Characterization of the nano–bio interaction between metallic oxide nanomaterials and freshwater microalgae using flow cytometry

References

• Abo-Shady, A. M., Y. A. Mohamed, and T. Lasheen. 1993. “Chemical Composition of the Cell Wall in Some Green Algae Species.” Biologia Plantarum 35 (4): 629–632. doi:10.1007/BF02928041.
   Web of Science ®Google Scholar
• Adeleye, A. S., and A. A. Keller. 2016. “Interactions Between Algal Extracellular Polymeric Substances and Commercial TiO2 Nanoparticles in Aqueous Media.” Environmental Science & Technology 50 (22): 12258–12265. doi:10.1021/acs.est.6b03684.
   PubMed Web of Science ®Google Scholar
• Alberts, B., A. Johnson, J. Lewis, M. Raff, K. Roberts, and P. Walter. 2002. “The Plant Cell Wall.” In Molecular Biology of the Cell. 4th ed. New York, NY: Garland Science.
   Google Scholar
• Angel, B. M., P. Vallotton, and S. C. Apte. 2015. “On the Mechanism of Nanoparticulate CeO2 Toxicity to Freshwater Algae.” Aquatic Toxicology (Amsterdam, Netherlands) 168: 90–97. doi:10.1016/j.aquatox.2015.09.015.
   PubMed Web of Science ®Google Scholar
• Arts, J. H. E., M.-A. Irfan, A. M. Keene, R. Kreiling, D. Lyon, M. Maier, K. Michel, et al. 2016. “Case Studies Putting the Decision-Making Framework for the Grouping and Testing of Nanomaterials (DF4nanoGrouping) into Practice.” Regulatory Toxicology and Pharmacology : RTP 76: 234–261. doi:10.1016/j.yrtph.2015.11.020.
   PubMed Web of Science ®Google Scholar
• Aruoja, V., H.-C. Dubourguier, K. Kasemets, and A. Kahru. 2009. “Toxicity of Nanoparticles of CuO, ZnO and TiO2 to Microalgae Pseudokirchneriella subcapitata.” The Science of the Total Environment 407 (4): 1461–1468. doi:10.1016/j.scitotenv.2008.10.053.
   PubMed Web of Science ®Google Scholar
• Blasco, J., and I. Corsi. 2019. Ecotoxicology of Nanoparticles in Aquatic Systems. Boca Raton, FL: CRC Press.
   Google Scholar
• Booth, A., and A. J. Keld. 2015. NANoREG D4.12 SOP Probe Sonicator Calibration for ecotoxicological testing.
   Google Scholar
• Booth, A., T. Størseth, D. Altin, A. Fornara, A. Ahniyaz, H. Jungnickel, P. Laux, A. Luch, and L. Sørensen. 2015. “Freshwater Dispersion Stability of PAA-Stabilised Cerium Oxide Nanoparticles and Toxicity Towards Pseudokirchneriella subcapitata.” The Science of the Total Environment 505: 596–605. doi:10.1016/j.scitotenv.2014.10.010.
   PubMed Web of Science ®Google Scholar
• Brown, M. D., and C. T. Wittwer. 2000. “Flow Cytometry: Principles and Clinical Applications in Hematology.” Clinical Chemistry 46 (8): 1221–1229. doi:10.1093/clinchem/46.8.1221.
   PubMedGoogle Scholar
• Campos, B., C. Rivetti, P. Rosenkranz, J. M. Navas, and C. Barata. 2013. “Effects of Nanoparticles of TiO2 on Food Depletion and Life-History Responses of Daphnia magna.” Aquatic Toxicology (Amsterdam, Netherlands) 130–131: 174–183. doi:10.1016/j.aquatox.2013.01.005.
   PubMed Web of Science ®Google Scholar
• Cao, Z., S. N. Tsai, and Y. Y. Zuo. 2019. “An Optical Method for Quantitatively Determining the Surface Free Energy of Micro- and Nanoparticles.” Analytical Chemistry 91 (20): 12819–12826. doi:10.1021/acs.analchem.9b02507.
