Mikrobiol. Z. 2021; 83(3):81-91.
doi: https://doi.org/10.15407/microbiolj83.03.081

Natural and Synthetic Nanomaterials in Microbial Biotechnologies for Crop Production

I.K. Kurdish

Zabolotny Institute of Microbiology and Virology, NAS of Ukraine
154 Akad. Zabolotny Str., Kyiv, 03143, Ukraine

Nanoparticles of various materials (up to 100 nm in size) are characterized by a large surface area, which significantly increases their reactive properties. This makes promissing the studies of their possible application in different technologies, including those in the agricultural production sector. This review summarizes the literature on the distribution and properties of natural nanoparticles in the environment. The features of the interaction between various types of microorganisms, nanoparticles of natural minerals, oxides of metals and carbon nanoparticles are analyzed. The review also summarizes the data on the effect of nanoparticles of different origin on microorganisms, plant growth and development. It also presents the information on the effectiveness of the use of clay mineral nanoparticles in the production of complex bacterial preparations for plant growing and the prospects of using nanoparticles of metal oxides in this industry.

Keywords: nanoparticles of natural and synthetic origin, interaction of nanoparticles, microorganisms and plants.

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  1. Bhupinder Singh Sekhon. Nanotechnology in agri-food production: an overview. Nanotechnol Sci Appl. 2014; 7:31–53. https://doi.org/10.2147/NSA.S39406
  2. Nelson GC, Rosegrant MW, Palazzo A, et al. Book: Food security, farming and climate change to 2050: scenarios, results, policy option. Washington: 2010.
  3. Mishra G, Kumar N, Giri K, Pandey S. In vitro interaction between fungicidal and beneficial plant growth promoting Rhizobacteria. Afr J Agric Res. 2013; 8(45):5630–5633.
  4. United Nations Environment Programme. Davos, Switzerland. 2014. http://www.unep.org
  5. Kurdish IK. [Granulated microbial preparation for plant-growing: science and practice]. Kyiv: KVITs; 2001. Russian.
  6. Kurdish IK. [Introduction of microorganisms in agroecosystems]. Kyiv: Naukova Dumka; 2010. Ukrainian.
  7. Godos A, Knauer K, Bucheli TD. Nanomaterials in Plant Protection and Fertilization: Current State, Foreseen Applications, and Research Priorities. J Agric Food Chem. 2012; 69(39):9781–9792. https://doi.org/10.1021/jf302154y
  8. Jampilek J, Kralova K. Nanomaterials for Delivery of Nutrients and Growth-Promoting Compounds to Plants. In Book: Nanotechnology: An Agricultural Paradigm. Springer Nature Singapure LTD; 2017. p. 177–226. https://doi.org/10.1007/978-981-10-4573-8_9
  9. Taniguchi N. On the Basic Concept of Nanotechnology. Proc Int Conf Prod Eng. Tokyo. 1974; Part. II.
  10. Ovcharenko FD, Vaschenko ZM, Pogrebnyak MK. [Development of domestic colloidal chemistry]. Kyiv: Naukova Dumka; 1984. Russian.
  11. Friedrichsberg DA. [Colloidal chemistry course]. Moscow: Chemistry; 1984. Russian.
  12. Wada K. Allophane and imogolite. In: Dixon JB, Weed SB, editors. Minerals in Soil Environments, second edition. Madison: Soil Science Society of America; 1989. p. 1051–1087.
