Understanding the role of nano-TiO₂ on the toxicity of Pb on C. dubia through modeling–Is it additive or synergistic?

Highlights

• A two-compartment model is able to quantify the effect of nano-TiO₂ on Pb toxicity.

• Nano-TiO₂ reduces Pb tolerance level and increased the killing rate for C. dubia.

• Thus, nano-TiO₂ synergistically enhances Pb toxicity.

• Algae reduce Pb transfer rate to the body tissue and the killing rate.

Abstract

Nano-TiO₂ can remarkably increase lead (Pb) toxicity in aquatic organisms. However, the mechanism of this toxicity, additive or synergistic, is not well understood. To explore this mechanism, we inspected the role of nano-TiO₂ in the toxicity of Pb on Ceriodaphnia dubia (C. dubia), a model water flea species typically used for ecotoxicity studies. The effect of algae, a diet for aquatic organisms, on the effect of this binary mixture was also investigated. A two-compartment toxicokinetic (TK)-toxicodynamic (TD) modeling approach was used to quantify the Pb toxicity under these complex conditions and to develop critical parameters for understanding the mechanism of toxicity. This two-compartment modeling approach adequately described the Pb accumulation in the gut and in the rest of the body tissue under different nano-TiO₂ concentrations, with and without algae, and predicted the toxicity response of C. dubia. It indicated that increasing the nano-TiO₂ concentration reduced the Pb tolerance level and concurrently increased the killing rate constant of C. dubia. Therefore, nano-TiO₂ synergistically enhanced Pb toxicity. Algae remarkably reduced the toxicity of this binary mixture through reducing the Pb transfer rate to the body tissue and the killing rate, although it did not affect the Pb tolerance level. This two-compartment modeling approach is useful in understanding the role of nanoparticles when assessing the overall toxicity of nanoparticles and other toxic elements in the environment.

Graphical abstract

Keywords

Algae / C. dubia / Lead / Nano-TiO₂ / Synergistic toxicity / Two-compartment toxicokinetic-toxicodynamic model

References

[1] Allen N S, Edge M, Verran J, Stratton J, Maltby J, Bygott C (2008). Photocatalytic titania based surfaces: Environmental benefits. Polymer Degradation & Stability, 93(9): 1632–1646

[2] Bundschuh M, Filser J, Lüderwald S, McKee M S, Metreveli G, Schaumann G E, Schulz R, Wagner S (2018). Nanoparticles in the environment: Where do we come from, Where do we go to? Environmental Sciences Europe, 30(1): 6

[3] Cai L, Sun X, Hao D, Li S, Gong X, Ding H, Yu K (2020). Sugarcane bagasse amendment improves the quality of green waste vermicompost and the growth of Eisenia fetida. Frontiers of Environmental Science & Engineering, 14(4): 61

[4] Cedergreen N, Dalhoff K, Li D, Gottardi M, Kretschmann A C (2017). Can toxicokinetic and toxicodynamic modeling be used to understand and predict synergistic interactions between chemicals? Environmental Science & Technology, 51(24): 14379–14389

[5] Dudefoi W, Moniz K, Allen-Vercoe E, Ropers M H, Walker V K (2017). Impact of food grade and nano-TiO₂ particles on a human intestinal community. Food and Chemical Toxicology, 106(Pt A): 242–249

[6] Ebert D P (2005).Ecology, Epidemiology, and Evolution of Parasitism in Daphnia. Bethesda (MD): National Library of Medicine (USA), National Center for Biotechnology Information

[7] Egorova K S, Ananikov V P (2017). Toxicity of metal compounds: Knowledge and myths. Organometallics, 36(21): 4071–4090

[8] EPA (1994). Using toxicity tests in ecological risk assessment. Washington, DC: Environmental Protection Agency

[9] EPA (2002). Methods for measuring the acute toxicity of effluents and receiving waters to freshwater and marine organisms. Washington, DC: Environmental Protection Agency

