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Biological Surface Coating and Molting Inhibition as Mechanisms of TiO2 Nanoparticle Toxicity in Daphnia magna
Open accessAbstract
The production and use of nanoparticles (NP) has steadily increased within the last decade; however, knowledge about risks of NP to human health and ecosystems is still scarce. Common knowledge concerning NP effects on freshwater organisms is largely limited to standard short-term (≤48 h) toxicity tests, which lack both NP fate characterization and an understanding of the mechanisms underlying toxicity. Employing slightly longer exposure times (72 to 96 h), we found that suspensions of nanosized (∼100 nm initial mean diameter) titanium dioxide (nTiO(2)) led to toxicity in Daphnia magna at nominal concentrations of 3.8 (72-h EC(50)) and 0.73 mg/L (96-h EC(50)). However, nTiO(2) disappeared quickly from the ISO-medium water phase, resulting in toxicity levels as low as 0.24 mg/L (96-h EC(50)) based on measured concentrations. Moreover, we showed that nTiO(2) (∼100 nm) is significantly more toxic than non-nanosized TiO(2) (∼200 nm) prepared from the same stock suspension. Most importantly, we hypothesized a mechanistic chain of events for nTiO(2) toxicity in D. magna that involves the coating of the organism surface with nTiO(2) combined with a molting disruption. Neonate D. magna (≤6 h) exposed to 2 mg/L nTiO(2) exhibited a "biological surface coating" that disappeared within 36 h, during which the first molting was successfully managed by 100% of the exposed organisms. Continued exposure up to 96 h led to a renewed formation of the surface coating and significantly reduced the molting rate to 10%, resulting in 90% mortality. Because coating of aquatic organisms by manmade NP might be ubiquitous in nature, this form of physical NP toxicity might result in widespread negative impacts on environmental health.
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“MPs may also adhere directly to organisms (Dabrunz et al., 2011;Cole et al., 2013).”
From Studies of the Effects of Microplastics on Aquatic Organisms: What Do We Know and Where Should We Focus Our Efforts in the Future? (2018) · cites this paper as Dabrunz et al., 2011
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“In other words, the relatively high ecotoxicity of 0 and 1 d aged particles can be associated with a potentially higher share of small sized nTiO2 in the water phase (see [11,28]) when compared to longer aging periods.”
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Monitoring the Fate and Transformation of Silver Nanoparticles in Natural Waters
Furtado, L. M., Bundschuh, M., & Metcalfe, C. D. (2016) · Bulletin of Environmental Contamination and Toxicology · doi:10.1007/s00128-016-1888-2 · Cited by 44
Zhang, Y.-Q., Dringen, R., Petters, C., Rastedt, W., Köser, J., Filser, J., & Stolte, S. (2016) · Environmental Science Nano · doi:10.1039/c5en00222b · Cited by 43
Nasser, F., Davis, A., Valsami‐Jones, E., & Lynch, I. (2016) · Nanomaterials · doi:10.3390/nano6120222 · Cited by 43
Bundschuh, M., Englert, D., Rosenfeldt, R. R., Bundschuh, R., Feckler, A., Lüderwald, S., Seitz, F., Zubrod, J. P., & Schulz, R. (2019) · Scientific Reports · doi:10.1038/s41598-019-52096-7 · Cited by 42
AKSAKAL, F. İ. (2020) · Comparative Biochemistry and Physiology Part C Toxicology & Pharmacology · doi:10.1016/j.cbpc.2020.108830 · Cited by 42
Lai, R. W. S., Yung, M. M. N., Zhou, G., He, Y. L., Ng, A. M. C., Djurišić, A. B., Shih, K., & Leung, K. (2020) · Environmental Science Nano · doi:10.1039/d0en00467g · Cited by 42
Bundschuh, M., Seitz, F., Rosenfeldt, R. R., & Schulz, R. (2012) · PLoS ONE · doi:10.1371/journal.pone.0048956 · Cited by 41
“00 mg/L treatment were verified weekly by inductively coupled plasma mass spectrometry [9].”
BackgroundMethodInfluentialLi, L., Xu, M., Mu, H., Wang, W., Sun, J., He, J., Qiu, J., & Luan, T. (2019) · Environmental Science & Technology · doi:10.1021/acs.est.9b00251 · Cited by 41
Nasser, F., & Lynch, I. (2019) · Safety Science · doi:10.1016/j.ssci.2019.05.045 · Cited by 41
Park, S., Woodhall, J. W., Ma, G., Veinot, J. G. C., Cresser, M. S., & Boxall, A. B. A. (2013) · Nanotoxicology · doi:10.3109/17435390.2013.818173 · Cited by 39
“…ecotoxicity studies follow traditional test method guidelines such as those developed by the Organisation for Economic Co-operation and Development (OECD) or U.S. Environmental Protection Agency (EPA) (e.g. Dabrunz et al. 2011; Wiench et al. 2009; Lovern & Klaper 2006; Rogers et al. 2010).”