  13. Balabanov VI. [Nanotechnology. Science of the future.] Moscow: Eksmo; 2009. Russian.
  14. Prasad R, Kumar V, Prasad KS. Nanotechnology in sustainable agriculture: present concerns and future aspects. Afr J Biotechnol. 2014; 13:705–713. https://doi.org/10.5897/AJBX2013.13554
  15. Jampílek J, Králová K. Application of nanotechnology in agriculture and food industry, its prospects and risks. Ecol Chem Eng. 2015; 22:321–361. https://doi.org/10.1515/eces-2015-0018
  16. Kurdish IK. Interaction of Microorganisms with Nanomaterials as a Basis for Creation of High-Efficiency Biotechnological Preparation. In: Prasad R, Kumar V, Kumar R, Choudhary D, editors. Nanobiotechnology in Bioformulations. Springer; 2019. p. 259–287. https://doi.org/10.1007/978-3-030-17061-5_11
  17. Emily S. Bernhardt, Benjamin P. Colman, Michael F. Hochella, Bradley J. Cardinale, Roger M. Nisbet, Curtis J. Richardson, Liyan Yin. 2010. An Ecological Perspective on Nanomaterial Impacts in the Environment. J Environ Qual. 2010; 39(1). https://doi.org/10.2134/jeq2009.0479
  18. Gilbert B, Banfield JF. Molecular-scale processes involving nanoparticulate minerals in biogeochemical systems. Rev Mineral Geochem. 2005; 59:109–155. https://doi.org/10.2138/rmg.2005.59.6
  19. Hochella MF, Lower SK, Maurice PA, Penn RL, Sahai N, Sparks DL, Twining BS. Nanominerals, mineral nanoparticles, and Earth systems. Science. 2008; 319:1631–1635. https://doi.org/10.1126/science.1141134
  20. Sharoon Griffin, Muhammad Irfan Masood, Muhammad Jawad Nasim, Muhammad Sarfraz, Azubuike Peter Ebokaiwe, Karl-Herbert Schäfer, Cornelia M. Keck, Claus Jacob. Natural  Nanoparticles: A Particular Matter Inspired by Nature Antioxidants (Basel). 2018; 7(1):3. https://doi.org/10.3390/antiox7010003
  21. Hailiang Dong, Anhuai Lu. Mineral microbe interactions  and implications for remediation. Elements. 2012; 8(2):95–100. https://doi.org/10.2113/gselements.8.2.95
  22. Hochella MF, Jr. Nanogeoscience: From origins to cutting-edge applications. Elements (Chantilly, VA, U.S.). 2008; 4:373–379. https://doi.org/10.2113/gselements.4.6.373
  23. Buseck PR, Adachi K. Nanoparticles in the atmosphere. Elements (Chantilly, VA, U.S.). 2008; 4:389–394. https://doi.org/10.2113/gselements.4.6.389
  24. Kulmala L, Kerminen VM. On the formation and growth of atmospheric nanoparticles. Atmos Res. 2008; 90:132–150. https://doi.org/10.1016/j.atmosres.2008.01.005
  25. Hassellov M, von der Kammer F. Iron oxides as geochemical nanovectors for metal transport in soil-river systems. Elements (Chantilly, VA, U.S.). 2008; 4:401–406. https://doi.org/10.2113/gselements.4.6.401
  26. Hochella MF, Mogk DW, Ranville J, et al. Natural, incidental and engineered nanomaterials and their impacts on the Earth system. Science. 2019; 363:82–99. https://doi.org/10.1126/science.aau8299
  27. Lahde A, Gudmundsdottir SS, Joutsensaari J, Tapper U, Ruusunen J, Ihalainen M, Karhunen T, Torvela T, Jokiniemi J, Jarvinen K, et al. In vitro evaluation of pulmonary deposition of airborne volcanic ash. Atmos Environ. 2013; 70:18–27. https://doi.org/10.1016/j.atmosenv.2012.12.048
  28. Murr LE, Guerrero PA. Carbon nanotubes in wood soot. Atmos Sci Lett. 2006; 7:93–95. https://doi.org/10.1002/asl.138
  29. Gorby YA, Yanina S, McLean JS, Rosso KM, et al. Electricity conductive bacterial nanowires produced by Shewanella oneidensis strain MR-1 and other microorganisms. PNAS. 2006; 103(30):11358–11363. https://doi.org/10.1073/pnas.0604517103
  30. Theng BKG, Yuan G. Nanoparticles in the Soil Environtments. Elements. 2007; 4(6):395–399. https://doi.org/10.2113/gselements.4.6.395