   PubMed Web of Science ®Google Scholar
• Dabrunz, A., L. Duester, C. Prasse, F. Seitz, R. Rosenfeldt, C. Schilde, G. E. Schaumann, and R. Schulz. 2011. “Biological Surface Coating and Molting Inhibition as Mechanisms of TiO2 Nanoparticle Toxicity in Daphnia magna.” Plos One 6 (5): e20112. doi:10.1371/journal.pone.0020112.
   PubMed Web of Science ®Google Scholar
• Domozych, D. S., M. Ciancia, J. U. Fangel, M. D. Mikkelsen, P. Ulvskov, and W. G. T. Willats. 2012. “The Cell Walls of Green Algae: A Journey Through Evolution and Diversity.” Front Plant Sci 3: 82. doi:10.3389/fpls.2012.00082.
   PubMed Web of Science ®Google Scholar
• European Commission Joint Research Centre. 2012. NM-Series of Representative Manufactured Nanomaterials: Zinc Oxide NM-110, NM-111, NM-112, NM-113 Characterisation and Test Item Preparation.
   Google Scholar
• European Commission Joint Research Centre. 2013. Synthetic Amorphous Silicon Dioxide (NM-200, NM-201, NM-202, NM-203, NM-204): Characterisation and Physico-Chemical Properties: JRC Repository: NM-Series of Representative Manufactured Nanomaterials.
   Google Scholar
• European Commission Joint Research Centre. 2014. Titanium Dioxide, NM-100, NM-101, NM-102, NM-103, NM-104, NM-105: Characterisation and Physico-Chemical Properties.
   Google Scholar
• Gao, X., K. Zhou, L. Zhang, K. Yang, and D. Lin. 2018. “Distinct Effects of Soluble and Bound Exopolymeric Substances on Algal Bioaccumulation and Toxicity of Anatase and Rutile TiO2 Nanoparticles.” Environmental Science: Nano 5 (3): 720–729. doi:10.1039/C7EN01176H.
   Web of Science ®Google Scholar
• Godwin, H., C. Nameth, D. Avery, L. L. Bergeson, D. Bernard, E. Beryt, W. Boyes, et al. 2015. “Nanomaterial Categorization for Assessing Risk Potential to Facilitate Regulatory Decision-Making.” ACS Nano 9 (4): 3409–3417. doi:10.1021/acsnano.5b00941.
   PubMed Web of Science ®Google Scholar
• Gorokhova, E., K. Ek, and S. Reichelt. 2020. “Algal Growth at Environmentally Relevant Concentrations of Suspended Solids: Implications for Microplastic Hazard Assessment (Preprint).” Ecology doi:10.1101/2020.04.11.036889.
   Google Scholar
• Hadjoudja, S., V. Deluchat, and M. Baudu. 2010. “Cell Surface Characterisation of Microcystis aeruginosa and Chlorella vulgaris.” Journal of Colloid and Interface Science 342 (2): 293–299. doi:10.1016/j.jcis.2009.10.078.
   PubMed Web of Science ®Google Scholar
• Hansen, S. F., S. N. Sørensen, L. M. Skjolding, N. B. Hartmann, and A. Baun. 2017. “Revising REACH Guidance on Information Requirements and Chemical Safety Assessment for Engineered Nanomaterials for Aquatic Ecotoxicity Endpoints: Recommendations from the EnvNano Project.” Environmental Sciences Europe 29 (1): 14. doi:10.1186/s12302-017-0111-3.
   PubMedGoogle Scholar
• Hartmann, N. B., C. Engelbrekt, J. Zhang, J. Ulstrup, K. O. Kusk, and A. Baun. 2013. “The Challenges of Testing Metal and Metal Oxide Nanoparticles in Algal Bioassays: Titanium Dioxide and Gold Nanoparticles as Case studies.” Nanotoxicology 7 (6): 1082–1094. doi:10.3109/17435390.2012.710657.
   PubMed Web of Science ®Google Scholar
• Hartmann, N. B., F. Von der Kammer, T. Hofmann, M. Baalousha, S. Ottofuelling, and A. Baun. 2010. “Algal Testing of Titanium Dioxide Nanoparticles–Testing Considerations, Inhibitory Effects and Modification of Cadmium Bioavailability.” Toxicology 269 (2–3): 190–197. doi:10.1016/j.tox.2009.08.008.
