Toxicity of biosynthetic silver nanoparticles on the growth, cell ultrastructure and physiological activities of barley plant

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Abstract

Silver nanoparticles (AgNPs) were biosynthesized using the cell-free filtrate of bacterium Proteus mirabilis, reacted with 1 mM of AgNO3 solutions at 37 °C. The synthesis of AgNPs was monitored by UV–Vis spectroscopy and transmission electron microscopy (TEM) equipped with selected area electron diffraction (SAED). The results point to formation of spherical to cubical particles of AgNPs ranging in size from 5 to 35 nm with an average of 25 nm in diameter. The toxicity of Ag on barley (Hordeum vulgare L. cv. Gustoe) that was subjected to Ag+ as AgNO3 and AgNPs was explored. The grain germination and seedling growth of barley decreased in the presence of 0.1 mM Ag+ and was inhibited at 1 mM Ag+. In contrast, our results indicated that the AgNPs at low concentration (0.1 mM) could be useful for barley grain germination and seedling growth. However, the higher concentrations of AgNPs (0.5 and 1 mM) reduced grain germination and exhibited a stronger reduction in the root length. A decline in the photosynthetic pigments and disorganization of chloroplast grana thylakoids in Ag+ and AgNPs-treated plants confirmed the leaf chlorosis. An increase of plastoglobuli within chloroplasts was observed in Ag+ and AgNPs-treated leaves. Ag+ caused dense aggregation of nuclear chromatin materials and degeneration of mitochondria. Ag+ and AgNPs increased contents of malondialdehyde, soluble proteins, total phenolic compounds and activity of guaiacol peroxidase in barley leaves; these results point to activation of plant defence mechanisms against oxidative stress in barley.

Keywords

Hordeum vulgare Proteus mirabilis Silver nanoparticles Ultrastructure Oxidative stress Metabolites Peroxidase 

Abbreviations

Chl

Chlorophyll

MDA

Malondialdehyde

NPs

Nanoparticles

POX

Peroxidase

ROS

Reactive oxygen species

SAED

Selected area electron diffraction

TBA

Thiobarbituric acid

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Notes

Acknowledgements

The project was funded by the University Research Projects (1-434-2623), Taif University, Saudi Arabia.

