical with a size < 50 nm. The biosynthesized silver nanoparticles were proved to be potential antioxidants by showing effective radical scavenging activity against 2, 2-diphenyl-1-picrylhydrazyl, hydroxyl radical and resazurin. The nanoparticles also showed potent antimicrobial activity against various pathogens, including bacteria and fungi as well as significant concentration-dependent cytotoxic effects against human breast cancer cells.


The powerful bioactivity of the synthesized silver nanoparticles recommends their biomedical use as antioxidant, antimicrobial as well as cytotoxic agents.


Penicillium italicum Silver nanoparticles Antioxidant Antimicrobial Cytotoxicity MCF-7 cells 


Author contributions

The authors alone are responsible for the content and writing of the paper.

Compliance with ethical standards

Conflicts of interest

The authors declare that there are no conflicts of interest.


  1. Ahmad A, Mukherjee P, Senapati S, Mandal D, Khan MI, Kumar R, Sastry M (2003) Extracellular biosynthesis of silver nanoparticles using the fungus Fusarium oxysporum. Colloids Surf B 28(4):313–318Google Scholar
  2. Al-Shmgani HSA, Mohammed WH, Sulaiman GM, Saadoon AH (2017) Biosynthesis of silver nanoparticles from Catharanthus roseus leaf extract and assessing their antioxidant, antimicrobial, and wound-healing activities. Artif Cells Nanomed Biotechnol 45(6):1234–1240Google Scholar
  3. Ammar HA, El-Desouky TA (2016) Green synthesis of nanosilver particles by Aspergillus terreus HA1 N and Penicillium expansum HA2 N and its antifungal activity against mycotoxigenic fungi. J Appl Microbiol 121(1):89–100Google Scholar
  4. Ammons MC, Ward LS, James GA (2011) Anti-biofilm efficacy of a lactoferrin/xylitol wound hydrogel used in combination with silver wound dressings. Int Wound J 8(3):268–273Google Scholar
  5. AshaRani PV, Low Kah Mun G, Hande MP, Valiyaveettil S (2009) Cytotoxicity and genotoxicity of silver nanoparticles in human cells. ACS Nano 3(2):279–290Google Scholar
  6. Balakumaran MD, Ramachandran R, Balashanmugam P, Mukeshkumar DJ, Kalaichelvan PT (2016) Mycosynthesis of silver and gold nanoparticles: optimization, characterization and antimicrobial activity against human pathogens. Microbiol Res 182:8–20Google Scholar
  7. Bhainsa KC, D’Souza SF (2006) Extracellular biosynthesis of silver nanoparticles using the fungus Aspergillus fumigatus. Colloids Surf B 47(2):160–164Google Scholar
  8. Bilal M, Tahir R, Iqbal HMN, Hu H, Zhang X (2017) Silver nanoparticles: biosynthesis and antimicrobial potentialities. Int J Pharmacol 13:832–845Google Scholar
  9. Boroumand Moghaddam A, Namvar F, Moniri M, Md Tahir P, Azizi S, Mohamad R (2015) Nanoparticles biosynthesized by fungi and yeast: a review of their preparation, properties, and medical applications. Molecules 20(9):16540–16565Google Scholar
  10. Choi O, Hu Z (2008) Size dependent and reactive oxygen species related nanosilver toxicity to nitrifying bacteria. Environ Sci Technol 42(12):4583–4588Google Scholar
  11. Devi SL, Donalad AB, Joshi SR (2014) Studies on biosynthesis of antimicrobial silver nanoparticles using endophytic fungi isolated from the ethno-medicinal plant Gloriosa superba L. Proc Natl Acad Sci India Sect B: Biol Sci 84(4):1091–1099Google Scholar
  12. Dhankhar S, Dhankhar S, Kumar S, Parkash Yadav J (2012) A novel and significant method for antioxidant activity utilizing microtitre-plate (resazurin reducing power assay). Curr Chem Biol 6(1):70–76Google Scholar