   PubMed Web of Science ®Google Scholar
• He, X., W. G. Aker, P. P. Fu, and H.-M. Hwang. 2015. “Toxicity of Engineered Metal Oxide Nanomaterials Mediated by Nano–Bio–Eco–Interactions: A Review and Perspective.” Environmental Science: Nano 2 (6): 564–582. doi:10.1039/C5EN00094G.
   Web of Science ®Google Scholar
• Hund-Rinke, K., K. Schlich, D. Kühnel, B. Hellack, H. Kaminski, and C. Nickel. 2018. “Grouping Concept for Metal and Metal Oxide Nanomaterials with Regard to Their Ecotoxicological Effects on Algae, Daphnids and Fish Embryos.” NanoImpact 9: 52–60. doi:10.1016/j.impact.2017.10.003.
   Web of Science ®Google Scholar
• Joonas, E., V. Aruoja, K. Olli, and A. Kahru. 2019. “Environmental Safety Data on CuO and TiO2 Nanoparticles for Multiple Algal Species in Natural Water: Filling the Data Gaps for Risk Assessment.” The Science of the Total Environment 647: 973–980. doi:10.1016/j.scitotenv.2018.07.446.
   PubMed Web of Science ®Google Scholar
• Ju-Nam, Y., and J. R. Lead. 2008. “Manufactured Nanoparticles: An Overview of Their Chemistry, Interactions and Potential Environmental Implications.” The Science of the Total Environment 400 (1–3): 396–414. doi:10.1016/j.scitotenv.2008.06.042.
   PubMed Web of Science ®Google Scholar
• Keld, A. J. 2014. The NANOGENOTOX dispersion protocol for NANoREG.
   Google Scholar
• Keller, A. A., H. Wang, D. Zhou, H. S. Lenihan, G. Cherr, B. J. Cardinale, R. Miller, and Z. Ji. 2010. “Stability and Aggregation of Metal Oxide Nanoparticles in Natural Aqueous Matrices.” Environmental Science & Technology 44 (6): 1962–1967.
   PubMed Web of Science ®Google Scholar
• Kühnel, D., C. Nickel, B. Hellack, E. van der Zalm, C. Kussatz, M. Herrchen, B. Meisterjahn, and K. Hund-Rinke. 2019. “Closing Gaps for Environmental Risk Screening of Engineered Nanomaterials.” NanoImpact 15: 100173. doi:10.1016/j.impact.2019.100173.
   Web of Science ®Google Scholar
• Kumar, A., A. K. Pandey, S. Singh, R. Shanker, and A. Dhawan. 2011. “A Flow Cytometric Method to Assess Nanoparticle Uptake in Bacteria.” Cytometry. Part A : The Journal of the International Society for Analytical Cytology 79 (9): 707–712. doi:10.1002/cyto.a.21085.
   PubMedGoogle Scholar
• Li, Y., N.-H. Lee, E. G. Lee, J. S. Song, and S.-J. Kim. 2004. “The Characterization and Photocatalytic Properties of Mesoporous Rutile TiO2 Powder Synthesized Through Self-Assembly of Nano Crystals.” Chemical Physics Letters 389 (1–3): 124–128. doi:10.1016/j.cplett.2004.03.081.
   Web of Science ®Google Scholar
• Ma, S., and D. Lin. 2013. “The Biophysicochemical Interactions at the Interfaces Between Nanoparticles and Aquatic Organisms: Adsorption and Internalization.” Environmental Science. Processes & Impacts 15 (1): 145–160. doi:10.1039/c2em30637a.
   PubMed Web of Science ®Google Scholar
• Manier, N., A. Bado-Nilles, P. Delalain, O. Aguerre-Chariol, and P. Pandard. 2013. “Ecotoxicity of Non-Aged and Aged CeO2 Nanomaterials Towards Freshwater Microalgae.” Environmental Pollution (Barking, Essex : 1987) 180: 63–70. doi:10.1016/j.envpol.2013.04.040.
