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Antibacterial and Antibiofilm Potential of Mono-dispersed Stable Copper Oxide Nanoparticles-Streptomycin Nano-drug: Implications for Some Potato Plant Bacterial Pathogen Treatment

  • Ahmed I. El-Batal
  • Naglaa M. Balabel
  • Mohamed S. Attia
  • Gharieb S. El-SayyadEmail author
Original Paper
  • 17 Downloads

Abstract

The novelty of this work is to estimate the antibacterial and antibiofilm capabilities of the mono-dispersed copper oxide nanoparticles (CuO NPs)-streptomycin nano-drug which synthesized by a cost-effective and eco-friendly gamma irradiation method. The incorporated CuO NPs-streptomycin was fully defined by UV–Vis., XRD, FTIR, HRTEM, DLS, HRSEM and EDX elemental analysis. In vitro antibacterial and antibiofilm activities of CuO NPs-streptomycin were examined towards pathogenic bacteria-causing brown, ring, soft rot and black leg diseases in potato plant. The proposed reaction mechanism regarding the synergistic potential between CuO NPs and streptomycin was estimated. The incorporated CuO NPs-streptomycin displayed an absorption peak at 585.0 nm specific for the Surface Plasmon Resonance. Results achieved from HRTEM, HRSEM and XRD verified the mono-dispersed crystalline character of the fabricated CuO NPs-streptomycin with a common particle size of 20.20 nm. CuO NPs-streptomycin exhibited an encouraging antibacterial activity against Clavibacter michiganensis subsp. sepedonicus (35.50 mm ZOI). Additionally, CuO NPs-streptomycin displayed enhanced biofilm inhibition percentage of about 90.99%, 84.23%, and 83.42% toward C. michiganensis subsp. sepedonicus, Ralstonia solanacearum, and Dickeya solani, respectively. Consequently, according to the prominent characteristics, this research could provide insights for determining dangerous agricultural challenges, potato packaging and processing and new nano-drug formula for invading potato pathogenic bacteria through the cultivation.

Keywords

Solanum tuberosum Potato pathogens Latent infection Quarantine diseases Nano-drug Gamma rays Antibacterial activity Mono-dispersed CuO NPs 

Notes

Acknowledgements

The authors would like to thank the Nanotechnology Research Unit (P.I. Prof. Dr. Ahmed I. El-Batal), Drug Microbiology Lab., Drug Radiation Research Department, NCRRT, Egypt, for financing and supporting this study under the project “Nutraceuticals and Functional Foods Production by using Nano/Biotechnological and Irradiation Processes”. Also, the authors would like to thank Prof. Mohamed Gobara (Military Technical College, Egyptian Armed Forces), and Zeiss microscope team in Cairo for their invaluable advice during this study.

Compliance with Ethical Standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. 1.
    C. Beaulieu and F. Van Gijsegem (1990). J.0 Bacteriol.172, (3), 1569–1575.CrossRefGoogle Scholar
  2. 2.
    A. Sletten and T. Rafoss Fire Blight in Norway—An Assessment of the Plant Health Risk for the Plant Disease Fire Blight in Norway (Bioforsk, Oslo, 2007).Google Scholar
  3. 3.
    M. Perombelon (2000). EPPO Bull.30, (3–4), 413–420.CrossRefGoogle Scholar
  4. 4.
    E. Parkin (1956). Annu. Rev. Entomol.1, (1), 223–240.CrossRefGoogle Scholar
  5. 5.
    F. Dadaşoğlu and R. Kotan (2017). J. Anim. Plant Sci.27, 647–654.Google Scholar
  6. 6.
    M. Pérombelon (1992). Neth. J. Plant Pathol.98, (2), 135–146.CrossRefGoogle Scholar
  7. 7.
    I. Toth, et al. (2011). Plant Pathol.60, (3), 385–399.CrossRefGoogle Scholar
  8. 8.
    J. M. van der Wolf and S. H. De Boer Bacterial pathogens of potato. Potato Biology and Biotechnology (Oxford, Elsevier, 2007), pp. 595–617.CrossRefGoogle Scholar
  9. 9.
    M. C. Perombelon and A. Kelman (1980). Annu. Rev. Phytopathol.18, (1), 361–387.CrossRefGoogle Scholar
  10. 10.
