Dissolved organic matter and aluminum oxide nanoparticles synergistically cause cellular responses in freshwater microalgae

References

• Handy, R. D.; von der Kammer, F.; Lead, J. R.; Hassellöv, M.; Owen, R.; Crane, M. The Ecotoxicology and Chemistry of Manufactured Nanoparticles. Ecotoxicology 2008, 17(4), 287–314. doi:10.1007/s10646-008-0199-8.
   PubMed Web of Science ®Google Scholar
• Nowack, B.; Bucheli, T. D. Occurrence, Behavior and Effects of Nanoparticles in the Environment. Environ. Pollut. 2007, 150(1), 5–22. doi:10.1016/j.envpol.2007.06.006.
   PubMed Web of Science ®Google Scholar
• Baun, A.; Hartmann, N. B.; Grieger, K.; Kusk, K. O. Ecotoxicity of Engineered Nanoparticles to Aquatic Invertebrates: A Brief Review and Recommendations for Future Toxicity Testing. Ecotoxicology 2008, 17(5), 387–395. doi:10.1007/s10646-008-0208-y.
   PubMed Web of Science ®Google Scholar
• Skjolding, L. M.; Sørensen, S. N.; Hartmann, N. B.; Hjorth, R.; Hansen, S. F.; Baun, A. Aquatic Ecotoxicity Testing of Nanoparticles—The Quest to Disclose Nanoparticle Effects. Angew. Chem. Int. Ed. 2016, 55(49), 15224–15239. doi:10.1002/anie.201604964.
   PubMed Web of Science ®Google Scholar
• Zhao, Y.; Sugiyama, S.; Miller, T.; Miao, X. Nanoceramics for Blood-Borne Virus Removal. Expert Rev. Med. Devices. 2008, 5(3), 395–405. doi:10.1586/17434440.5.3.395.
   PubMed Web of Science ®Google Scholar
• Miao, X.; Gorring, N. M. Nanoceramics and Nanoceramic Composites for Biomedical Applications. In Tseng, T.-Y., Nalwa, H. S. (Eds.) Handbook of Nanoceramics and Their Based Nanodevices. American Scientific Publishers: Stevenson Ranch, Calif., 2009.
   Google Scholar
• Pakrashi, S.; Kumar, D.; Iswarya, V.; Bhuvaneshwari, M.; Chandrasekaran, N.; Mukherjee, A. A Comparative Ecotoxicity Analysis of α- and γ-Phase Aluminium Oxide Nanoparticles Towards a Freshwater Bacterial Isolate Bacillus Licheniformis. Bioprocess Biosyst. Eng. 2014, 37(12), 2415–2423. doi:10.1007/s00449-014-1218-1.
   PubMed Web of Science ®Google Scholar
• Aiken, G.; Hsu-Kim, H.; Ryan, J.; Alvarez, P. Nanoscale Metal-Organic Matter Interactions. Environ. Sci. Technol. 2011, 45(8), 3194–3195. doi:10.1021/es2007148.
   PubMed Web of Science ®Google Scholar
• Grillo, R.; Rosa, A. H.; Fraceto, L. F. Engineered Nanoparticles and Organic Matter: A Review of the State-of-the-art. Chemosphere 2015, 119, 608–619. doi:10.1016/j.chemosphere.2014.07.049.
   PubMed Web of Science ®Google Scholar
• Wang, Z.; Quik, J. T.; Song, L.; Van Den Brandhof, E. J.; Wouterse, M.; Peijnenburg, W. J. Humic Substances Alleviate the Aquatic Toxicity of Polyvinylpyrrolidone-Coated Silver Nanoparticles to Organisms of Different Trophic Levels. Environ. Toxicol. Chem. 2015, 34(6), 1239–1245. doi:10.1002/etc.2936.
   PubMed Web of Science ®Google Scholar
• Xie, B.; Xu, Z.; Guo, W.; Li, Q. Impact of Natural Organic Matter on the Physicochemical Properties of Aqueous C60 Nanoparticles. Environ. Sci. Technol. 2008, 42(8), 2853–2859. doi:10.1021/es702231g.