[10] Ercal N, Gurer-Orhan H, Aykin-Burns N (2001). Toxic metals and oxidative stress part I: Mechanisms involved in metal-induced oxidative damage. Current Topics in Medicinal Chemistry, 1(6): 529–539

[11] Fan W, Cui M, Liu H, Wang C, Shi Z, Tan C, Yang X (2011). Nano-TiO₂ enhances the toxicity of copper in natural water to Daphnia magna. Environmental Pollution (Barking, Essex: 1987), 159(3): 729–734

[12] Gillis P L, Chow-Fraser P, Ranville J F, Ross P E, Wood C M (2005). Daphnia need to be gut-cleared too: the effect of exposure to and ingestion of metal-contaminated sediment on the gut-clearance patterns of D. magna. Aquatic Toxicology (Amsterdam, Netherlands), 71(2): 143–154

[13] Horton P A, Rowan M, Webster K E, Peters R H (1979). Browsing and grazing by cladoceran filter feeders. Canadian Journal of Zoology, 57(1): 206–212

[14] Hu J, Shipley H J (2012). Evaluation of desorption of Pb (II), Cu (II) and Zn (II) from titanium dioxide nanoparticles. Science of the Total Environment, 431: 209–220

[15] Hu J, Wang D, Forthaus B E, Wang J (2012b). Quantifying the effect of nanoparticles on As(V) ecotoxicity exemplified by nano-Fe₂O₃ (magnetic) and nano-Al₂O₃. Environmental Toxicology and Chemistry, 31(12): 2870–2876

[16] Hu J, Wang D, Wang J, Wang J (2012a). Toxicity of lead on Ceriodaphnia dubia in the presence of nano-CeO₂ and nano-TiO₂. Chemosphere, 89(5): 536–541

[17] Huang C P, Chou H W, Tseng Y H, Fan M (2010a). Responses of Ceriodaphnia dubia to photocatalytic nano-titanium dioxide particles. In: Fan M, Huang C, Bland A, Wang Z, Slimane R, Wright I, eds. Environanotechnology. Amsterdam: Elsevier, 1–21

[18] Huang Y W, Wu C H, Aronstam R S (2010b). Toxicity of transition metal oxide nanoparticles: Recent insights from in vitro studies. Materials (Basel), 3(10): 4842–4859

[19] ICMM (2007). Health Risk Assessment Guidance for Metals. Fact Sheet 4. London: International Council on Mining and Metals

[20] Kerper L E, Hinkle P M (1997). Cellular uptake of lead is activated by depletion of intracellular calcium stores. Journal of Biological Chemistry, 272(13): 8346–8352

[21] Kiela P R, Ghishan F K (2016). Physiology of intestinal absorption and secretion. Best Practice & Research. Clinical Gastroenterology, 30(2): 145–159

[22] Lademann J, Weigmann H, Rickmeyer C, Barthelmes H, Schaefer H, Mueller G, Sterry W (1999). Penetration of titanium dioxide microparticles in a sunscreen formulation into the horny layer and the follicular orifice. Skin Pharmacology and Applied Skin Physiology, 12(5): 247–256

[23] Li F, Liang Z, Zheng X, Zhao W, Wu M, Wang Z (2015). Toxicity of nano-TiO₂ on algae and the site of reactive oxygen species production. Aquatic Toxicology (Amsterdam, Netherlands), 158: 1–13

[24] Liu X, Wang J (2020). Algae (Raphidocelis subcapitata) mitigate combined toxicity of microplastic and lead on Ceriodaphnia dubia. Frontiers of Environmental Science & Engineering, 14(6): 97

[25] Liu X, Wang J, Huang Y W (2021). Quantifying the effect of nano-TiO₂ on the toxicity of lead on C. dubia using a two-compartment modeling approach. Chemosphere, 263: 127958

[26] Liu X, Wang J, Huang Y W, Kong T (2019). Algae (Raphidocelis) reduce combined toxicity of nano-TiO₂ and lead on C. dubia. Science of the Total Environment, 686: 246–253

