Environmental Toxicity and Antimicrobial Efficiency of Titanium Dioxide Nanoparticles in Suspension

Abstract

The aim of this work was to evaluate the photokilling efficiency of synthesized titanium dioxide nanoparticles in suspension. Two strains of Escherichia coli, Lactobacillus casei rhamnosus and Staphylococcus aureus were used as probes to test the photokilling activities of the nanoparticles. The toxicity effects of TiO2 nanoparticles on the environment were determined by a standard test using gram-negative bioluminescent bacteria Vibrio fischeri. The antimicrobial activity of these nanoparticles (NPs) was then investigated versus NPs concentration, UV irradiation time and micro- organism strains. We evaluated the LC50 values of the nanoparticles suspension by counting the Colony-Forming Units. Results highlighted the differences in bacteria sensitivity facing photokilling treatment induced by the irradiation of anatase TiO2 nanoparticles suspension. At the concentration of 1 g·L-1 TiO2, tested bacteria were killed after 30 minutes of photo-treatment. Using different TiO2 concentrations, the Staphylococcus aureus gram-positive/catalase-positive bacteria were more resistant than gram-negative/catalase-positive ones or gram-positive/catalase-negative bacteria. An effect of UV irradiation was evaluated by the quantification of hydrogen peroxide generated by the photolysis of water molecules in presence of the nanoparticles with or without the most resistant bacterium (S. aureus). After 30 minutes with UV irradiation in these two conditions, the concentration of hydrogen peroxide was 35 μM in presence of 1.2 g·L-1 TiO2 suspension. This result suggested that the resistance mechanism of S. aureus was not due to an extracelullar H2O2 enzymatic degradation.

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Bonnet, M. , Massard, C. , Veisseire, P. , Camares, O. and Awitor, K. (2015) Environmental Toxicity and Antimicrobial Efficiency of Titanium Dioxide Nanoparticles in Suspension. Journal of Biomaterials and Nanobiotechnology, 6, 213-224. doi: 10.4236/jbnb.2015.63020.

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1] Backer, L.C., Ashley, D.L., Bonin, M.A., Cardinali, F.L., Kieszak, S.M. and Wooten, J.V. (2000) Household Exposures to Drinking Water Disinfection By-Products: Whole Blood Trihalomethane Levels. Journal of Exposure Science and Environmental Epidemiology, 10, 321-326.
http://dx.doi.org/10.1038/sj.jea.7500098
[2] Batterman, S., Zhang, L.Z. and Wang, S.Q. (2000) Quenching of Chlorination Disinfection By-Product Formation in Drinking Water by Hydrogen Peroxide. Water Research, 34, 1652-1658.
http://dx.doi.org/10.1016/S0043-1354(99)00294-8
[3] Miltner, R.J., Shukairy, H.M. and Summers, R.S. (1992) Disinfection By-Product Formation and Control by Ozonation and Biotreatment. Journal of the American Water Works Association, 84, 53-62.
[4] von Gunten, U. (2003) Ozonation of Drinking Water: Part II. Disinfection and By-Product Formation in Presence of Bromide, Iodide or Chlorine. Water Research, 37, 1469-1487.
http://dx.doi.org/10.1016/S0043-1354(02)00458-X
[5] Hammes, F., Salhi, E., Kster, O., Kaiser, H.P., Egli, T. and von Gunten, U. (2006) Mechanistic and Kinetic Evaluation of Organic Disinfection By-Product and Assimilable Organic Carbon (AOC) Formation during the Ozonation of Drinking Water. Water Research, 40, 2275-2286.
http://dx.doi.org/10.1016/j.watres.2006.04.029
[6] Sunada, K., Watanabe, T. and Hashimoto, K. (2003) Studies on Photokilling of Bacteria on TiO2 Thin Film. Journal of Photochemistry and Photobiology A: Chemistry, 156, 227-233.
http://dx.doi.org/10.1016/S1010-6030(02)00434-3
[7] Tsuang, Y.H., Sun, J.S., Huang, Y.C., Lu, C.H., Chang, W.H.S. and Wang, C.C. (2008) Studies of Photokilling of Bacteria Using Titanium Dioxide Nanoparticles. Artificial Organs, 32, 167-174.
http://dx.doi.org/10.1111/j.1525-1594.2007.00530.x
[8] Guan, K.S. (2005) Relationship between Photocatalytic Activity, Hydrophilicity and Self-Cleaning Effect of TiO2/ SiO2 Films. Surface and Coatings Technology, 191, 155-160.