   PubMed Web of Science ®Google Scholar
• Quik, J. T.; Lynch, I.; Van Hoecke, K.; Miermans, C. J.; De Schamphelaere, K. A.; Janssen, C. R.; Dawson, K. A.; Stuart, M. A.; Van De Meent, D. Effect of Natural Organic Matter on Cerium Dioxide Nanoparticles Settling in Model Fresh Water. Chemosphere 2010, 81, 711–715. doi:10.1016/j.chemosphere.2010.07.062.
   PubMed Web of Science ®Google Scholar
• Wang, Z.; Chen, J.; Sun, Q.; Peijnenburg, W. J. C60-DOM Interactions and Effects on C60 Apparent Solubility: A Molecular Mechanics and Density Functional Theory Study. Environ. Int. 2011, 37(6), 1078–1082. doi:10.1016/j.envint.2011.02.016.
   PubMed Web of Science ®Google Scholar
• Wang, Z.; Quik, J. T.; Song, L.; Wouterse, M.; Peijnenburg, W. J. Dissipative Particle Dynamic Simulation and Experimental Assessment of the Impacts of Humic Substances on Aqueous Aggregation and Dispersion of Engineered Nanoparticles. Environ. Toxicol. Chem. 2017, in press. doi:10.1002/etc.4059.
   Web of Science ®Google Scholar
• Cerrillo, C.; Barandika, G.; Igartua, A.; Areitioaurtena, O.; Mendoza, G. Towards the Standardization of Nanoecotoxicity Testing: Natural Organic Matter ‘Camouflages’ the Adverse Effects of TiO2 and CeO2 Nanoparticles on Green Microalgae. Sci. Total Environ. 2016, 543, 95–104. doi:10.1016/j.scitotenv.2015.10.137.
   PubMed Web of Science ®Google Scholar
• Wang, Z.; Li, J.; Zhao, J.; Xing, B. Toxicity and Internalization of CuO Nanoparticles to Prokaryotic Alga Microcystis Aeruginosa as Affected by Dissolved Organic Matter. Environ. Sci. Technol. 2011, 45(14), 6032–6040. doi:10.1021/es2010573.
   PubMed Web of Science ®Google Scholar
• Van Hoecke, K.; De Schamphelaere, K. A.; Ramirez-Garcia, S.; Van der Meeren, P.; Smagghe, G.; Janssen, C. R. Influence of Alumina Coating on Characteristics and Effects of SiO2 Nanoparticles in Algal Growth Inhibition Assays at Various pH and Organic Matter Contents. Environ. Int. 2011, 37(6), 1118–1125. doi:10.1016/j.envint.2011.02.009.
   PubMed Web of Science ®Google Scholar
• Fang, T.; Yu, L. P.; Zhang, W. C.; Bao, S. P. Effects of Humic Acid and Ionic Strength on TiO₂ Nanoparticles Sublethal Toxicity to Zebrafish. Ecotoxicology 2015, 24(10), 2054–2066. doi:10.1007/s10646-015-1541-6.
   PubMed Web of Science ®Google Scholar
• He, X.; McAlliser, D.; Aker, W. G.; Hwang, H. M. Assessing the Effect of Different Natural Dissolved Organic Matters on the Cytotoxicity of Titanium Dioxide Nanoparticles with Bacteria. J. Environ. Sci. (China) 2016, 48, 230–236. doi:10.1016/j.jes.2016.02.012.
   PubMedGoogle Scholar
• Seitz, F.; Rosenfeldt, R. R.; Müller, M.; Lüderwald, S.; Schulz, R.; Bundschuh, M. Quantity and Quality of Natural Organic Matter Influence the Ecotoxicity of Titanium Dioxide Nanoparticles. Nanotoxicology 2016, 10(10), 1415–1421. doi:10.1080/17435390.2016.1222458.
   PubMed Web of Science ®Google Scholar
• Yang, S. P.; Bar-Ilan, O.; Peterson, R. E.; Heideman, W.; Hamers, R. J.; Pedersen, J. A. Influence of Humic Acid on Titanium Dioxide Nanoparticle Toxicity to Developing Zebrafish. Environ. Sci. Technol. 2013, 47(9), 4718–4725. doi:10.1021/es3047334.