References

  1. Abd-Alla MH, Nafady NA, Khalaf DM (2016) Assessment of silver nanoparticles contamination on faba bean-Rhizobium leguminosarum bv. viciae-Glomus aggregatum symbiosis: Implications for induction of autophagy process in root nodule. Agric Ecosyst Environ 218:163–177CrossRefGoogle Scholar
  2. Al-Harbi M, El-Deeb B, Mostafa N, Amer S (2014) Extracellular biosynthesis of AgNPs by the bacterium Proteus mirabilis and its toxic effect on some aspects of animal physiology. Adv Nanoparticl 3:83–91CrossRefGoogle Scholar
  3. American Society for Testing and Materials (2006) Standard terminology relating to nanotechnology. E 2456-06. West Conshohocken PAGoogle Scholar
  4. Amooaghaie R, Saeri MR, Azizi M (2015) Synthesis characterization and biocompatibility of silver nanoparticles synthesized from Nigella sativa leaf extract in comparison with chemical silver nanoparticles. Ecotoxicol Environ Saf 120:400–408CrossRefPubMedGoogle Scholar
  5. Anjum N, Sofo A, Scopa A, Roychoudhury A, Gill S, Iqbal M, Lukatkin A, Pereira E, Duarte A, Ahmad I (2015) Lipids and proteins-major targets of oxidative modifications in abiotic stressed plants. Environ Sci Pollut Res 22:4099–4121CrossRefGoogle Scholar
  6. Aruoja V, Dubourguie H, Kasemets K, Kahru A (2009) Toxicity of nanoparticles of CuO, ZnO andTiO2 to microalgae Pseudokirchneriella subcapitata. Sci Total Environ 407:1461–1468CrossRefPubMedGoogle Scholar
  7. Barbasz A, Kreczmer B, Oćwieja M (2016) Effects of exposure of callus cells of two wheat varieties to silver nanoparticles and silver salt (AgNO3). Acta Physiol Plant 38:1–11CrossRefGoogle Scholar
  8. Bartosz G (1997) Oxidative stress in plants. Acta Physiol Plant 19:47–64CrossRefGoogle Scholar
  9. Battke F, Leopold K, Maier M, Schmidhalter U, Schuster M (2008) Palladium exposure of barley: uptake and effects. Plant Biol 10:272–276CrossRefPubMedGoogle Scholar
  10. Bhainsa KC, D’Souza SF (2006) Extracellular biosynthesis of silver nanoparticles using the fungus Aspergillus fumigatus. Colloids Surf B: Biointerfaces 47:160–164CrossRefPubMedGoogle Scholar
  11. Chairuangkitti P, Lawanprasert S, Roytrakul S, Aueviriyavit S, Phummiratch D, Kulthong K, Chanvorachote P, Maniratanachote R (2013) Silver nanoparticles induce toxicity in a549 cells via ROS-dependent and ROS-independent pathways. Toxicol In Vitro 27:330–338CrossRefPubMedGoogle Scholar
  12. Chen L, Zhou L, Liu Y, Deng S, Wu H, Wang G (2012) Toxicological effects of nanometer titanium dioxide (nano-TiO2) on Chlamydomonas reinhardtii. Ecotoxicol Environ Saf 84:155–162CrossRefPubMedGoogle Scholar
  13. Chen A, Zeng G, Chen G, Liu L, Shang C, Hu X, Lu L, Chen M, Zhou Y, Zhang Q (2014) Plasma membrane behavior, oxidative damage, and defense mechanism in Phanerochaete chrysosporium under cadmium stress. Process Biochem 49:589–598CrossRefGoogle Scholar
  14. Choi O, Hu Z (2008) Size dependent and reactive oxygen species related nanosilver toxicity to nitrifying bacteria. Environ Sci Technol 42:4583–4588CrossRefPubMedGoogle Scholar
  15. Cvjetko P, Milošić A, Domijan A-M, Vinković Vrček I, Tolić S, Peharec Štefanić P, Letofsky-Papst I, Tkalec M, Balen B (2017) Toxicity of silver ions and differently coated silver nanoparticles in Allium cepa roots. Ecotoxicol Environ Saf 137:18–28CrossRefPubMedGoogle Scholar
  16. Dai GH, Andary C, Cosson-Monodol L, Boubals D (1994) Polyphenols and resistance of grapevines to downy mildew. Acta Horticult 381:763–766CrossRefGoogle Scholar
  17. Delalonde M, Barret Y, Coumans MP (1996) Development of phenolic compounds in maize anthers (Zea mays) during cold pretreatment prior to androgenesis. J Plant Physiol 149:612–616CrossRefGoogle Scholar
  18. Dietz K-J, Herth S (2011) Plant nanotoxicology. Trends Plant Sci 16:582–589CrossRefPubMedGoogle Scholar