   PubMed Web of Science ®Google Scholar
• Manier, N., S. Le Manach, A. Bado-Nilles, and P. Pandard. 2016. “Effect of Two TiO2 Nanoparticles on the Growth of Unicellular Green Algae Using the OECD 201 Test Guideline: Influence of the Exposure System.” Toxicological & Environmental Chemistry 98: 860–876. doi:10.1080/02772248.2015.1124881.
   Web of Science ®Google Scholar
• Mathé, C., S. Devineau, J.-C. Aude, G. Lagniel, S. Chédin, V. Legros, M.-H. Mathon, et al. 2013. “Structural Determinants for Protein Adsorption/Non-Adsorption to Silica Surface.” Plos One 8 (11): e81346. doi:10.1371/journal.pone.0081346.
   PubMed Web of Science ®Google Scholar
• Ma, H., P. L. Williams, and S. A. Diamond. 2013. “Ecotoxicity of Manufactured ZnO nanoparticles – A Review.” Environmental Pollution (Barking, Essex : 1987) 172: 76–85. doi:10.1016/j.envpol.2012.08.011.
   PubMed Web of Science ®Google Scholar
• Ma, S., K. Zhou, K. Yang, and D. Lin. 2015. “Heteroagglomeration of Oxide Nanoparticles with Algal Cells: Effects of Particle Type, Ionic Strength and pH.” Environmental Science & Technology 49 (2): 932–939. doi:10.1021/es504730k.
   PubMed Web of Science ®Google Scholar
• Monikh, F. A., D. Arenas-Lago, P. Porcal, R. Grillo, P. Zhang, Z. Guo, M. G. Vijver, and W. J. G. M. Peijnenburg. 2020. “Do the Joint Effects of Size, Shape and Ecocorona Influence the Attachment and Physical Eco(cyto)toxicity of nanoparticles to algae?” Nanotoxicology 14 (3): 310–325. doi:10.1080/17435390.2019.1692381.
   PubMed Web of Science ®Google Scholar
• Nolte, T. M., N. B. Hartmann, J. M. Kleijn, J. Garnaes, D. van de Meent, A. Jan Hendriks, and A. Baun. 2017. “The Toxicity of Plastic Nanoparticles to Green Algae as Influenced by Surface Modification, Medium Hardness and Cellular Adsorption.” Aquatic Toxicology (Amsterdam, Netherlands) 183: 11–20. doi:10.1016/j.aquatox.2016.12.005.
   PubMed Web of Science ®Google Scholar
• OECD. 2011. Test No. 201: Freshwater Alga and Cyanobacteria, Growth Inhibition Test.
   Google Scholar
• Oukarroum, A., S. Bras, F. Perreault, and R. Popovic. 2012. “Inhibitory Effects of Silver Nanoparticles in Two Green Algae, Chlorella vulgaris and Dunaliella tertiolecta.” Ecotoxicology and Environmental Safety 78: 80–85. doi:10.1016/j.ecoenv.2011.11.012.
   PubMed Web of Science ®Google Scholar
• Pajerski, W., D. Ochonska, M. Brzychczy-Wloch, P. Indyka, M. Jarosz, M. Golda-Cepa, Z. Sojka, and A. Kotarba. 2019. “Attachment Efficiency of Gold Nanoparticles by Gram-Positive and Gram-Negative Bacterial Strains Governed by Surface Charges.” Journal of Nanoparticle Research 21 (8): 186. doi:10.1007/s11051-019-4617-z.
   Web of Science ®Google Scholar
• Pakrashi, S., S. Dalai, P. T.C, S. Trivedi, R. Myneni, A. M. Raichur, N. Chandrasekaran, and A. Mukherjee. 2013. “Cytotoxicity of Aluminium Oxide Nanoparticles Towards Fresh Water Algal Isolate at Low Exposure Concentrations.” Aquatic Toxicology 132–133: 34–45. doi:10.1016/j.aquatox.2013.01.018.
   PubMed Web of Science ®Google Scholar
• Renault, S., M. Baudrimont, N. Mesmer-Dudons, P. Gonzalez, S. Mornet, and A. Brisson. 2008. “Impacts of Gold Nanoparticle Exposure on Two Freshwater Species: A Phytoplanktonic Alga (Scenedesmus subspicatus) and a Benthic Bivalve (Corbicula fluminea).” Gold Bulletin 41 (2): 116–126. doi:10.1007/BF03216589.