http://dx.doi.org/10.1016/j.surfcoat.2004.02.022
[9] Mellott, N., Durucan, C., Pantano, C. and Guglielmi, M. (2006) Commercial and Laboratory Prepared Titanium Dioxide Thin Films for Self-Cleaning Glasses: Photocatalytic Performance and Chemical Durability. Thin Solid Films, 502, 112-120.
http://dx.doi.org/10.1016/j.tsf.2005.07.255
[10] Guan, H.M., Zhu, L.H., Zhou, H.H. and Tang, H.Q. (2008) Rapid Probing of Photocatalytic Activity on Titania-Based Self-Cleaning Materials Using 7-Hydroxycoumarin Fluorescent Probe. Analytica Chimica Acta, 608, 73-78.
http://dx.doi.org/10.1016/j.aca.2007.12.009
[11] Wu, D., Long, M., Zhou, J., Cai, W., Zhu, X., Chen, C. and Wu, Y. (2009) Synthesis and Characterization of Self- Cleaning Cotton Fabrics Modified by TiO2 through a Facile Approach. Surface and Coatings Technology, 203, 3728- 3733.
http://dx.doi.org/10.1016/j.surfcoat.2009.06.008
[12] Chen, W.J., Tsai, P.J. and Chen, Y.C. (2008) Functional Fe3O4/TiO2 Core/Shell Magnetic Nanoparticles as Photo- Killing Agents for Pathogenic Bacteria. Small, 4, 485-491.
http://dx.doi.org/10.1002/smll.200701164
[13] Choi, J.Y., Kim, K.H., Choy, K.C., Oh, K.T. and Kim, K.N. (2007) Photocatalytic Antibacterial Effect of TiO2 Film Formed on Ti and TiAg Exposed to Lactobacillus acidophilus. Journal of Biomedical Materials Research Part B: Applied Biomaterials, 80, 353-359.
http://dx.doi.org/10.1002/jbm.b.30604
[14] Kubacka, A., Ferrer, M., Martnez-Arias, A. and Fernández-Garca, M. (2008) Ag Promotion of TiO2-Anatase Disinfection Capability: Study of Escherichia coli Inactivation. Applied Catalysis B: Environmental, 84, 87-93.
[15] Kahru, A., Tomson, K., Pall, T. and Külm, I. (1996) Study of Toxicity of Pesticides Using Luminescent Bacteria Photobacterium phosphoreum. Water Science and Technology, 33, 147-154.
http://dx.doi.org/10.1016/0273-1223(96)00292-2
[16] Barrena, R., Casals, E., Colon, J., Font, X., Sanchez, A. and Puntes, V. (2009) Evaluation of the Ecotoxicity of Model Nanoparticles. Chemosphere, 75, 850-857.
http://dx.doi.org/10.1016/j.chemosphere.2009.01.078
[17] Cai, R., Kubota, Y., Shuin, T., Sakai, H., Hashimoto, K. and Fujishima, A. (1992) Induction of Cytotoxicity by Photoexcited TiO2 Particles. Cancer Research, 52, 2346-2348.
[18] Gogniat, G., Thyssen, M., Denis, M., Pulgarin, C. and Dukan, S. (2006) The Bactericidal Effect of TiO2 Photocatalysis Involves Adsorption onto Catalyst and the Loss of Membrane Integrity. FEMS Microbiology Letters, 258, 18-24.
http://dx.doi.org/10.1111/j.1574-6968.2006.00190.x
[19] Jang, H.D., Kim, S.K. and Kim, S.J. (2001) Effect of Particle Size and Phase Composition of Titanium Dioxide Nanoparticles on the Photocatalytic Properties. Journal of Nanoparticle Research, 3, 141-147.
http://dx.doi.org/10.1023/A:1017948330363
[20] Braydich-Stolle, L.K., Schaeublin, N.M., Murdock, R.C., Jiang, J., Biswas, P., Schlager, J.J. and Hussain, S.M. (2009) Crystal Structure Mediates Mode of Cell Death in TiO2 Nanotoxicity. Journal of Nanoparticles Research, 11, 1361- 1374.
http://dx.doi.org/10.1007/s11051-008-9523-8
[21] Xia, T., Kovochich, M., Brant, J., Hotze, M., Sempf, J. and Oberley, T. (2006) Comparison of the Abilities of Ambient and Manufactured Nanoparticles to Induce Cellular Toxicity According to an Oxidative Stress Paradigm. Nano Letters, 6, 1794-1807.