  19. Doshi R, Braida W, Christodoulatos C, Wazne M, O’Connor G (2008) Nano-aluminum: Transport through sand columns and environmental effects on plants and soil communities. Environ Res 106:296–303CrossRefPubMedGoogle Scholar
  20. Dubey P, Matai I, Kumar SU, Sachdev A, Bhushan B, Gopinath P (2015) Perturbation of cellular mechanistic system by silver nanoparticle toxicity: cytotoxic, genotoxic and epigenetic potentials. Adv Colloid Interface Sci 221:4–21CrossRefPubMedGoogle Scholar
  21. El-Temsah YS, Joner EJ (2012) Impact of Fe and Ag nanoparticles on seed germination and differences in bioavailability during exposure in aqueous suspension and soil. Environ Toxicol 27:42–49CrossRefPubMedGoogle Scholar
  22. Fabrega J, Luoma SN, Tyler CR, Galloway TS, Lead JR (2011) Silver nanoparticles: behaviour and effects in the aquatic environment. Environ Int 37:517–531CrossRefPubMedGoogle Scholar
  23. Falco WF, Queiroz AM, Fernandes J, Botero ER, Falcão EA, Guimarães FEG, M’Peko JC, Oliveira SL, Colbeck I, Caires ARL (2015) Interaction between chlorophyll and silver nanoparticles: a close analysis of chlorophyll fluorescence quenching. J Photochem Photobiol A Chem 299:203–209CrossRefGoogle Scholar
  24. Fayez KA (2000) Action of photosynthetic diuron herbicide on cell organelles and biochemical constituents of the leaves of two soybean cultivars. Pest Biochem Physiol 66:105–115CrossRefGoogle Scholar
  25. Fayez KA, Abd-Elfattah Z (2007) Alteration in growth and physiological activities in Chlorella vulgaris under the effect of photosynthetic inhibitor diuron. Inter J Agri Biol 9:631–634Google Scholar
  26. Fayez KA, Bazaid SA (2014) Improving drought and salinity tolerance in barley by application of salicylic acid and potassium nitrate. J Saudi Soc Agric Sci 13:45–55Google Scholar
  27. Fayez KA, Mahmoud SY (2011) Detection and partial characterization of a putative closterovirus affecting Ficus carica: molecular ultrastructural and physiological aspects of infected leaves. Acta Physiol Plant 33:2187–2198CrossRefGoogle Scholar
  28. Fayez KA, Radwan DEM, Mohamed AK, Abdelrahman AM (2014) Fusilade herbicide causes alterations in chloroplast ultrastructure pigment content and physiological activities of peanut leaves. Photosynthetica 52:548–554CrossRefGoogle Scholar
  29. Godin B, Sakamoto JH, Serda RE, Grattoni A, Bouamrani A (2010) Emerging applications of nanomedicine for the diagnosis and treatment of cardiovascular diseases. Trends Pharmacol Sci 31:199–205CrossRefPubMedPubMedCentralGoogle Scholar
  30. Gorczyca A, Pociecha E, Kasprowicz M, Niemiec M (2015) Effect of nanosilver in wheat seedlings and Fusarium culmorum culture systems. Eur J Plant Pathol 142:251–261CrossRefGoogle Scholar
  31. Gurunathan S, Kalishwaralal K, Vaidyanathan R, Venkataraman D, Pandian SRK, Muniyandi J, Hariharan N, Eom SH (2009) Biosynthesis purification and characterization of silver nanoparticles using Escherichia coli. Colloids Surf B: Biointerfaces 74:328–335CrossRefPubMedGoogle Scholar
  32. Hassan FAS, Ali EF, El-Deeb BA (2014) Improvement of postharvest quality of cut rose cv. ‘First Red’ by biologically synthesized silver nanoparticles. Sci Hortic 179:340–348CrossRefGoogle Scholar
  33. Haverkamp RG, Marshall AT (2009) The mechanism of metal nanoparticle formation in plants: limits on accumulation. J Nanopart Res 11:1453–1463CrossRefGoogle Scholar
  34. Hernández JA, Almansa MS (2002) Short-term effects of salt stress on antioxidant systems and leaf water relations of pea leaves. Physiol Plant 115:251–257CrossRefPubMedGoogle Scholar
  35. Hood E (2004) Nanotechnology: looking as we leap. Environ Health Perspect 112:A740–A749CrossRefPubMedPubMedCentralGoogle Scholar