    M. Pérombelon (2002). Plant Pathol.51, (1), 1–12.CrossRefGoogle Scholar
  11. 11.
    A. O. Charkowski The soft rot Erwinia. Plant-Associated Bacteria (Springer, Dordrecht, 2007), pp. 423–505.Google Scholar
  12. 12.
    F. Barras, F. van Gijsegem, and A. K. Chatterjee (1994). Annu. Rev. Phytopathol.32, (1), 201–234.CrossRefGoogle Scholar
  13. 13.
    S. Reverchon and W. Nasser (2013). Environ. Microbiol. Rep.5, (5), 622–636.PubMedGoogle Scholar
  14. 14.
    S. Baghaee-Ravari, et al. (2011). Eur. J. Plant Pathol.129, (3), 413–425.CrossRefGoogle Scholar
  15. 15.
    C. Picard, et al. (2019). BASE23, (1), 36–45.Google Scholar
  16. 16.
    I. Hadizadeh, et al. (2019). Plant Pathol.68, (2), 297–311.CrossRefGoogle Scholar
  17. 17.
    N. F. Sommer, R. J. Fortlage, and D. C. Edwards (2002). Postharvest. Technol. Hortic. Crops3311, 197.Google Scholar
  18. 18.
    L. R. Jones, M. Miller, and E. Bailey Frost Necrosis of Potato Tubers, vol. 46 (Agricultural Experiment Station of the University of Wisconsin, Madison, 1919).Google Scholar
  19. 19.
    P. Ark (1946). Am. J. Potato Res.23, (5), 170–181.CrossRefGoogle Scholar
  20. 20.
    V. Divya Rani and H. Sudini (2013). Int. J. Plant Anim. Environ. Sci.3, (4), 156–164.Google Scholar
  21. 21.
    R. Trias, et al. (2008). Int. Microbiol.11, (4), 231.PubMedGoogle Scholar
  22. 22.
    A. Makhlouf and R. Abdeen (2014). J. Biol. Agric. Healthc.4, (10), 31–44.Google Scholar
  23. 23.
    D. R. Fravel (1988). Annu. Rev. Phytopathol.26, (1), 75–91.CrossRefGoogle Scholar
  24. 24.
    M. Salanoubat, et al. (2002). Nature415, (6871), 497.PubMedCrossRefGoogle Scholar
  25. 25.
    E. Yabuuchi, et al. (1995). Microbiol. Immunol.39, (11), 897–904.PubMedCrossRefGoogle Scholar
  26. 26.
    C. Allen, P. Prior, and A. Hayward Bacterial Wilt Disease and the Ralstonia solanacearum Species Complex (American Phytopathological Society (APS Press), St. Paul, 2005).Google Scholar
  27. 27.
    G. Granada and L. Sequeira (1983). Can. J. Microbiol.29, (4), 433–440.CrossRefGoogle Scholar
  28. 28.
    S. Weller, et al. (2000). Appl. Environ. Microbiol.66, (7), 2853–2858.PubMedPubMedCentralCrossRefGoogle Scholar
  29. 29.
    A. Hayward (1991). Annu. Rev. Phytopathol.29, (1), 65–87.PubMedCrossRefGoogle Scholar
  30. 30.
    E. Guchi (2015). World J. Agric. Res.3, (1), 34–42.Google Scholar
  31. 31.
    M. M. López, et al. (2003). Int. Microbiol.6, (4), 233–243.PubMedCrossRefPubMedCentralGoogle Scholar
  32. 32.
    D. Baer and N. C. Gudmestad (1993). Phytopathology83, (2), 157–163.CrossRefGoogle Scholar
  33. 33.
    J. T. Seil and T. J. Webster (2012). Int. J. Nanomed.7, 2767.Google Scholar
  34. 34.
    A. El-Batal, et al. (2014). Br. J. Pharm. Res.4, (11), 1341.CrossRefGoogle Scholar
  35. 35.
    M. A. Maksoud, et al. (2018). Mater. Sci. Eng. C92, 644–656.CrossRefGoogle Scholar
  36. 36.
    A. F. El-Baz, et al. (2016). J. Basic Microbiol.56, (5), 531–540.PubMedCrossRefPubMedCentralGoogle Scholar
  37. 37.
    K. Pal, et al. (2019). Electron. Mater. Lett.15, (1), 84–101.CrossRefGoogle Scholar
  38. 38.