  31. Kaurichev IS, Panov NP, Rozov NN, Stratonovich MV, Fokin AD. [Soil Science]. Moscow: Agropromizdat; 1989. Russian.
  32. Tate RL. Soil microbial diversity research: whither to now? Soil Sci. 1997; 162(9):605–606. https://doi.org/10.1097/00010694-199709000-00001
  33. Sukhovitskaya LA, Mohort TG, Klyshko GM. [Survival of Rhizobium in binary populations with phosphate-mobilizing bacteria and some criteria for the selection of rhizobial-phosphate-mobilizing composites]. Vestsi AN Belarus, ser. Biological Sciences. 1997; 3:64–69. Russian.
  34. Umarov MM, Kurakov AV, Stepanov AL. [Microbiological transformation of nitrogen in soil]. Moscow: GEOS; 2007. Russian.
  35. Blango MG, Mulvey MA. Bacterial landlines: Contact-dependent signaling in bacterial populations. Curr Opin Microbiol. 2009; 12:177–181. https://doi.org/10.1016/j.mib.2009.01.011
  36. Gordienko AS, Zbanatskaja IV, Kurdish IK. Change in electrosurface properties of Methylomonas rubra cells at contact interaction with particles of silicon dioxide. Can J Microbiol. 1993; 39(9):902–905. https://doi.org/10.1139/m93-136
  37. Fomina M, Skorochod I. Microbial Interaction with Clay Minerals and its Environmental and Biotechnological Implications. Minerals. 2020; 10(10):861. https://doi.org/10.3390/min10100861
  38. Gadd GM. Metals, minerals and microbes: geomicrobiology and bioremediation. Microbiology. 2010; 156:609–643. https://doi.org/10.1099/mic.0.037143-0
  39. Wacey D, Kilburn MR, Saunders M, Cliff J, Brasier MD. Microfossils of sulphur-metabolizing cells in 3.4-billion-year-old rocks of Western Australia. Nature Geoscience. 2011; 4:698–702. https://doi.org/10.1038/ngeo1238
  40. Altermann W, Kazmierczak J, Oren A, Wright DT. Cyanobacterial calcification and its rockbuilding potential during 3.5 billion years of Earth history. Geobiology. 2006; 4:147–166. https://doi.org/10.1111/j.1472-4669.2006.00076.x
  41. Konhauser KO, Lalonde SV, Planavsky NJ, Pecoits E, Lyons TW, Mojzsis S, Rouxel OJ, Barley M, Rosiere C, Fralick PW, Kump LR, Bekker A. Aerobic bacterial pyrite oxidation and acid rock drainage during the Great Oxidation Event. Nature. 2011; 478:369–373. https://doi.org/10.1038/nature10511
  42. Hazen RM, Ferry JM. Mineral evolution: Mineralogy in the fourth dimension. Elements. 2010; 6:9–12. https://doi.org/10.2113/gselements.6.1.9
  43. Kennedy M, Droser M, Mayer LM, Pevear D, Mrofka D. Late Precambrian oxygenation: Inception of the clay mineral factory. Science. 2006; 311:1446–1449. https://doi.org/10.1126/science.1118929