[27] López-Serrano A, Olivas R M, Landaluze J S, Cámara C (2014). Nanoparticles: A global vision. Characterization, separation, and quantification methods. Potential environmental and health impact. Analytical Methods, 6(1): 38–56

[28] O’Regan B, Grätzel M (1991). A low-cost, high-efficiency solar cell based on dye-sensitized colloidal TiO₂ films. Nature, 353(6346): 737–740

[29] Poljsak B, Šuput D, Milisav I (2013). Achieving the balance between ROS and antioxidants: when to use the synthetic antioxidants. Oxidative Medicine and Cellular Longevity, 2013: 956792

[30] Roell K R, Reif D M, Motsinger-Reif A A (2017). An introduction to terminology and methodology of chemical synergy—Perspectives from across disciplines. Frontiers in Pharmacology, 8: 158

[31] Romay C, Armesto J, Remirez D, González R, Ledon N, García I (1998). Antioxidant and anti-inflammatory properties of C-phycocyanin from blue-green algae. Inflammation Research, 47(1): 36–41

[32] Roy D, Greenlaw P N, Shane B S (1993). Adsorption of heavy metals by green algae and ground rice hulls. Journal of Environmental Science and Health, Part A: Environmental Science and Engineering, 28(1): 37–50

[33] Sparks D L (2005). Toxic metals in the environment: the role of surfaces. Elements, 1(4): 193–197

[34] Tan C, Fan W H, Wang W X (2012). Role of titanium dioxide nanoparticles in the elevated uptake and retention of cadmium and zinc in Daphnia magna. Environmental Science & Technology, 46(1): 469–476

[35] Tan C, Wang W X (2017). Influences of TiO₂ nanoparticles on dietary metal uptake in Daphnia magna. Environmental Pollution (Barking, Essex : 1987), 231(Pt 1): 311–318

[36] Tan L Y, Huang B, Xu S, Wei Z B, Yang L Y, Miao A J (2017). Aggregation reverses the carrier effects of TiO₂ nanoparticles on cadmium accumulation in the waterflea Daphnia magna. Environmental Science & Technology, 51(2): 932–939

[37] Tan Q G, Wang W X (2012). Two-compartment toxicokinetic-toxicodynamic model to predict metal toxicity in Daphnia magna. Environmental Science & Technology, 46(17): 9709–9715

[38] Vohra M S, Davis A P (1997). Adsorption of Pb(II), NTA, and Pb(II)-NTA onto TiO₂. Journal of Colloid and Interface Science, 194(1): 59–67

[39] Wang D, Hu J, Forthaus B E, Wang J (2011b). Synergistic toxic effect of nano-Al₂O₃ and As(V) on Ceriodaphnia dubia. Environmental Pollution (Barking, Essex: 1987), 159(10): 3003–3008

[40] Wang D, Hu J, Irons D R, Wang J (2011a). Synergistic toxic effect of nano-TiO and As(V) on Ceriodaphnia dubia. Science of the Total Environment, 409(7): 1351–1356

[41] Wani A L, Ara A, Usmani J A (2015). Lead toxicity: A review. Interdisciplinary Toxicology, 8(2): 55–64

[42] Zhou Z, Son J, Harper B, Zhou Z, Harper S (2015). Influence of surface chemical properties on the toxicity of engineered zinc oxide nanoparticles to embryonic zebrafish. Beilstein Journal of Nanotechnology, 6: 1568–1579

Acknowledgements

The authors appreciate instrumentation support from the Center for Research in Energy and Environment (CREE) at Missouri University of Science and Technology (USA). The authors also appreciate the invaluable suggestions made by Natalie Holl from the Department of Biological Sciences.

Electronic Supplementary Material

ƒSupplementary material is available in the online version of this article at https://doi.org/10.1007/s11783-021-1493-4 and is accessible for authorized users.

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