  13. Dubey M, Sharma S, Bhadauria S, Katoch VM (2012) Fungal biosynthesis of antimicrobioal nanosilver solution: a green approach. In: Srivastava MM, Khemani LD, Srivastava S (eds) Chemistry of phytoproteins: health energy environmental perspectives. Springer, Berlin, pp 53–57Google Scholar
  14. Duran N, Marcato PD, de Souza GIH, Alves OL, Esposito E (2007) Antibacterial effect of silver nanoparticles produced by fungal process on textile fabrics and their effluent treatment. J Biomed Nanotechnol 3(2):203–208Google Scholar
  15. El-Sonbaty SM (2013) Fungus-mediated synthesis of silver nanoparticles and evaluation of antitumor activity. Cancer Nanotechnol 4(4–5):73–79Google Scholar
  16. Feng QL, Wu J, Chen GQ, Cui FZ, Kim TN, Kim JO (2000) A mechanistic study of the antibacterial effect of silver ions on Escherichia coli and Staphylococcus aureus. J Biomed Mater Res 52(4):662–668Google Scholar
  17. Frisvad JC, Samson RA (2004) Polyphasic taxonomy of Penicillium subgenus Penicillium A guide to identification of food and air-borne terverticillate Penicillia and their mycotoxins. Stud Mycol 49(1):1–174Google Scholar
  18. Ghorbani HR, Molaei M (2017) Antibacterial nanocomposite preparation of polypropylene-Silver using Corona discharge. Prog Org Coat 112:187–190Google Scholar
  19. Ghorbani HR, Alizadeh V, Mehr FP, Jafarpourgolroudbary H, Erfan K, Yeganeh SS (2018) Preparation of polyurethane/CuO coating film and the study of antifungal activity. Prog Org Coat 123:322–325Google Scholar
  20. Govindappa M, Farheen H, Chandrappa CP, Channabasava R, Rai RV, Raghavendra VB (2016) Mycosynthesis of silver nanoparticles using extract of endophytic fungi, Penicillium species of Glycosmis mauritiana, and its antioxidant, antimicrobial, anti-inflammatory and tyrokinase inhibitory activity. Adv Nat Sci: Nanosci Nanotechnol 7:035014Google Scholar
  21. Gurunathan S, Kalishwaralal K, Vaidyanathan R, Deepak V, Pandian SRK, Muniyandi J (2009) Biosynthesis, purification and characterization of silver nanoparticles using Escherichia coli. Colloids Surf B 74(1):328–335Google Scholar
  22. Hafeli UO, Riffle JS, Harris-Shekhawat L, Carmichael-Baranauskas A, Mark F, Dailey JP, Bardenstein D (2009) Cell uptake and in vitro toxicity of magnetic nanoparticles suitable for drug delivery. Mol Pharm 6(5):1417–1428Google Scholar
  23. Honary S, Barabadi H, Gharaei-Fathabad E, Naghibi F (2013) Green synthesis of silver nanoparticles induced by the fungus Penicillium citrinum. Trop J Pharm Res 12(1):7–11Google Scholar
  24. Hotze EM, Phenrat T, Lowry GV (2010) Nanoparticle aggregation: challenges to understanding transport and reactivity in the environment. J Environ Qual 39(6):1909–1924Google Scholar
  25. Ishida K, Gustavo TF, Rocha M, Weissmuller G, Gomes F, Miranda K, Rozenta S (2014) Silver nanoparticle production by the fungus Fusarium oxysporum: nanoparticle characterisation and analysis of antifungal activity against pathogenic yeasts. Memórias do Instituto Oswaldo Cruz 109(2):220–228Google Scholar
  26. Ismail RA, Sulaiman GM, Mohsin MH, Saadoon AH (2018) Preparation of silver iodide nanoparticles using laser ablation in liquid for antibacterial applications. IET Nanobiotechnol. Google Scholar
  27. 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(2):635–641Google Scholar
  28. Kathiresan K, Manivannan S, Nabeal MA, Dhivya B (2009) Studies on silver nanoparticles synthesized by a marine fungus, Pencillium fellutanum isolated from coastal mangrove sediment. Colloids Surf B 71(1):133–137Google Scholar