  44. Konhauser KO. Introduction to Geomicrobiology. Oxford: Blackwell Publishing; 2007.
  45. Dong H, Lu A. Mineral microbe interactions and implications for remediation. Elements. 2012; 8(2):95–100. https://doi.org/10.2113/gselements.8.2.95
  46. Lu X, Wang H. Microbial oxidation of sulfide tailings and its environmental consequences. Elements. 2012; 8:119–124. https://doi.org/10.2113/gselements.8.2.119
  47. Rogers JR, Bennett PC. Mineral stimulation of subsurface microorganisms: release of limiting nutrients from silicates. Chemical Geology. 2004; 203:91–108. https://doi.org/10.1016/j.chemgeo.2003.09.001
  48. Kostka JE, Dalton DD, Skeleton H, Dollhopf S, Stucki JW. Growth of Iron(III)-Reducing Bacteria on Clay Minerals as the Sole Electron Acceptor and Comparison of Growth Yields on a Variety of Oxidized Iron Forms. Applied and Environmental Microbiology. 2002; 68(12):6256–6262. https://doi.org/10.1128/AEM.68.12.6256-6262.2002
  49. Ehrlich HL. How microbe influence mineral growth and dissolution. Chem Geol. 1996; 132(1):5–9. https://doi.org/10.1016/S0009-2541(96)00035-6
  50. Yanbo Wang, Jianzhong Han. Interaction of photosynthetic bacterium, Rhodopseudomonas palustris, with montmorillonite clay. International Journal of Engineering, Science and Technology. 2010; 2(7):36–43. https://doi.org/10.4314/ijest.v2i7.63738
  51. Jacoby R, Peukert M, Succurro A, Koprivova A, Kopriva S. The Role of Soil Microorganisms in Plant Mineral Nutrition – Current Knowledge and Future Directions. Front Plant Sci. 2017; 8:16–17. https://doi.org/10.3389/fpls.2017.01617
  52. Xie XD, Zhang GS. Environmental significance of the interaction between minerals and microbes. Acta Petrologica et Mineralogica. 2001; 20(4):382–386.
  53. Chaerun SK, Tazaki K, Asada R, Kogure K. Interaction between clay minerals and hydrocarbon-utilizing indigenous microorganisms in high concentrations of heavy oil: implications for bioremediation. Clay Miner. 2005; 40(1):105–114. https://doi.org/10.1180/0009855054010159
  54. Kurdish IK, Titova LV, Tsimberg EA. [Effect of aerosil on the growth of Azotobacter chroococcum]. Mikrobiol Z. 1993; 55(1):38–42. Russian.
  55. Kurdish IK, Kigel NF, Bortnik SF. [Stabilization of the physiological activity of the methanotroph Methylomonas rubra 15sh during storage]. Mikrobiol Z. 1993; 55(4):37–43. Russian.
  56. Kurdish IK, Antonyuk TS. [The influence of clay minerals on the viability of some bacteria at elevated  temperatures]. Mikrobiol Z. 1999; 61(3):3–8. Russian.
  57. Gordienko AS, Kurdish IR. [The effect of the clay mineral palygorskite on the survival of bacteria during their dehydration]. Microbiology. 1999; 32(5):75–78. Russian.
  58. Kurdish IK, Titova LV. [Granular Preparation of Azotobacter Containig Clay Minerals]. Appl Biochem and Microbiol. 2000; 36(4):418–420. Russian. https://doi.org/10.1007/BF02738054
  59. Kurdish IK, Titova LV. [Use of High-Dispersion Materials for Culturing and Obtaining Granular Agrobacterium radiobacter Preparations]. Appl Biochem and Microbiol. 2001; 37(3):318–321. Russian. https://doi.org/10.1023/A:1010201806576
  60. Kurdish IK, Roy AA, Garagulya AD, Kiprianova EA. [Survival and antagonistic activity of Pseudomonas aureofaciens UKM B-111 when stored in highly dispersed materials]. Microbiology. 1999; 68(3):387–391. Russian.