   Web of Science ®Google Scholar
• Ribeiro, F., J. A. Gallego-Urrea, R. M. Goodhead, C. A. M. V. Gestel, J. Moger, A. M. V. M. Soares, and S. Loureiro. 2015. “Uptake and Elimination Kinetics of Silver Nanoparticles and Silver Nitrate by Raphidocelis subcapitata: The Influence of Silver Behaviour in Solution.” Nanotoxicology 9 (6): 686–695. doi:10.3109/17435390.2014.963724.
   PubMed Web of Science ®Google Scholar
• Rodea-Palomares, I., K. Boltes, F. Fernández-Piñas, F. Leganés, E. García-Calvo, J. Santiago, and R. Rosal. 2011. “Physicochemical Characterization and Ecotoxicological Assessment of CeO2 Nanoparticles Using Two Aquatic Microorganisms.” Toxicological Sciences : An Official Journal of the Society of Toxicology 119 (1): 135–145. doi:10.1093/toxsci/kfq311.
   PubMed Web of Science ®Google Scholar
• Rogers, N. J., N. M. Franklin, S. C. Apte, G. E. Batley, B. M. Angel, J. R. Lead, and M. Baalousha. 2010. “Physico-Chemical Behaviour and Algal Toxicity of Nanoparticulate CeO2 in Freshwater.” Environmental Chemistry 7 (1): 50–60. doi:10.1071/EN09123.
   Web of Science ®Google Scholar
• Rosendal Tangaa, S., Selck, H., Winther-Nielsen, M., and Khan. R. F. 2016. “Trophic Transfer of Metal-Based Nanoparticles in Aquatic Environments: A Review and Recommendations for Future Research Focus.” Environmental Science: Nano 3 (5): 966–981. doi:10.1039/C5EN00280J.
   Web of Science ®Google Scholar
• Sendra, M., M. P. Yeste, J. M. Gatica, I. Moreno-Garrido, and J. Blasco. 2017. “Homoagglomeration and Heteroagglomeration of TiO2, in Nanoparticle and Bulk Form, onto Freshwater and Marine Microalgae.” The Science of the Total Environment 592: 403–411. doi:10.1016/j.scitotenv.2017.03.127.
   PubMed Web of Science ®Google Scholar
• Sheng, G.-P., H.-Q. Yu, and X.-Y. Li. 2010. “Extracellular Polymeric Substances (EPS) of Microbial Aggregates in Biological Wastewater Treatment Systems: A Review.” Biotechnology Advances 28 (6): 882–894. doi:10.1016/j.biotechadv.2010.08.001.
   PubMed Web of Science ®Google Scholar
• Showalter, A. M. 1993. “Structure and Function of Plant Cell Wall Proteins.” The Plant Cell 5 (1): 9–23. doi:10.2307/3869424.
   PubMed Web of Science ®Google Scholar
• Skjolding, L. M., S. N. Sørensen, N. B. Hartmann, R. Hjorth, S. F. Hansen, and A. Baun. 2016. “Aquatic Ecotoxicity Testing of Nanoparticles-The Quest To Disclose Nanoparticle Effects.” Angewandte Chemie (International Ed. in English) 55 (49): 15224–15239. doi:10.1002/anie.201604964.
   PubMed Web of Science ®Google Scholar
• Slaveykova, V. I., M. Li, I. A. Worms, and W. Liu. 2020. “When Environmental Chemistry Meets Ecotoxicology: Bioavailability of Inorganic Nanoparticles to Phytoplankton.” Chimia 74 (3): 115–121. doi:10.2533/chimia.2020.115.
   PubMed Web of Science ®Google Scholar
• Sørensen, S. N., C. Engelbrekt, H.-C. H. Lützhøft, J. Jiménez-Lamana, J. S. Noori, F. A. Alatraktchi, C. G. Delgado, V. I. Slaveykova, and A. Baun. 2016. “A Multimethod Approach for Investigating Algal Toxicity of Platinum Nanoparticles.” Environmental Science & Technology 50 (19): 10635–10643. doi:10.1021/acs.est.6b01072.