  29. Kim S, Hyeong SL, Ryu S, Choi SJ, Lee DS (2011) Antibacterial Activity of Silver-nanoparticles against Staphylococcus aureus and Escherichia coli. Korean J Microbiol Biotechnol 39(1):77–85Google Scholar
  30. Klueh U, Wagner V, Kelly S, Johnson A, Bryers JD (2000) Efficacy of silver-coated fabric to prevent bacterial colonization and subsequent device-based biofilm formation. J Biomed Mater Res 53:621–631Google Scholar
  31. Kumari J, Ajeet S (2017) Evaluation of antibacterial activity from phytosynthesized silver nanoparticles against medical devices infected with Staphylococcus spp. J Taibah Univ Med Sci 12(1):47–54Google Scholar
  32. Li G, He D, Qian Y, Guan B, Gao S, Cui Y, Yokoyama K, Wang L (2012) Fungus-mediated green synthesis of silver nanoparticles using Aspergillus terreus. Int J Mol Sci 13(1):466–476Google Scholar
  33. 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(3):311–317Google Scholar
  34. Luo K, Jung S, Park KH, Kim YR (2018) Microbial biosynthesis of silver nanoparticles in different culture media. J Agric Food Chem 66(4):957–962Google Scholar
  35. Ma L, Su W, Liu JX, Zeng XX, Huang Z, Li W, Liu ZC, Tang JX (2017) Optimization for extracellular biosynthesis of silver nanoparticles by Penicillium aculeatum Su1 and their antimicrobial activity and cytotoxic effect compared with silver ions. Mater Sci Eng C 77:963–971Google Scholar
  36. Magdi HM, Mourad MHE, Abd El-Aziz MM (2014) Biosynthesis of silver nanoparticles using fungi and biological of mycosynthesized silver nanoparticles. Egypt J Exp Biol 10(1):1–12Google Scholar
  37. Majeed S, Danish M, Zahrudin AHB, Dash GK (2018) Biosynthesis and characterization of silver nanoparticles from fungal species and its antibacterial and anticancer effect. Karbala Int J Mod Sci 4(1):86–92Google Scholar
  38. Moaddab S, Ahari H, Shahbazzadeh D, Motallebi AA, Anvar AA, Rahman-Nya J, Shokrgozar MR (2011) Toxicity study of nanosilver (Nanocid) on osteoblast cancer cell line. Int Nano Lett 1:11–16Google Scholar
  39. Mohanpuria P, Rana NK, Yadav SK (2008) Biosynthesis of nanoparticles: technological concepts and future applications. J Nanopart Res 10(3):507–517Google Scholar
  40. Morones JR, Elechiguerra JL, Camacho A, Holt K, Kouri JB, Ramirez JT, Yacaman MJ (2005) The bactericidal effect of silver nanoparticles. Nanotechnology 16(10):2346–2353Google Scholar
  41. Mukherjee S, Chowdhury D, Kotcherlakota R, Patra S, Bhadra MP, Patra CR (2014) Potential theranostics application of biosynthesized silver nanoparticles (4-in-1 system). Theranostics 4(3):316–335Google Scholar
  42. Netala VR, Bethu MS, Pushpalatha B, Baki VB, Aishwarya S, Rao JV, Tartte V (2016) Biogenesis of silver nanoparticles using endophytic fungus Pestalotiopsis microspora and evaluation of their antioxidant and anticancer activities. Int J Nanomed 11:5683–5696Google Scholar
  43. Ninganagouda S, Rathod V, Jyoti H, Singh D, Prema K, Haq MU (2013) Extracellular biosynthesis of silver nanoparticles using Aspergillus flavus and their antimicrobial activity against gram negative MDR strains. Int J Pharma Bio Sci 4(4):222–229Google Scholar
  44. Pitt JI (1991) A laboratory guide to common Penicillium species. Commonwealth scientific and industrial research organization - Division of food processing, North WalesGoogle Scholar
  45. Rasheed T, Bilal M, Iqbal HMN, Li C (2017) Green biosynthesis of silver nanoparticles using leaves extract of Artemisia vulgaris and their potential biomedical applications. Colloids Surf, B 1(158):408–415Google Scholar
  46. Rosicka D, Sembera J (2013) Changes in the nanoparticle aggregation rate due to the additional effect of electrostatic and magnetic forces on mass transport coefficients. Nanoscale Res Lett 8(1):1–9Google Scholar