  61. Rong X, Huang Q, ChenW. Microcalorimetric investigation on the metabolic activity of Bacillus thuringiensis as influenced by kaolinite, montmorillonite and goethite. Appl Clay Sci. 2007; 38(1–2):97–103. https://doi.org/10.1016/j.clay.2007.01.015
  62. Dale A. Pelletier, Anil K. Suresh, Gregory A. Holton, Catherine K, et al. Effects of Engineered Cerium Oxide Nanoparticles on Bacterial Growth and Viability. Appl and Environm Microbiol. 2010; 76(24):7981–7989. https://doi.org/10.1128/AEM.00650-10
  63. Jiang D, Huang Q, Cai P, Rong X, Chen W. Adsorption of Pseudomonas putida on clay minerals and iron oxide. Colloids and Surfaces B: Biointerfaces. 2007; 54(2):217–221. https://doi.org/10.1016/j.colsurfb.2006.10.030
  64. Wang Y, Han J. Interaction of photosynthetic bacterium, Rhodopseudomonas palustris, with montmorillonite clay. International Journal of Engineering, Science and Technology. 2010; 2(7):36–43. https://doi.org/10.4314/ijest.v2i7.63738
  65. Karunakaran G, Suriyaprabha R, Manivasakan P, et al. Effect of nanosilica and silicon sources on plant growth promoting rhizobacteria, soil nutrients and maise seed germination. JIET Nanotechnology. 2013; 7(3):70–77. https://doi.org/10.1049/iet-nbt.2012.0048
  66. Titova LV, Antipchuk AF, Kurdish IK, et al. [Influence of highly dispersed materials on the physiological activity of bacteria of the genus Azotobacter]. Mikrobiol Z. 1994; 56 (3):60–65. Russian.
  67. Kurdish IK, Bega ZT. [Effect of Argillaceous Minerals on the Growth of Phosphate-mobilizing Bacteria Bacillus subtilis]. Appl Biochem and Microbiol. 2006; 42(4):438–442. Russian. https://doi.org/10.1134/S0003683806040089
  68. Kurdish I, Chobotarov A, Gritsay R. Effect of nanoparticles of natural minerals, iron and mangan compounds, on the growth and superoxide dismutase activity of Bacillus subtilis IMV B-7023. Journal of Microbiology, Biotechnology and Food Science. 2020; 10(1):130–133. https://doi.org/10.15414/jmbfs.2020.10.1.130-133
  69. Kurdish I, Roy A, Skorochod I, et al. Free-flowing complex bacterial preparation for crop and efficiency of its use in agroecosystems. J Microbiol Biotechnol and Food Science. 2015; 4(6):527–531. https://doi.org/10.15414/jmbfs.2015.4.6.527-531
  70. Kurdish IK, Gordienko AS. [Interaction of microorganisms with clay minerals is the basis for creation of granulated bacterial preparations in complex diy for growing]. Silskogosp microbiol. 2006; 4:31–38. Ukrainian.
  71. Skorochod IO, Roy AO, Kurdish IK. Influence of Silica Nano- particles on Antioxidant Potential of Bacillus subtilis IMV B-7023. Nanoscale Research Letters. 2016; 139:1–11. https://doi.org/10.1186/s11671-016-1348-2
  72. Skorochod IO, Kurdish IK. [Influence of nanoparticles of silica and vermiculite on activity of enzymes of antioxidant defense Bacillus subtilis IMV B-7023]. Microbiology & Biotechnology. 2013; 1:59–67. Ukrainian.
  73. Rios F, Fernandez-Alteaga A, Fernandez-Serrano M, et al. Silica micro-and nanoparticles reduce the toxicity of surfactant solutions. J Hazardous Materials. 2018; 353:436–443. https://doi.org/10.1016/j.jhazmat.2018.04.040
  74. Cobotarov A, Volkogon M, Voytenko L, Kurdish I. Accumulation of phytohormones by soil bacteria Azotobacter vinelandii and Bacillus subtilis under the influence of nanomaterials. J Microbiol Biotechnol and Food Science. 2017; 18(73):271–274. https://doi.org/10.15414/jmbfs.2017/18.7.3.271-274