  36. Impellitteri CA, Tolaymat TM, Scheckel KG (2009) The speciation of silver nanoparticles in antimicrobial fabric before and after exposure to a hypochlorite/detergent solution. J Environ Qual 38:1528–1530CrossRefPubMedGoogle Scholar
  37. Kaveh R, Li YS, Ranjbar S, Tehrani R, Brueck CL, Van Aken B (2013) Changes in Arabidopsis thaliana gene expression in response to silver nanoparticles and silver ions. Environ Sci Technol 18:10637–10644CrossRefGoogle Scholar
  38. Kim JS, Kuk E, Yu KN, Kim JH, Park SJ, Lee HJ, Cho MH (2007) Antimicrobial effects of silver nanoparticles. Nanomed Nanotechnol Biol Med 3:95–101CrossRefGoogle Scholar
  39. Klaine SJ, Alvarez PJJ, Batley GE, Fernandes TF, Handy RD, Lyon DY, Mahendra S, McLaughlin MJ, Lead JR (2008) Nanomaterials in the environment: behavior fate bioavailability and effects. Environ Toxicol Chem 27:1825–1851CrossRefPubMedGoogle Scholar
  40. Kokura S, Handa O, Takagi T, Ishikawa T, Naito Y, Yoshikawa T (2010) Silver nanoparticles as a safe preservative for use in cosmetics. Nanomed Nanotechnol Biol Med 6:570–574CrossRefGoogle Scholar
  41. Krishnaraj C, Jagan EG, Ramachandran R, Abirami SM, Mohan N, Kalaichelvan PT (2012) Effect of biologically synthesized silver nanoparticles on Bacopa monnieri (Linn.) Wettst. plant growth metabolism. Process Biochem 47:651–658CrossRefGoogle Scholar
  42. Kumar V, Yadav SK (2009) Plant-mediated synthesis of silver and gold nanoparticles and their applications. J Chem Technol 84:151–157Google Scholar
  43. Kumari M, Mukherjee A, Chandrasekaran N (2009) Genotoxicity of silver nanoparticles in Allium cepa. Sci Tot Environ 407:5243–5246CrossRefGoogle Scholar
  44. Lee CW, Mahendra S, Zodrow K, Li D, Tsai Y-C, Braam J, Alvarez PJJ (2010) Developmental phytotoxicity of metal oxide nanoparticles to Arabidopsis thaliana. Environ Toxicol Chem 29:669–675CrossRefPubMedGoogle Scholar
  45. Lee W-M, Kwak JI, An Y-J (2012) Effect of silver nanoparticles in crop plants Phaseolus radiatus and Sorghum bicolor: media effect on phytotoxicity. Chemosphere 86:491–499CrossRefPubMedGoogle Scholar
  46. Lichtenthaler HK (1987) Chlorophylls and carotenoids–pigments of photosynthetic biomembranes. In: Colowick SP, Kaplan NO (eds) Methods in enzymology, vol 148. Academic Press, San Diego, pp 350–382Google Scholar
  47. Lin DH, Xing BS (2007) Phytotoxicity of nanoparticles: inhibition of seed germination and root growth. Environ Pollut 150:243–250CrossRefPubMedGoogle Scholar
  48. Lowry OH, Rosebrough NJ, Farr AI, Randall RJ (1951) Protein measurement with the folin phenol reagent. J Biol Chem 193:291–297Google Scholar
  49. Lü P, Cao J, He S, Liu J, Li H, Cheng G, Ding Y, Joyce DC (2010) Nano-silver pulse treatments improve water relations of cut rose cv. Movie Star flowers. Postharvest Biol Technol 57:196–202CrossRefGoogle Scholar
  50. Luft JH (1961) Improvements in epoxy embedding methods. J Biophys Biochem Cytol 9:409–414CrossRefPubMedPubMedCentralGoogle Scholar
  51. Ma X, Geiser-Lee J, Deng Y, Kolmakov A (2010) Interactions between engineered nanoparticles (ENPs) and plants: phytotoxicity uptake and accumulation. Sci Total Environ 408:3053–3061CrossRefPubMedGoogle Scholar
  52. Manios T, Stentiford EI, Millner PA (2003) The effect of heavy metals accumulation on the chlorophyll concentration of Typha latifolia plants growing in a substrate containing sewage sludge compost and watered with metaliferus water. Ecol Eng 20:65–74CrossRefGoogle Scholar
  53. Marambio-Jones C, Hoek EM (2010) A review of the antibacterial effects of silver nanomaterials and potential implications for human health and the environment. J Nanopart Res 12:1531–1551CrossRefGoogle Scholar