http://dx.doi.org/10.1021/nl061025k
[22] Singh, N., Manshian, B., Jenkins, G.J.S., Griffiths, S.M., Williams, P.M., Maffeis, T.G.G., Wright, C.J. and Doak, S.H. (2009) NanoGenotoxicology: The DNA Damaging Potential of Engineered Nanomaterials. Biomaterials, 30, 3891- 3914.
http://dx.doi.org/10.1016/j.biomaterials.2009.04.009
[23] Gou, N. and Gu, A.Z. (2011) A New Transcriptional Effect Level Index (TELI) for Toxicogenomics-Based Toxicity Assessment. Environmental Science and Technology, 45, 5410-5417.
http://dx.doi.org/10.1021/es200455p
[24] Hu, C., Lan, Y.Q., Qu, J.H., Hu, X.X. and Wang, A.M. (2006) Ag/AgBr/TiO2 Visible Light Photocatalyst for Destruction of Azodyes and Bacteria. Journal of Physical Chemistry B, 110, 4066-4072.
http://dx.doi.org/10.1021/jp0564400
[25] Unfried, K., Albrecht, C., Klotz, L.O., Von Mikecz, A., Grether-Beck, S. and Schins, R.P.F. (2007) Cellular Responses to Nanoparticles: Target Structures and Mechanisms. Nanotoxicology, 1, 52-71.
http://dx.doi.org/10.1080/00222930701314932
[26] Verma, A., Uzun, O., Hu, Y., Hu, Y., Han, H.S., Watson, N., Chen, S., Irvine, D.J. and Stellacci, F. (2008) Surface- Structure-Regulated Cell-Membrane Penetration by Monolayer-Protected Nanoparticles. Nature Materials, 7, 588-595. >
http://dx.doi.org/10.1038/nmat2202
[27] Nel, A.E., Mdler, L., Velegol, D., Xia, T., Hoek, E.M.V., Somasundaran, P., Klaessig, F., Castranova, V. and Thompson, M. (2009) Understanding Biophysicochemical Interactions at the Nano-Bio Interface. Nature Materials, 8, 543-557.
http://dx.doi.org/10.1038/nmat2442
[28] Verma, A. and Stellacci, F. (2010) Effect of Surface Properties on Nanoparticle Cell Interactions. Small, 6, 12-21.
http://dx.doi.org/10.1002/smll.200901158
[29] Chance, B., Sies, H. and Boveris, A. (1979) Hydroperoxide Metabolism in Mammalian Organs. Physiological Reviews, 59, 527-605.
[30] Goodhew, P.J. and Humphrey, F.J. (1988) Electron Microscopy and Analysis. Taylor and Francis Inc., Philadelphia.
[31] Batdorj, B., Trinetta, V., Dalgalarrondo, M., Prevost, H., Dousset, X., Ivanova, I., Haertle, T. and Chobert, J.M. (2007) Isolation, Taxonomic Identification and Hydrogen Peroxide Production by Lactobacillus delbrueckii subsp. Lactis T31, Isolated from Mongolian Yoghurt: Inhibitory Activity on Food-Borne Pathogens. Journal of Applied Microbiology, 103, 584-593.
http://dx.doi.org/10.1111/j.1365-2672.2007.03279.x
[32] Parvez, S., Venkataraman, C. and Mukherji, S. (2006) A Review on Advantages of Implementing Luminescence Inhibition Test (Vibrio fischeri) for Acute Toxicity Prediction of Chemicals. Environment International, 32, 265-268.
http://dx.doi.org/10.1016/j.envint.2005.08.022
[33] Kahru, A., Dubourguier, H.C., Blinova, I., Ivask, A. and Kasemets, K. (2008) Biotests and Biosensors for Ecotoxicology of Metal Oxide Nanoparticles: A Minireview. Sensors, 8, 5153-5170.
http://dx.doi.org/10.3390/s8085153
[34] Binaeian, E., Rashidi, A.M. and Attar, H. (2012) Toxicity Study of Two Different Synthesized Silver Nanoparticles on Bacteria Vibrio fischeri. World Academy of Science, Engineering and Technology, 67, 1219-1225.