  47. Satyavani K, Gurudeeban S, Ramanathan T, Balasubramanian T (2011) Biomedical potential of silver nanoparticles synthesized from calli cells of Citrullus colocynthis (L.) Schrad. J Nanobiotechnol 9:43Google Scholar
  48. Shu Z, Zhang Y, Yang Q, Yang H (2017) Halloysite nanotubes supported Ag and ZnO nanoparticles with synergistically enhanced antibacterial activity. Nanoscale Res Lett 12:135. Google Scholar
  49. Singh P, Kim YJ, Zhang D, Yang DC (2016) Biological synthesis of nanoparticles from plants and microorganisms. Trends Biotechnol 34(7):588–599Google Scholar
  50. Smirnoff N, Cumbes QJ (1989) Hydroxyl radical scavenging activity of compatible solutes. J Phytochem 28(4):1057–1060Google Scholar
  51. Sondi I, 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(1):177–182Google Scholar
  52. Sulaiman GM, Hussien HT, Saleem MMNM (2015) Biosynthesis of silver nanoparticles synthesized by Aspergillus flavus and their antioxidant, antimicrobial and cytotoxicity properties. Bull Mater Sci 38(3):639–644Google Scholar
  53. Sulaiman GM, Tawfeeq AT, Jaaffer MD (2018) Biogenic synthesis of copper oxide nanoparticles using olea europaea leaf extract and evaluation of their toxicity activities: an in vivo and in vitro study. Biotechnol Prog 34(1):218–230Google Scholar
  54. Suresh AK, Pelletier DA, Wang W, Broich ML, Moon JW, Gu B, Allison DP, Joy DC, Phelps TJ, Doktycz MJ (2011) Biofabrication of discrete spherical gold nanoparticles using the metal-reducing bacterium Shewanella oneidensis. Acta Biomater 7(5):2148–2152Google Scholar
  55. Taha ZK, Howar SN, Sulaiman GM (2019) Isolation and identification of Penicillium italicum from Iraqi citrus lemon fruits and its ability manufacture of silver nanoparticles and their antibacterial and antifungal activity. Res J Pharm Technol 12(3):1320–1326Google Scholar
  56. Tripathi RM, Gupta RK, Shrivastav A, Singh MP, Shrivastav BR, Singh P (2013) Trichoderma koningii assisted biogenic synthesis of silver nanoparticles and evaluation of their antibacterial activity. Adv Nat Sci: Nanosci Nanotechnol 4(3):035005Google Scholar
  57. Udayasoorian C, Kumar RV, Jayabalakrishnan M (2011) Extracellular synthesis of silver nanoparticles using leaf extract of Cassia auriculata. Digest J Nanomater Biostruct 6(1):279–283Google Scholar
  58. Wang C, Kim YJ, Singh P, Mathiyalagan R, Jin Y, Yang DC (2016) Green synthesis of silver nanoparticles by Bacillus methylotrophicus, and their antimicrobial activity. Artif Cells Nanomed Biotechnol 44(4):1127–1132Google Scholar
  59. Wiley BJ, Im SH, Li ZY, Mc Lellan J, Siekkinen A, Xia Y (2006) Maneuvering the surface plasmon resonance of silver nanostructures through shape-controlled synthesis. J Phys Chem B 110(32):15666–15675Google Scholar
  60. Yamanaka M, Hara K, Kudo J (2005) Bactericidal actions of a silver ion solution on Escherichia coli, studied by energy-filtering transmission electron microscopy and proteomic analysis. Appl Environ Microbiol 71(11):7589–7593Google Scholar
  61. Zhang XF, Liu ZG, Shen W, Gurunathan S (2016) Silver nanoparticles: synthesis, characterization, properties, applications, and therapeutic approaches. Int J Mol Sci 17(9):1534Google Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Biology Department, College of Education for Pure Sciences/Ibn al-HaithamUniversity of BaghdadBaghdadIraq
  2. 2.Biotechnology Division, Applied Science DepartmentUniversity of TechnologyBaghdadIraq

Personalised recommendations