  54. Mazumdar H, Ahmed GU (2011) Phytotoxicity effect of silver nanoparticles on Oryza sativa. Inter J Chem Tech Res 3:1494–1500Google Scholar
  55. McGillicuddy E, Murray I, Kavanagh S, Morrison L, Fogarty A, Cormican M, Dockery P, Prendergast M, Rowan N, Morris D (2017) Silver nanoparticles in the environment: sources, detection and ecotoxicology. Sci Total Environ 575:231–246CrossRefPubMedGoogle Scholar
  56. Miao AJ, Schwehr KA, Xu C, Zhang SJ, Luo Z, Quigg A, Santschi PH (2009) The algal toxicity of silver engineered nanoparticles and detoxification by exopolymeric substances. Environ Pollut 157:3034–3041CrossRefPubMedGoogle Scholar
  57. Mulvaney P (1996) Surface plasmon spectroscopy of nanosized metal particles. Langmuir 12:788–800CrossRefGoogle Scholar
  58. Musante C, White JC (2012) Toxicity of silver and copper to Cucurbita pepo: differential effects of nano and bulk-size particles. Environ Toxicol 27:510–517CrossRefPubMedGoogle Scholar
  59. Nair PMG, Chung IM (2014) Physiological and molecular level effects of silver nanoparticles exposure in rice (Oryza sativa L.) seedlings. Chemosphere 112:105–111CrossRefPubMedGoogle Scholar
  60. Navarro E, Baun A, Behra R, Hartmann N, Filser J, Miao A-J, Quigg A, Santschi P, Sigg L (2008a) Environmental behavior and ecotoxicity of engineered nanoparticles to algae plants and fungi. Ecotoxicology 17:372–386CrossRefPubMedGoogle Scholar
  61. Navarro E, Piccapietra F, Wagner B, Marconi F, Kaegi R, Odzak N, Sigg L, Behra R (2008b) Toxicity of silver nanoparticles to Chlamydomonas reinhardtii. Environ Sci Technol 42:8959–8964CrossRefPubMedGoogle Scholar
  62. Nel A, Xia T, Madler L, Li N (2006) Toxic potential of materials at the nanolevel. Science 311:622–627CrossRefPubMedGoogle Scholar
  63. Oukarroum A, Bras S, Perreault F, Popovic R (2012) Inhibitory effects of silver nanoparticles in two green algae, Chlorella vulgaris and Dunaliella tertiolecta. Ecotoxicol Environ Saf 78:80–85CrossRefPubMedGoogle Scholar
  64. Oukarroum A, Gaudreault M-H, Pirastru L, Popovic R (2013) Alleviation of silver toxicity by calcium chloride (CaCl2) in Lemna gibba L. Plant Physiol Biochem 71:235–239CrossRefPubMedGoogle Scholar
  65. 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 73:1712–1720CrossRefPubMedPubMedCentralGoogle Scholar
  66. Polle A, Otter T, Seifert F (1994) Apoplastic peroxidases and lignification in needles of Norway spruce (Picea abies L.). Plant Physiol 106:53–60CrossRefPubMedPubMedCentralGoogle Scholar
  67. Qian H, Peng X, Han X, Ren J, Sun L, Fu Z (2013) Comparison of the toxicity of silver nanoparticles and silver ions on the growth of terrestrial plant model Arabidopsis thaliana. J Environ Sci 25:1947–1956CrossRefGoogle Scholar
  68. Rajan A, Vilas V, Philip D (2015) Catalytic and antioxidant properties of biogenic silver nanoparticles synthesized using Areca catechu nut. J Mol Liq 207:231–236CrossRefGoogle Scholar
  69. Rasband WS (1997) Image U.S. National Institutes of Health Bethesda Maryland USA. http://imagej.nih.gov/ij/
  70. Raut R, Kolekar N, Lakkakula J, Mendhulkar V, Kashid S (2010) Extracellular synthesis of silver nanoparticles using dried leaves of Pongamia pinnata (L) pierre. Nano-Micro Lett 2:106–113CrossRefGoogle Scholar
  71. Sakihama Y, Cohen MF, Grace SC, Yamasaki H (2002) Plant phenolic antioxidant and prooxidant activities: phenolics-induced oxidative damage mediated by metals in plants. Toxicology 177:67–80CrossRefPubMedGoogle Scholar
  72. Sevanian A, Ursini F (2000) Lipid peroxidation in membranes and low–density lipoproteins: similarities and differences. Free Radical Biol Med 29:306–311CrossRefGoogle Scholar
  73. Shaddad MA, Ahmed AM, Fayez KA (1988) Alleviation of the adverse effects of salinity by nitrogen fertilization. Biol Plant 30:343–350CrossRefGoogle Scholar