   PubMed Web of Science ®Google Scholar
• Suzuki, H., T. Toyooka, and Y. Ibuki. 2007. “Simple and Easy Method to Evaluate Uptake Potential of Nanoparticles in Mammalian Cells Using a Flow Cytometric Light Scatter Analysis.” Environmental Science & Technology 41 (8): 3018–3024. doi:10.1021/es0625632.
   PubMed Web of Science ®Google Scholar
• Taylor, G., D. J. Baird, and A. M. V. M. Soares. 1998. “Surface Binding of Contaminants by Algae: Consequences for Lethal Toxicity and Feeding to Daphnia magna Straus.” Environmental Toxicology and Chemistry 17 (3): 412–419. doi:10.1002/etc.5620170310.
   Web of Science ®Google Scholar
• Vallotton, P., B. Angel, M. Mccall, M. Osmond, and J. Kirby. 2015. “Imaging Nanoparticle-Algae Interactions in Three Dimensions Using Cytoviva Microscopy.” Journal of Microscopy 257 (2): 166–169. doi:10.1111/jmi.12199.
   PubMed Web of Science ®Google Scholar
• Valsesia, A., C. Desmet, I. Ojea-Jiménez, A. Oddo, R. Capomaccio, F. Rossi, and P. Colpo. 2018. “Direct Quantification of Nanoparticle Surface Hydrophobicity.” Communications Chemistry 1 (1): 53. doi:10.1038/s42004-018-0054-7.
   Google Scholar
• Van Hoecke, K., K. A. C. De Schamphelaere, P. Van der Meeren, S. Lcucas, and C. R. Janssen. 2008. “Ecotoxicity of Silica Nanoparticles to the Green Alga Pseudokirchneriella subcapitata: Importance of Surface Area.” Environmental Toxicology and Chemistry 27 (9): 1948–1957. doi:10.1897/07-634.1.
   PubMed Web of Science ®Google Scholar
• Viana, M. M., V. F. Soares, and N. D. S. Mohallem. 2010. “Synthesis and Characterization of TiO2 Nanoparticles.” Ceramics International 36 (7): 2047–2053. doi:10.1016/j.ceramint.2010.04.006.
   Web of Science ®Google Scholar
• Wang, F., W. Guan, L. Xu, Z. Ding, H. Ma, A. Ma, and N. Terry. 2019. “Effects of Nanoparticles on Algae: Adsorption, Distribution, Ecotoxicity and Fate.” Applied Sciences 9: 1534. doi:10.3390/app9081534.
   Google Scholar
• Wang, Y., X. Zhu, Y. Lao, X. Lv, Y. Tao, B. Huang, J. Wang, J. Zhou, and Z. Cai. 2016. “TiO2 Nanoparticles in the Marine Environment: Physical Effects Responsible for the Toxicity on Algae Phaeodactylum tricornutum.” The Science of the Total Environment 565: 818–826. doi:10.1016/j.scitotenv.2016.03.164.
   PubMed Web of Science ®Google Scholar
• Zhao, J., X. Cao, X. Liu, Z. Wang, C. Zhang, J. C. White, and B. Xing. 2016. “Interactions of CuO Nanoparticles with the Algae Chlorella pyrenoidosa: Adhesion, Uptake, and Toxicity.” Nanotoxicology 10 (9): 1297–1305. doi:10.1080/17435390.2016.1206149.
   PubMed Web of Science ®Google Scholar
• Zhou, K., Y. Hu, L. Zhang, K. Yang, and D. Lin. 2016. “The Role of Exopolymeric Substances in the Bioaccumulation and Toxicity of Ag Nanoparticles to Algae.” Scientific Reports 6: 32998–32911. doi:10.1038/srep32998.
   PubMed Web of Science ®Google Scholar
• Zucker, R. M., E. J. Massaro, K. M. Sanders, L. L. Degn, and W. K. Boyes. 2010. “Detection of TiO2 Nanoparticles in Cells by Flow Cytometry.” Cytometry. Part A : The Journal of the International Society for Analytical Cytology 77 (7): 677–685. doi:10.1002/cyto.a.20927.
   PubMedGoogle Scholar