    T. Thirugnanasambandan, et al. (2018). Nano-Struct Nano-Objects16, 224–233.CrossRefGoogle Scholar
  39. 39.
    S. Sajjadifar, et al. (2019). Chem. Methodol.3, (2), 226–236.Google Scholar
  40. 40.
    K. Pal, et al. (2015). J. Mater. Chem. C3, (45), 11907–11917.CrossRefGoogle Scholar
  41. 41.
    M. A. Elkodous, et al. (2019). J. Mater. Sci. Mater. Electron.30, (9), 8312–8328.CrossRefGoogle Scholar
  42. 42.
    M. A. Elkodous, et al. (2018). Charact. Appl. Nanomater..  https://doi.org/10.24294/can.v1i2.585.CrossRefGoogle Scholar
  43. 43.
    M. I. A. A. Maksoud, et al. (2019). J. Mater. Sci. Mater. Electron.30, (5), 4908–4919.CrossRefGoogle Scholar
  44. 44.
    A. Khatua, et al. (2019). J. Clust. Sci..  https://doi.org/10.1007/s10876-019-01624-6.CrossRefGoogle Scholar
  45. 45.
    A. I. El-Batal, et al. (2017). J. Clust. Sci.28, (3), 1083–1112.CrossRefGoogle Scholar
  46. 46.
    M. Abd Elkodous, et al. (2019). Colloids Surf. B Biointerfaces180, 411–428.PubMedCrossRefPubMedCentralGoogle Scholar
  47. 47.
    M. Abd Elkodous, et al. (2019). J. Clust. Sci.30, (3), 531–540.CrossRefGoogle Scholar
  48. 48.
    H. Barabadi, et al. (2019). J. Clust. Sci..  https://doi.org/10.1007/s10876-019-01554-3.CrossRefGoogle Scholar
  49. 49.
    M. Saravanan, et al. (2018). Microb. Pathog.115, 57–63.PubMedCrossRefPubMedCentralGoogle Scholar
  50. 50.
    S. Laurent, et al. (2008). Chem. Rev.108, (6), 2064–2110.PubMedCrossRefPubMedCentralGoogle Scholar
  51. 51.
    C. Xu and X. Qu (2014). NPG Asia Mater.6, (3), e90.CrossRefGoogle Scholar
  52. 52.
    D. Ling and T. Hyeon (2013). Small9, (9–10), 1450–1466.PubMedCrossRefPubMedCentralGoogle Scholar
  53. 53.
    J. W. Rasmussen, et al. (2010). Expert Opin. Drug Deliv.7, (9), 1063–1077.PubMedPubMedCentralCrossRefGoogle Scholar
  54. 54.
    V. Ravishankar Rai, and A. Jamuna Bai Nanoparticles and their potential application as antimicrobials. A. Méndez-Vilas (ed.), Science Against Microbial Pathogens: Communicating Current Research and Technological Advances (Formatex, Mysore, 2011).Google Scholar
  55. 55.
    M. Ghorab, et al. (2016). Br. Biotechnol. J.16, (1), 1–25.CrossRefGoogle Scholar
  56. 56.
    K. Pal, et al. (2015). Appl. Surf. Sci.357, 1499–1510.CrossRefGoogle Scholar
  57. 57.
    D. V. Ponnuvelu, et al. (2016). Mater. Res. Express3, (10), 105005.CrossRefGoogle Scholar
  58. 58.
    G. S. El-Sayyad, et al. (2019). J. Clust. Sci..  https://doi.org/10.1007/s10876-019-01629-1.CrossRefGoogle Scholar
  59. 59.
    A. I. El-Batal, et al. (2019). J. Clust. Sci..  https://doi.org/10.1007/s10876-019-01619-3.CrossRefGoogle Scholar
  60. 60.
    R. Emmanuel, et al. (2017). Microb. Pathog.113, 295–302.PubMedCrossRefPubMedCentralGoogle Scholar
  61. 61.
    M. Saravanan, et al. (2014). J. Bionanosci.8, (1), 21–27.CrossRefGoogle Scholar
  62. 62.
    N. A. Dhas, C. P. Raj, and A. Gedanken (1998). Chem. Mater.10, (5), 1446–1452.CrossRefGoogle Scholar
  63. 63.