  75. Sekhon BS. Nanotechnology in agri-food production: an overview. Nanotechnol Sci Appl. 2014; 20(7):31–53. https://doi.org/10.2147/NSA.S39406
  76. Prasad R, Bhattacharyya A, Nguyen QD. Nanotechnology in Sustainable Agriculture: Recent Development, Challenges, and Perspective. Front Microbiol. 2017. https://doi.org/10.3389/fmicb.2017.01014
  77. Singh S, Kumar V, Romero R, Sharma R, Singh J. Application of Nanoparticles in Wastewater Treatment In Book: Nanotechnology in Bioformulation. Ram Prasad, et al., editors. 2019. p. 317–329. https://doi.org/10.1007/978-3-030-17061-5_17
  78. Nasr M. Nanotechnology Application in Agricultural Sector. In Book: Nanotechnology in Bioformulation. Ram Prasad, et al., editors. 2019. p. 317–329. https://doi.org/10.1007/978-3-030-17061-5_13
  79. Ditta A. How helpful is nanotechnology in agriculture? Advances in Natural Sciences: Nanoscience and Nanotechnology. 2012; 3(3):1–10. https://doi.org/10.1088/2043-6262/3/3/033002
  80. Roy DN, Goswami R, Pal A. Nanomaterial and toxicity: What can proteomics tell us about the nanotoxicology? Xenobiotica. 2017; 47:632–643. https://doi.org/10.1080/00498254.2016.1205762
  81. Haira A, Mondel NK. Effect of ZnO and TiO2 nanoparticles on germination, biochemical and morphoanatomical attributes of Cicer arientinum. Energ Ecol Environ. 2017; 2(4):277–288. https://doi.org/10.1007/s40974-017-0059-6
  82. Stasik OO, Pryadkina GO, Kiriziy DA, Sytnik SK, Kapitanska OS, Michno AI, Makharinska NM. Effect of foliar treatment with microelement complex, obtained by nanotechnology, on the photosynthetic activity of winter wheat plants under different moisture. Plant Physiology and Genetics. Fiziol rast genet. 2020; 52(1):46–63. https://doi.org/10.15407/frg2020.01.046
  83. Mukherjee A, Majumdar S, Servin AD, Pagano L, Dankher OP, White JC. Carbon Nanomaterials in Agriculture: A Critical Review. 2016; 7:172. https://doi.org/10.3389/fpls.2016.00172
  84. Du W, Tan W, Peralta-Videa JR, Gardea-Torresdey JL, Ji R, Yin Y, Guo H. Interaction of metal oxide nanoparticles with higher terrestrial plants: Physiological and biochemical aspects. Plant Physiol Biochem. 2017; 110:210–225. https://doi.org/10.1016/j.plaphy.2016.04.024
  85. Tripathi DK, Singh S, Singh VP, Prasad SM, Dubey NK, Chauhan DK. Silicon nanoparticles more effectively alleviated UV-B stress than silicon in wheat (Triticum aestivum) seedlings. Plant Physiol Biochem. 2017; 110:70–81. https://doi.org/10.1016/j.plaphy.2016.06.026
  86. Parada J, Rubilar O, Fernandez-Baldo MA, et al. The nanotechnology among US: are metal and metal oxides nanoparticles a nano or mega risk for soil microbial communities? Journal Critical Rewiews in Biotechnology. 2019; 39(2):157–172. https://doi.org/10.1080/07388551.2018.1523865
  87. Vishnu D. Rajput, Tatiana Minkina, Svetlana Sushkova, Viktoriia Tsitsuashvili, Saglara Mandzhieva, Andrey Gorovtsov, Dina Nevidomskyaya, Natalya Gromacova. Effect of Nanoparticles on Crops and Soil Microbial Communities. Journal of Soils and Sediments. 2018; 18:2179–2187. https://doi.org/10.1007/s11368-017-1793-2
  88. Parameswari E, Udayasoorian C, Sebastian SP, Jayabalakrishnan RM. The bacterial potential of silver nanoparticles. Int Res J Biotechnol. 2010; 1(3):44–49.