   PubMed Web of Science ®Google Scholar
• Tang, Y.; Li, S.; Lu, Y.; Li, Q.; Yu, S. The Influence of Humic Acid on the Toxicity of Nano-ZnO and Zn2+ to the Anabaena sp. Environ. Toxicol. 2014, 30(8), 895–903. doi:10.1002/tox.21964.
   PubMed Web of Science ®Google Scholar
• Kennedy, A. J.; Hull, M. S.; Bednar, A. J.; Goss, J. D.; Gunter, J. C.; Bouldin, J. L.; Vikesland, P. J.; Steevens, J. A. Fractionating Nanosilver: Importance for Determining Toxicity to Aquatic Test Organisms. Environ. Sci. Technol. 2010, 44(24), 9571–9577. doi:10.1021/es1025382.
   PubMed Web of Science ®Google Scholar
• Pakrashi, S.; Dalai, S.; Sabat, D.; Singh, S.; Chandrasekaran, N.; Mukherjee, A. Cytotoxicity of Al2O3 Nanoparticles at Low Exposure Levels to a Freshwater Bacterial Isolate. Chem. Res. Toxicol. 2011, 24(11), 1899–1904. doi:10.1021/tx200244g.
   PubMed Web of Science ®Google Scholar
• Chen, P.; Powell, B. A.; Mortimer, M.; Ke, P. C. Adaptive Interactions between Zinc Oxide Nanoparticles and Chlorella sp. Environ. Sci. Technol. 2012, 46(21), 12178–12185. doi:10.1021/es303303g.
   PubMed Web of Science ®Google Scholar
• OECD Guidelines for the testing of chemicals. Section 2: Effects on Biotic Systems. Test No. 201: Freshwater Alga and Cyanobacteria, growth inhibition test. Organization for Economic Co-operation and Development. Paris, France, 2011. Available at http://www.oecd.org.
   Google Scholar
• Ye, N.; Wang, Z.; Fang, H.; Wang, S.; Zhang, F. Combined Ecotoxicity of Binary Zinc Oxide and Copper Oxide Nanoparticles to Scenedesmus Obliquus. J. Environ. Sci. Health., Part A, Tox. Hazard. Subst. Environ. Eng. 2017, 52(6), 555–560. doi:10.1080/10934529.2017.1284434.
   PubMed Web of Science ®Google Scholar
• Li, Q.; Xie, B.; Hwang, Y. S.; Xu, Y. Kinetics of C60 Fullerene Dispersion in Water Enhanced by Natural Organic Matter and Sunlight. Environ. Sci. Technol. 2009, 43(10), 3574–3579. doi:10.1021/es803603x.
   PubMed Web of Science ®Google Scholar
• Johnson, R. L.; Johnson, G. O.; Nurmi, J. T.; Tratnyek, P. G. Natural Organic Matter Enhanced Mobility of Nano Zerovalent Iron. Environ. Sci. Technol. 2009, 43(14), 5455–5460. doi:10.1021/es900474f.
   PubMed Web of Science ®Google Scholar
• Wang, Z.; Chen, J.; Li, X.; Shao, J.; Peijnenburg, W. J. Aquatic Toxicity of Nanosilver Colloids to Different Trophic Organisms: Contributions of Particles and Free Silver Ion. Environ. Toxicol. Chem. 2012, 31(10), 2408–2413. doi:10.1002/etc.1964.
   PubMed Web of Science ®Google Scholar
• Hu, C.; Wang, Q.; Zhao, H.; Wang, L.; Guo, S.; Li, X. Ecotoxicological Effects of Graphene Oxide on the Protozoan Euglena Gracilis. Chemosphere 2015, 128, 184–190. doi:10.1016/j.chemosphere.2015.01.040.
   PubMed Web of Science ®Google Scholar
• Wang, S.; Wang, Z.; Chen, M. D.; Fang, H.; Wang, D. Co-Exposure of Freshwater Microalgae to Tetrabromobisphenol A and Sulfadiazine: Oxidative Stress Biomarker Responses and Joint Toxicity Prediction. Bull. Environ. Contam. Toxicol. 2017, 99, 438–444. doi:10.1007/s00128-017-2153-z.