[35] Garcia, A., Espinosa, R., Delgado, L., Casals, E., Gonzalez, E., Puntes, V., Barata, C., Font, X. and Sanchez, A. (2011) Acute Toxicity of Cerium Oxide and Iron Oxide Nanoparticles Using Standardized Tests. Desalination, 269, 136-141.
http://dx.doi.org/10.1016/j.desal.2010.10.052
[36] Lopes, I., Ribeiro, R., Antunes, F.E., Rocha-Santos, T.A., Rasteiro, M.G., Soares, A.M., Gonalves, F. and Pereira, R. (2012) Toxicity and Genotoxicity of Organic and Inorganic Nanoparticles to the Bacteria Vibrio fischeri and Salmonella typhimurium. Ecotoxicology, 21, 637-648.
http://dx.doi.org/10.1007/s10646-011-0808-9
[37] Straganz, G.D., Glieder, A., Brecker, L., Ribbons, D.W. and Steiner, W. (2003) Acetylacetone-Cleaving Enzyme Dke1: A Novel C-C-Bond-Cleaving Enzyme from Acinetobacter johnsonii. Biochemistry Journal, 369, 573-581.
http://dx.doi.org/10.1042/BJ20021047
[38] Massard, C., Bonnet, M., Veisseire, P., Sibaud, Y., Caudron, E. and Awitor, K.O. (2013) Photokilling of Escherichia coli Using Hybrid Titania Nanoparticles Suspended in an Aqueous Liquid. Journal of Biomaterials and Nanobiotechnology, 4,137-144.
http://dx.doi.org/10.4236/jbnb.2013.42019
[39] Wang, J., Li, C., Zhuang, H. and Zhang, J. (2013) Photocatalytic Degradation of Methylene Blue and Inactivation of Gram-Negative Bacteria by TiO2 Nanoparticles in Aqueous Suspension. Food Control, 34, 372-377.
http://dx.doi.org/10.1016/j.foodcont.2013.04.046
[40] Marugán, J., van Grieken, R., Sordo, C. and Cruz, C. (2008) Kinetics of the Photocatalytic Disinfection of Escherichia coli Suspensions. Applied Catalysis B: Environmental, 82, 27-36.
http://dx.doi.org/10.1016/j.apcatb.2008.01.002
[41] Nair, S., Sasidharan, A., Rani, V.V.D., Menon, D., Nair, S. and Manzoor, K. (2009) Role of Size Scale of ZnO Nanoparticles and Microparticles on Toxicity toward Bacteria and Osteoblast Cancer Cells. Journal of Materials Science: Materials in Medicine, 20, 235-241.
http://dx.doi.org/10.1007/s10856-008-3548-5
[42] Tamboli, D.P. and Lee, D.S. (2013) Mechanistic Antimicrobial Approach of Extracellularly Synthesized Silver Nanoparticles against Gram Positive and Gram Negative Bacteria. Journal of Hazardous Materials, 260, 878-884.
http://dx.doi.org/10.1016/j.jhazmat.2013.06.003
[43] Shrivastava, S., Bera, T., Roy, A., Singh, G., Ramachandrarao, P. and Dash, D. (2007) Characterization of Enhanced Antibacterial Effects of Novel Silver Nanoparticles. Nanotechnology, 18, 103-112.
[44] Premanathan, M., Karthikeyan, K., Jeyasubramanian, K. and Manivannan, G. (2011) Selective Toxicity of ZnO Nanoparticles toward Gram-Positive Bacteria and Cancer Cells by Apoptosis through Lipid Peroxidation. Nanomedicine: Nanotechnology, Biology and Medicine, 7, 184-192.
http://dx.doi.org/10.1016/j.nano.2010.10.001
[45] Yadav, H.M., Otari, S.V., Koli, V.B., Mali, S.S., Hong, C.K., Pawar, S.H. and Delekar, S.D. (2014) Preparation and Characterization of Copper-Doped Anatase TiO2 Nanoparticles with Visible Light Photocatalytic Antibacterial Activity. Journal of Photochemistry and Photobiology A: Chemistry, 280, 32-38.
http://dx.doi.org/10.1016/j.jphotochem.2014.02.006
[46] Yadav, H.M., Otari, S.V., Bohara, R.A., Mali, S.S., Pawar, S.H. and Delekar, S.D. (2014) Synthesis and Visible Light Photocatalytic Antibacterial Activity of Nickel-Doped Nanoparticles against Gram-Positive and Gram-Negative Bacteria. Journal of Photochemistry and Photobiology A: Chemistry, 294, 130-136.
http://dx.doi.org/10.1016/j.jphotochem.2014.07.024
[47] van Grieken, R., Marugán, J., Pablos, C., Furones, L. and López, A. (2010) Comparison between the Photocatalytic Inactivation of Gram-Positive E. faecalis and Gram Negative E. coli Faecal Contamination Indicator Microorganisms. Applied Catalysis B: Environmental, 100, 212-220.
http://dx.doi.org/10.1016/j.apcatb.2010.07.034
[48] Rijnaarts, H.H.M., Norde, W., Lyklema, J. and Zehnder, A. (1995) The Isoelectric Point of Bacteria as an Indicator for the Presence of Cell Surface Polymers That Inhibit Adhesion. Colloid Surface B, 4, 191-197.