  89. Laberty-Robert C, Long JW, Lucas EM, Pettigrew KA, Stroud RM, Doescher MS, Rolison DR. Sol-gel-derived ceria nanoarchitectures: synthesis, characterization, and electrical properties. Chem Mater. 2006; 18:50–58. https://doi.org/10.1021/cm051385t
  90. Laberty-Robert C, Long JW, Pettigrew KA, Stroud RM, Rolison DR. Ionic nanowires at 600°C: using nanoarchitecture to optimize electrical transport in nanocrystalline gadolinium-doped ceria. Adv Mater. 2007; 19:1734–1739. https://doi.org/10.1002/adma.200601840
  91. Perez JM, Asati A, Nath S, Kaittanis C. Synthesis of biocompatible dextran-coated nanoceria with pH-dependent antioxidant properties. Small. 2008; 4:552–556. https://doi.org/10.1002/smll.200700824
  92. Tarnuzzer RW, Colon J, Patil S, Seal S. Vacancy engineered ceria nanostructures for protection from radiation-induced cellular damage. Nano Lett. 2005; 5:2573–2577. https://doi.org/10.1021/nl052024f
  93. Brayner R, Ferrari-Iliou R, Brivois N, Djediat S, Benedetti MF, Fievet F. Toxicological impact studies based on Escherichia coli bacteria in ultrafine ZnO nanoparticles colloidal medium. Nano Lett. 2006; 6:866–870. https://doi.org/10.1021/nl052326h
  94. Kasemets K, Ivask A, Dubourguier HC, Kahru A. Toxicity of nanoparticles of ZnO, CuO and TiO2 to yeast Saccharomyces cerevisiae. Toxicol in Vitro. 2009; 23(6):1116–1122. https://doi.org/10.1016/j.tiv.2009.05.015
  95. Chavan S, Nadanathangam V. Effects of Nanoparticles on Plant Growth-Promoting Bacteria in Indian Agricultural Soil. Journal Agronomy. 2019; 9(3):140. https://doi.org/10.3390/agronomy9030140
  96. Lin D, Xing B. Root Uptake and Phytotoxicity of ZnO Nanoparticles. Environ Sci Technol. 2008; 42:5580–5585. https://doi.org/10.1021/es800422x
  97. Lee CW, Mahendra S, Zodrow K, Li D, Tsai YC, Braam J, Alvarez PJ. Developmental phytotoxicity of metal oxide nanoparticles to Arabidopsis taliana. Environ Toxicol Chem. 2010; 29:669–675. https://doi.org/10.1002/etc.58
  98. Boonyanitipong P, Kositsup B, Kumar P, Baruah S, Dutta J. Toxicity of ZnO and TiO2 nanoparticles on germinating rice seed Oryza sativa L. Int J Biosci Biochem and Bioinforma. 2011; 1(4):282–285. https://doi.org/10.7763/IJBBB.2011.V1.53
  99. Battke F, Leopold K, Maier M, Schmidhalter U, Schuster M. Palladium exposure of barley: uptake and effects. Plant Biol. 2008; 10:272–276. https://doi.org/10.1111/j.1438-8677.2007.00017.x
  100. Zhu H, Han J, Xiao JQ, Jin Y. Uptake translocation and accumulation of manufactured iron oxide nanoparticles by pumpkin plants. J Environ Monit. 2008; 10:713–717. https://doi.org/10.1039/b805998e
  101. Liu Q, Chen B, Wang Q, Shi X, Xiao Z, Lin J, Fang X. Carbon nanotubes as molecular transporters for walled plant cell. Nano Lett. 2009; 9:1007–1010. https://doi.org/10.1021/nl803083u
  102. Tan XM, Lin C, Fugetsu B. Studies on toxicity of multi-walled carbon nanotubes on suspension rice cells. Carbon. 2009; 47:3479–3487. https://doi.org/10.1016/j.carbon.2009.08.018
  103. Qiao R, Roberts AP, Mount AS, Klaine SJ, Ke PC. Translocation of C60 and its derivatives across a lipid bilayer. Nano Lett. 2007; 7(3):614–619. https://doi.org/10.1021/nl062515f
  104. Cabiscol E, Tamarit J, Ros J. Oxidative stress in bacteria and protein damage by reactive oxygen species. Int Microbiol. 2000; 3:3–8.
  105. Adams LK, Lyon DY, Alvarez PJ. Comparative eco-toxicity of nanoscale TiO2, SiO2, and ZnO water suspensions. Water Res. 2006; 40:3527–3532. https://doi.org/10.1016/j.watres.2006.08.004