  74. Shaligram NS, Bule M, Bhambure R, Singhal RS, Singh SK, Szakacs G, Pandey A (2009) Biosynthesis of silver nanoparticles using aqueous extract from the compactin producing fungal strain. Process Biochem 44:939–943CrossRefGoogle Scholar
  75. Sharma VK, Yngard RA, Lin Y (2009) Silver nanoparticles: green synthesis and their antimicrobial activities. Adv Colloid Interface Sci 145:83–96CrossRefPubMedGoogle Scholar
  76. Shivaji S, Madhu S, Singh S (2011) Extracellular synthesis of antibacterial silver nanoparticles using psychrophilic bacteria. Process Biochem 46:1800–1807CrossRefGoogle Scholar
  77. Sytar O, Cai Z, Brestic M, Kumar A, Prasad MNV, Taran N, Smetanska I (2013) Foliar applied nickel on buckwheat (Fagopyrum esculentum) induced phenolic compounds as potential antioxidants. Clean-Soil Air Water 41:1129–1137CrossRefGoogle Scholar
  78. Szivák I, Behra R, Sigg L (2009) Metal-induced reactive oxygen species production in Chlamydomonas reinhardtii (Chlorophyceae). J Phycol 45:427–435CrossRefPubMedGoogle Scholar
  79. Thuesombat P, Hannongbua S, Akasit S, Chadchawan S (2014) Effect of silver nanoparticles on rice (Oryza sativa L. cv. KDML 105) seed germination and seedling growth. Ecotoxicol Environ Saf 104:302–309CrossRefPubMedGoogle Scholar
  80. Tiede K, Boxall ABA, Tear SP, Lewis J, David H, Hassellöv M (2008) Detection and characterization of engineered nanoparticles in food and the environment. Food Addit Contam 25:795–821CrossRefGoogle Scholar
  81. Vannini C, Domingo G, Onelli E, Prinsi B, Marsoni M, Espen L, Bracale M (2013) Morphological and proteomic responses of Eruca sativa exposed to silver nanoparticles or silver nitrate. PLoS ONE 8:e68752CrossRefPubMedPubMedCentralGoogle Scholar
  82. Vannini C, Domingo G, Onelli E, De Mattia F, Bruni I, Marsoni M, Bracale M (2014) Phytotoxic and genotoxic effects of silver nanoparticles exposure on germinating wheat seedlings. J Plant Physiol 171:1142–1148CrossRefPubMedGoogle Scholar
  83. Xu QS, Hu JZ, Xie KB, Yang HY, Du KH, Shi GX (2010) Accumulation and acute toxicity of silver in Potamogeton crispus L. J Hazard Mater 173:186–193CrossRefPubMedGoogle Scholar
  84. Yasur J, Rani P (2013) Environmental effects of nanosilver: impact on castor seed germination seedling growth and plant physiology. Environ Sci Pollut Res 20:8636–8648CrossRefGoogle Scholar
  85. Yin L, Cheng Y, Espinasse B, Colman BP, Auffan M, Wiesner M, Rose J, Liu J, Bernhardt ES (2011) More than the ions: the effects of silver nanoparticles on Lolium multiflorum. Environ Sci Technol 45:2360–2367CrossRefPubMedGoogle Scholar
  86. Yin L, Colman BP, McGill BM, Wright JP, Bernhardt ES (2012) Effects of silver nanoparticle exposure on germination and early growth of eleven wetland plants. PLoS One 7:47674CrossRefGoogle Scholar
  87. Yuan Z, Li J, Cui L, Xu B, Zhang H, Yu C-P (2013) Interaction of silver nanoparticles with pure nitrifying bacteria. Chemosphere 90:1404–1411CrossRefPubMedGoogle Scholar
  88. Zheng W, Fei Y, Huang Y (2009) Soluble protein and acid phosphatase exuded by ectomycorrhizal fungi and seedlings in response to excessive Cu and Cd. J Environ Sci 21:1667–1672CrossRefGoogle Scholar

Copyright information

© Franciszek Górski Institute of Plant Physiology, Polish Academy of Sciences, Kraków 2017

Authors and Affiliations

  • K. A. Fayez
    • 1
    • 2
  • B. A. El-Deeb
    • 1
    • 2
  • N. Y. Mostafa
    • 1
    • 3
  1. 1.Biology Department, Faculty of ScienceTaif University, Al-HaweiahTaifSaudi Arabia
  2. 2.Botany Department, Faculty of ScienceSohag UniversitySohagEgypt
  3. 3.Chemistry Department, Faculty of ScienceSuez Canal UniversityIsmailiaEgypt

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