http://dx.doi.org/10.1016/0927-7765(94)01164-Z
[49] Juang, D.F., Yang, P.C., Lee, C.H., Hsueh, S.C. and Kuo, T.H. (2011) Electrogenic Capabilities of Gram Negative and Gram Positive Bacteria in Microbial Fuel Cell Combined with Biological Wastewater Treatment. International Journal of Environmental Science and Technology, 8, 781-792.
http://dx.doi.org/10.1007/BF03326261
[50] Klaine, S.J., Alvarez, P.J.J., Batley, G.E., Fernandes, T.F., Hande, R.D., Lyon, D.Y., Mahendra, S., McLaughlin, M.J. and Lead, J.R. (2008) Nanomaterials in the Environment: Behavior, Fate, Bioavailability, and Effects. Environmental Toxicology and Chemistry, 27, 1825-1851.
http://dx.doi.org/10.1897/08-090.1
[51] Pelletier, D.A., Suresh, A.K., Holton, G.A., McKeown, C.K., Wang, W., Gu, B., Mortensen, N.P., Allison, D.P., Joy, D.C., Allison, M.R., Brown, S.D., Phelps, T.J. and Doktycz, M.J. (2010) Effects of Engineered Cerium Oxide Nanoparticles on Bacterial Growth and Viability. Applied and Environmental Microbiology, 76, 7981-7989.
http://dx.doi.org/10.1128/AEM.00650-10
[52] Bartoli, M. and Dusseau, J.Y. (1995) Oxydants. In: Fleurette, J., Fresney, J. and Reverdy, M.E., Eds., Antiseptie et désinfection, Editions Eska, Paris, 305-314.
[53] Hamouda, T. and Baker Jr., J.R. (2000) Antimicrobial Mechanism of Action of Surfactant Lipid Preparations in Enteric Gram-Negative Bacilli. Journal of Applied Microbiology, 89, 397-403.
http://dx.doi.org/10.1046/j.1365-2672.2000.01127.x
[54] Sondi, I. and Salopek-Sondi, B. (2004) Silver Nanoparticles as Antimicrobial Agent: A Case Study on E. coli as a Model for Gram-Negative Bacteria. Journal of Colloid and Interface Science, 275, 177-182.
http://dx.doi.org/10.1016/j.jcis.2004.02.012
[55] Fujishima, A. and Honda, K. (1972) Electrochemical Photocatalysis of Water at a Semiconductor Electrode. Nature, 238, 37-38.
http://dx.doi.org/10.1038/238037a0
[56] Carp, O., Huisman, C.L. and Reller, A. (2004) Photoinduced Reactivity of Titanium Dioxide. Progress in Solid State Chemistry, 32, 33-177.
http://dx.doi.org/10.1016/j.progsolidstchem.2004.08.001
[57] Liu, H. and Yang, T.C. (2003) Photocatalytic Inactivation of Escherichia coli and Lactobacillus helveticus by ZnO and TiO2 Activated with Ultraviolet Light. Process Biochemistry, 39, 475-481.
http://dx.doi.org/10.1016/S0032-9592(03)00084-0
[58] Cushman, J.C. and Bohnert, H.J. (2000) Genomic Approaches to Plant Stress Tolerance. Current Opinion in Plant Biology, 3, 117-124.
http://dx.doi.org/10.1016/S1369-5266(99)00052-7
[59] Lovric, J., Cho, S.J., Winnik, F.M. and Maysinger, D. (2005) Unmodified Cadmium Telluride Quantum Dots Induce Reactive Oxygen Species Formation Leading to Multiple Organelle Damage and Cell Death. Chemistry and Biology, 12, 1227-1234.
http://dx.doi.org/10.1016/j.chembiol.2005.09.008
[60] Long, T.C., Saleh, N., Tilton, R.D., Lowry, G.V. and Veronesi, B. (2006) Titanium Dioxide (P25) Produces Reactive Oxygen Species in Immortalized Brain Microglia (BV2): Implications for Nanoparticle Neurotoxicity. Environmental Science and Technology, 40, 4346-4352.
http://dx.doi.org/10.1021/es060589n
[61] Kumar, A., Pandey, A.K., Singh, S.S., Shanker, R. and Dhawan, A. (2011) Engineered ZnO and TiO2 Nanoparticles Induce Oxidative Stress and DNA Damage Leading to Reduced Viability of Escherichia coli. Free Radical Biology and Medicine, 51, 1872-1881.
http://dx.doi.org/10.1016/j.freeradbiomed.2011.08.025

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