    M.-S. Yeh, et al. (1999). J. Phys. Chem. B103, (33), 6851–6857.CrossRefGoogle Scholar
  64. 64.
    M. Yang and J.-J. Zhu (2003). J. Cryst. Growth256, (1–2), 134–138.CrossRefGoogle Scholar
  65. 65.
    P. Boomi, et al. (2019). J. Clust. Sci.30, (3), 715–726.CrossRefGoogle Scholar
  66. 66.
    J. Cheon, J. Lee, and J. Kim (2012). Thin Solid Films520, (7), 2639–2643.CrossRefGoogle Scholar
  67. 67.
    A. Pugazhendhi, et al. (2019). J. Photochem. Photobiol. B Biol.190, 86–97.CrossRefGoogle Scholar
  68. 68.
    R. Balachandar, et al. (2019). J. Clust. Sci.30, 1–8.CrossRefGoogle Scholar
  69. 69.
    K. Kanagamani, et al. (2019). J. Clust. Sci.30, (6), 1415–1424.CrossRefGoogle Scholar
  70. 70.
    G. S. El-Sayyad, F. M. Mosallam, and A. I. El-Batal (2018). Adv. Powder Technol.29, (11), 2616–2625.CrossRefGoogle Scholar
  71. 71.
    H. Barabadi, et al. (2019). J. Clust. Sci..  https://doi.org/10.1007/s10876-019-01668-8.CrossRefGoogle Scholar
  72. 72.
    H. Barabadi, et al. (2014). Braz. J. Microbiol.45, (4), 1493–1501.PubMedCrossRefPubMedCentralGoogle Scholar
  73. 73.
    H. Barabadi, et al. (2017). Green Chem. Lett. Rev.10, (4), 285–314.CrossRefGoogle Scholar
  74. 74.
    H. Barabadi, F. Kobarfard, and H. Vahidi (2018). Iran. J. Pharm. Res.17, (Special Issue 2), 87–97.PubMedPubMedCentralGoogle Scholar
  75. 75.
    H. Barabadi, et al. (2019). J. Clust. Sci.30, (2), 259–279.CrossRefGoogle Scholar
  76. 76.
    P. Kazakevich, et al. (2006). Appl. Surf. Sci.252, (13), 4373–4380.CrossRefGoogle Scholar
  77. 77.
    G. Granata, et al. (2016). J. Nanoparticle Res.18, (5), 133.CrossRefGoogle Scholar
  78. 78.
    C. Y. Ho, Y. H. Tsai, and F. M. Sui Thermal transport in the copper powders with nanometer and micrometer particles. Advanced Materials Research (Trans Tech Publ, Zurich, 2010).Google Scholar
  79. 79.
    J. B. Fathima, et al. (2018). J. Mol. Liq.260, 1–8.CrossRefGoogle Scholar
  80. 80.
    S. N. Sinha, et al. (2015). Appl. Nanosci.5, (6), 703–709.CrossRefGoogle Scholar
  81. 81.
    Z. Jiang, et al. (2019). Life Sci.220, 156–161.PubMedCrossRefGoogle Scholar
  82. 82.
    N. Cioffi, et al. (2005). Anal. Bioanal. Chem.381, (3), 607–616.PubMedCrossRefGoogle Scholar
  83. 83.
    R. G. Saratale, et al. (2018). J. Environ. Manag.223, 1086–1097.CrossRefGoogle Scholar
  84. 84.
    S. Vasantharaj, et al. (2019). J. Photochem. Photobiol. B Biol.191, 143–149.CrossRefGoogle Scholar
  85. 85.
    S. Sathiyavimal, et al. (2018). J. Photochem. Photobiol. B Biol.188, 126–134.CrossRefGoogle Scholar
  86. 86.
    F. M. Mosallam, et al. (2018). Microb. Pathog.122, 108–116.PubMedCrossRefPubMedCentralGoogle Scholar
  87. 87.
    Z. Klencsár, et al. (2019). Mater. Chem. Phys.223, 122–132.CrossRefGoogle Scholar
  88. 88.
    H. Nosrati, et al. (2018). Int. J. Biol. Macromol.108, 909–915.PubMedCrossRefPubMedCentralGoogle Scholar
  89. 89.
    M.-N. Yap Analysis of Erwinia Diversity and Cell Aggregation (The University of Wisconsin-Madison, Madison, 2006).Google Scholar
  90. 90.