   PubMed Web of Science ®Google Scholar
• Liu, W.; Chen, S.; Quan, X.; Jin, Y. H. Toxic Effect of Serial Perfluorosulfonic and Perfluorocarboxylic Acids on the Membrane System of a Freshwater Alga Measured by Flow Cytometry. Environ. Toxicol. Chem. 2008, 27(7), 1597–1604. doi:10.1897/07-459.1.
   PubMed Web of Science ®Google Scholar
• Vigneault, B.; Percot, A.; Lafleur, M.; Campbell, P. G. Permeability Changes in Model and Phytoplankton Membranes in the Presence of Aquatic Humic Substances. Environ. Sci. Technol. 2000, 34(18), 3907–3913. doi:10.1021/es001087r.
   Web of Science ®Google Scholar
• Sal'nikov, D. S.; Pogorelova, A. S.; Makarov, S. V.; Vashurina, I. Y. Silver Ion Reduction with Peat Fulvic Acids. Russ. J. Appl. Chem. 2009, 82(4), 545–548. doi:10.1134/S107042720904003X.
   Web of Science ®Google Scholar
• Steinberg, C. E.; Meinelt, T.; Timofeyev, M. A.; Bittner, M.; Menzel, R. Humic Substances. Part 2: Interactions with Organisms. Environ. Sci. Pollut. Res. Int. 2008, 15(2), 128–135. doi:10.1065/espr2007.07.434.
   PubMedGoogle Scholar
• Bährs, H.; Steinberg, C. E. Impact of Two Different Humic Substances on Selected Coccal Green Algae and Cyanobacteria–Changes in Growth and Photosynthetic Performance. Environ. Sci. Pollut. Res. Int. 2012, 19(2), 335–346. doi:10.1007/s11356-011-0564-7.
   PubMed Web of Science ®Google Scholar
• Weckx, J. E.; Clijsters, H. M. Oxidative Damage and Defense Mechanisms in Primary Leaves of Phaseolus Vulgaris as a Result of Root Assimilation of Toxic Amounts of Copper. Physiol. Plant. 1996, 96, 506–512. doi:10.1111/j.1399-3054.1996.tb00465.x.
   Web of Science ®Google Scholar
• Foyer, C. H.; Shigeoka, S. Understanding Oxidative Stress and Antioxidant Functions to Enhance Photosynthesis. Plant Physiol. 2011, 155(1), 93–100. doi:10.1104/pp.110.166181.
   PubMed Web of Science ®Google Scholar
• Li, Y.; Niu, J.; Shang, E.; Crittenden, J. C. Influence of Dissolved Organic Matter on Photogenerated Reactive Oxygen Species and Metal-Oxide Nanoparticle Toxicity. Water Res. 2016, 98, 9–18. doi:10.1016/j.watres.2016.03.050.
   PubMed Web of Science ®Google Scholar
• Li, M.; Hu, C.; Zhu, Q.; Chen, L.; Kong, Z.; Liu, Z. Copper and Zinc Induction of Lipid Peroxidation and Effects on Antioxidant Enzyme Activities in the Microalga Pavlova Viridis (Prymnesiophyceae). Chemosphere 2006, 62, 565–572. doi:10.1016/j.chemosphere.2005.06.029.
   PubMed Web of Science ®Google Scholar
• dos Santos, G. A.; Abreu e Lima, R. S.; Pestana, C. R.; Lima, A. S.; Scheucher, P. S.; Thome´, C. H.; Gimenes-Teixeira, H. L.; Santana-Lemos, B. A.; Lucena-Araujo, A. R.; Rodrigues, F. P., et al. (+)α-Tocopheryl Succinate Inhibits the Mitochondrial Respiratory Chain Complex I and is as Effective as Arsenic Trioxide or ATRA Against Acute Promyelocytic Leukemia in Vivo. Leukemia 2012, 26(3), 451–460. doi:10.1038/leu.2011.216.
   PubMed Web of Science ®Google Scholar