    F. Casano, J. Wells, and T. Van der Zwet (1988). J. Phytopathol.121, (3), 267–274.CrossRefGoogle Scholar
  91. 91.
    H. Jansing and K. Rudolph (1998). J. Plant Dis. Prot.105, 590–601.Google Scholar
  92. 92.
    Ahmed, M.E.E., Detection and effects of latent contamination of potato tubers by soft rot bacteria, and investigations on the effect of hydrogen peroxide on lipopolysaccharides of Erwinia carotovora in relation to acquired resistance against biocides. 2001, Citeseer.Google Scholar
  93. 93.
    H. A. Wahab and N. M. Balabel (2011). Egypt J. Phytopathol.39, (3), 154–168.Google Scholar
  94. 94.
    Doloman, A., Optimization of biogas production by use of a microbially enhanced inoculum. 2019.Google Scholar
  95. 95.
    J. Janse (1988). Eppo Bull.18, (3), 343–351.CrossRefGoogle Scholar
  96. 96.
    G. Somodi, J. Jones, and J. Scott. Comparison of inoculation techniques for screening tomato genotypes for bacterial wilt resistance. in ACIAR Proceedings. (Australian Centre for International Agricultural Research, 1993).Google Scholar
  97. 97.
    J. Van der Wolf, et al., Epidemiology of Clavibacter michiganensis subsp. sepedonicus in relation to control of bacterial ring rot. 2005, PRI Bioscience.Google Scholar
  98. 98.
    R. Bryaskova, et al. (2011). J. Chem. Biol.4, (4), 185.PubMedPubMedCentralCrossRefGoogle Scholar
  99. 99.
    M. Balouiri, M. Sadiki, and S. K. Ibnsouda (2016). J. Pharm. Anal.6, (2), 71–79.PubMedCrossRefGoogle Scholar
  100. 100.
    C. W. Wong, et al. (2019). J. Clust. Sci..  https://doi.org/10.1007/s10876-019-01651-3.CrossRefGoogle Scholar
  101. 101.
    H. C. Diogo, et al. (2010). An. Bras. Dermatol.85, (3), 324–330.PubMedCrossRefGoogle Scholar
  102. 102.
    A. I. El-Batal, et al. (2019). J. Clust. Sci.30, (4), 947–964.CrossRefGoogle Scholar
  103. 103.
    A. I. El-Batal, F. M. Mosallam, and G. S. El-Sayyad (2018). J. Clust. Sci.29, 1–13.CrossRefGoogle Scholar
  104. 104.
    M. Abd Elkodous, et al. (2019). Biol. Trace Elem. Res..  https://doi.org/10.1007/s12011-019-01894-1.CrossRefPubMedGoogle Scholar
  105. 105.
    G. D. Christensen, et al. (1982). Infect. Immun.37, (1), 318–326.PubMedPubMedCentralGoogle Scholar
  106. 106.
    M. A. Ansari, et al. (2014). Appl. Nanosci.4, (7), 859–868.CrossRefGoogle Scholar
  107. 107.
    G. S. El-Sayyad, et al. (2019). Biol. Trace Elem. Res..  https://doi.org/10.1007/s12011-019-01842-z.CrossRefPubMedGoogle Scholar
  108. 108.
    S. H. Abidi, et al. (2013). BMC Ophthalmol.13, (1), 57.PubMedPubMedCentralCrossRefGoogle Scholar
  109. 109.
    T. Mathur, et al. (2006). Indian J. Med. Microbiol.24, (1), 25.PubMedCrossRefGoogle Scholar
  110. 110.
    K. Brownlee Probit Analysis: A Statistical Treatment of the Sigmoid Response Curve (Cambridge Univ. Press, New York, 1952).Google Scholar
  111. 111.
    N. Gudmestad and G. Secor Management of soft rot and ring rot. Potato Health Management (American Phytopathological Society, St. Paul, 1993), pp. 135–139.Google Scholar
  112. 112.
    M. Składanowski, et al. (2017). J. Clust. Sci.28, (1), 59–79.CrossRefGoogle Scholar
  113. 113.
    S. Link and M. A. El-Sayed (2003). Ann. Rev. Phys. Chem.54, (1), 331–366.CrossRefGoogle Scholar
  114. 114.
    G. Das, K.-H. Baek, and J. K. Patra (2019). PLoS ONE14, (6), e0217318.PubMedPubMedCentralCrossRefGoogle Scholar
  115. 115.
    N. Pauzi, N. M. Zain, and N. A. A. Yusof (2019). J. Environ. Chem. Eng..  https://doi.org/10.1016/j.jece.2019.103331.CrossRefGoogle Scholar
  116. 116.
    N. Pauzi, N. M. Zain, and N. A. A. Yusof (2019). Bull. Chem. React. Eng. Catal.14, (1), 182–188.CrossRefGoogle Scholar
  117. 117.
    L. Alrehaily, et al. (2013). Phys. Chem. Chem. Phys.15, (1), 98–107.PubMedCrossRefPubMedCentralGoogle Scholar
  118. 118.
    A. El-Batal, et al. (2016). J. Chem. Pharm. Res.8, (4), 934–951.Google Scholar
  119. 119.
    H. Barabadi, et al. (2019). Inorg. Nano-Metal Chem.49, (2), 33–43.CrossRefGoogle Scholar
  120. 120.
    A. I. El-Batal, et al. (2019). J. Clust. Sci.30, (3), 687–705.CrossRefGoogle Scholar
  121. 121.
    M. S. Attia, et al. (2019). J. Clust. Sci.30, (4), 919–935.CrossRefGoogle Scholar
  122. 122.
    A. I. El-Batal, et al. (2016). Bioengineering3, (2), 14.PubMedCentralCrossRefGoogle Scholar
  123. 123.
    A. I. El-Batal, et al. (2017). J. Photochem. Photobiol. B Biol.173, 120–139.CrossRefGoogle Scholar
  124. 124.
    A. El-Batal, et al. (2013). J. Chem. Pharm. Res.5, (8), 1–15.Google Scholar
  125. 125.
    A. I. El-Batal, et al. (2018). Microb. Pathog.118, 159–169.PubMedCrossRefPubMedCentralGoogle Scholar
  126. 126.
    A. Baraka, et al. (2017). Chem. Pap.71, (11), 2271–2281.CrossRefGoogle Scholar
  127. 127.
    A. I. El-Batal, et al. (2016). Nanomater. Nanotechnol.6, 13.CrossRefGoogle Scholar
  128. 128.
    A. El-Batal, et al. (2014). Br. J. Pharm. Res.4, (21), 2525.CrossRefGoogle Scholar
  129. 129.
    A. Hanora, et al. (2016). J. Chem. Pharm. Res.8, (3), 405–423.Google Scholar
  130. 130.
    A. Ashour, et al. (2018). Particuology40, 141–151.CrossRefGoogle Scholar
  131. 131.
    G. Govindasamy, et al. (2019). J. Mater. Sci. Mater. Electron.30, (17), 16463–16477.CrossRefGoogle Scholar
  132. 132.
    P. K. Tiwari, et al. (2019). Ecotoxicol. Environ. Saf.176, 321–329.PubMedCrossRefPubMedCentralGoogle Scholar
  133. 133.
    H. Dong and G. M. Koenig (2019). CrystEngComm.  https://doi.org/10.1039/C9CE00679F.CrossRefGoogle Scholar
  134. 134.
    M. I. A. Abdel Maksoud, et al. (2019). J. Sol–Gel Sci. Technol.90, (3), 631–642.CrossRefGoogle Scholar
  135. 135.
    P. Belavi, et al. (2012). Mater. Chem. Phys.132, (1), 138–144.CrossRefGoogle Scholar
  136. 136.
    M. A. Maksoud, et al. (2019). J. Mater. Sci. Mater. Electron.30, 1–12.CrossRefGoogle Scholar
  137. 137.
    K. Pal, M. A. Elkodous, and M. M. Mohan (2018). J. Mater. Sci. Mater. Electron.29, (12), 10301–10310.CrossRefGoogle Scholar
  138. 138.
    M. Bashir and S. Haripriya (2016). Int. J. Biol. Macromol.93, 476–482.PubMedCrossRefPubMedCentralGoogle Scholar
  139. 139.
    E. R. Arakelova, et al. (2014). Int. J. Med. Heal. Pharm. Biomed. Eng.8, 33–38.Google Scholar
  140. 140.
    M. A. Maksoud, et al. (2019). Microb. Pathog.127, 144–158.PubMedCrossRefPubMedCentralGoogle Scholar
  141. 141.
    S. Pal, Y. K. Tak, and J. M. Song (2007). Appl. Environ. Microbiol.73, (6), 1712–1720.PubMedPubMedCentralCrossRefGoogle Scholar
  142. 142.
    A. Satyvaldiev, et al. Copper nanoparticles: synthesis and biological activity. IOP Conference Series: Materials Science and Engineering (IOP Publishing, Bristol, 2018).Google Scholar
  143. 143.
    V. Belava, et al. (2017). Nanoscale Res. Lett.12, (1), 250.PubMedPubMedCentralCrossRefGoogle Scholar
  144. 144.
    M. S. Rubina, et al. (2017). J. Nanostruct. Chem.7, (3), 249–258.CrossRefGoogle Scholar
  145. 145.
    A. Pugazhendhi, et al. (2018). Microb. Pathog.122, 84–89.PubMedCrossRefPubMedCentralGoogle Scholar
  146. 146.
    C. Ashajyothi, et al. (2016). J. Nanostruct. Chem.6, (4), 329–341.CrossRefGoogle Scholar
  147. 147.
    H.-J. Park, et al. (2013). Chemosphere92, (5), 524–528.PubMedCrossRefPubMedCentralGoogle Scholar
  148. 148.
    H. A. Ammar, G. H. Rabie, and E. Mohamed (2019). Bioprocess Biosyst. Eng..  https://doi.org/10.1007/s00449-019-02188-5.CrossRefPubMedPubMedCentralGoogle Scholar
  149. 149.
    E. Prokhorov, et al. (2019). Colloids Surf. B Biointerfaces180, 186–192.PubMedCrossRefPubMedCentralGoogle Scholar
  150. 150.
    P. K. Stoimenov, et al. (2002). Langmuir18, (17), 6679–6686.CrossRefGoogle Scholar
  151. 151.
    M. F. Khan, et al. (2016). Sci. Rep.6, 27689.PubMedPubMedCentralCrossRefGoogle Scholar
  152. 152.
    A. Shinde, J. Ganu, and P. Naik (2012). J. Dental Allied Sci.1, (2), 63.CrossRefGoogle Scholar
  153. 153.
    H. E. Alexander and G. Leidy (1947). J. Exp. Med.85, (4), 329–338.PubMedPubMedCentralCrossRefGoogle Scholar
  154. 154.
    W. Umbreit (1949). J. Biol. Chem.177, (2), 703–714.PubMedPubMedCentralGoogle Scholar
  155. 155.
    H. Barabadi, et al. (2019). Medicina55, (8), 439.PubMedCentralCrossRefGoogle Scholar
  156. 156.
    K. Mortezaee, et al. (2019). Chem. Biol. Interact.312, 108814.PubMedCrossRefPubMedCentralGoogle Scholar
  157. 157.
    E. Assadian, et al. (2018). Biol. Trace Elem. Res.184, (2), 350–357.PubMedCrossRefPubMedCentralGoogle Scholar
  158. 158.
    R. Mani, et al. (2019). Environ. Sci. Pollut. Res..  https://doi.org/10.1007/s11356-019-06095-w.CrossRefGoogle Scholar
  159. 159.
    S. Mahjouri, et al. (2018). Plant Cell Tissue Organ Cult.135, (2), 223–234.CrossRefGoogle Scholar
  160. 160.
    K. Shahzad, et al. (2018). Environ. Sci. Pollut Res.25, (16), 15943–15953.CrossRefGoogle Scholar
  161. 161.
    J.-K. Wan, et al. (2018). J. Appl. Phycol.30, (6), 3153–3165.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Drug Radiation Research Department, Biotechnology DivisionNational Center for Radiation Research and Technology (NCRRT), Atomic Energy AuthorityCairoEgypt
  2. 2.Bacterial Disease Research Department, Plant Pathology Research InstituteAgricultural Research Center (ARC)GizaEgypt
  3. 3.Potato Brown Rot ProjectMinistry of AgricultureGizaEgypt
  4. 4.Botany and Microbiology Department, Faculty of ScienceAl-Azhar UniversityCairoEgypt
  5. 5.Chemical Engineering Department, Military Technical CollegeCairoEgypt

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