BackgroundMethodFood web effects of titanium dioxide nanoparticles in an outdoor freshwater mesocosm experiment
Jovanović, B., Bezirci, G., Çağan, A. S., Coppens, J., Levi, E. E., Oluz, Z., Tuncel, E., Duran, H., & Beklioğlu, M. (2016) · Nanotoxicology · doi:10.3109/17435390.2016.1140242 · Cited by 39
“, 2012) and zooplankton (Dabrunz et al., 2011) has been described as the”
BackgroundInfluentialChitosan-silver nanocomposites in goldfish aquaria: A new perspective in Lernaea cyprinacea control
Abu‐Elala, N. M., Attia, M. M., & Abd‐Elsalam, R. M. (2017) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2017.12.133 · Cited by 39
The Toxicity of Nanoparticles to Organisms in Freshwater
Lekamge, S., Ball, A. S., Shukla, R., & Nugegoda, D. (2018) · Reviews of Environmental Contamination and Toxicology · doi:10.1007/398_2018_18 · Cited by 40
Different modes of TiO2 uptake by Ceriodaphnia dubia: Relevance to toxicity and bioaccumulation
Dalai, S., Iswarya, V., Bhuvaneshwari, M., Pakrashi, S., Chandrasekaran, N., & Mukherjee, A. (2014) · Aquatic Toxicology · doi:10.1016/j.aquatox.2014.04.002 · Cited by 37
“23% at 16, 32 and 64 g/mL respectively), which is probably due to bigger size of the particle aggregates (Dabrunz et al., 2012; Zhao and Wang, 2012).”
BackgroundBehavior and chronic toxicity of two differently stabilized silver nanoparticles to Daphnia magna
Sakka, Y., Skjolding, L. M., Mackevica, A., Filser, J., & Baun, A. (2016) · Aquatic Toxicology · doi:10.1016/j.aquatox.2016.06.025 · Cited by 37
“Attachment to the carapax has been reported for several NPs with different core materials and coatings (Asghari et al., 2012; Baumann et al., 2014a; Bozich et al., 2014; Dabrunz et al., 2011; Zhao and Wang, 2012).”
BackgroundInfluentialHansen, S. F., Sørensen, S. N., Skjolding, L. M., Hartmann, N. B., & Baun, A. (2017) · Environmental Sciences Europe · doi:10.1186/s12302-017-0111-3 · Cited by 37
Toxicity of Zn-Fe Layered Double Hydroxide to Different Organisms in the Aquatic Environment
Koba, O., Ölmez-Hancı, T., Arslan‐Alaton, I., Arefi-Oskoui, S., Khataee, A., Kobya, M., & Orooji, Y. (2021) · Molecules · doi:10.3390/molecules26020395 · Cited by 37
“As has been reported previously, NMs can be agglomerated into microscopic particles in a high ionic strength medium as in the present case, inducing a change in their morphology and instability in surface properties [51].”
BackgroundInfluentialSize matters – The phototoxicity of TiO2 nanomaterials
Wyrwoll, A., Lautenschläger, P., Bach, A. D., Hellack, B., Dybowska, A. D., Kuhlbusch, T. A. J., Hollert, H., Schäffer, A., & Maes, H. M. (2015) · Environmental Pollution · doi:10.1016/j.envpol.2015.10.035 · Cited by 37
Effects of nano-TiO2 in combination with ambient UV-irradiation on a leaf shredding amphipod
Bundschuh, M., Zubrod, J. P., Englert, D., Seitz, F., Rosenfeldt, R. R., & Schulz, R. (2011) · Chemosphere · doi:10.1016/j.chemosphere.2011.07.060 · Cited by 36
Castro, G. B., Bernegossi, A. C., Felipe, M. C., & Corbi, J. J. (2020) · Journal of Environmental Science and Health Part A · doi:10.1080/10934529.2020.1756656 · Cited by 38
“[69] We observed that polyethylene microplastic did not cause a change in the molting process, which could be caused by ingestion or interaction of the microparticles with the body surface of the organisms, causing a rupture of the molting process, as observed when the species was exposed to TiO2 NPs [70] and Fe2O3 NP…”
BackgroundGalhano, V., Hartmann, S., Monteiro, M. S., Zeumer, R., Mozhayeva, D., Steinhoff, B., Müller, K., Prenzel, K., Kunze, J., Kuhnert, K.-D., et al. (2020) · Aquatic Toxicology · doi:10.1016/j.aquatox.2020.105404 · Cited by 35
Li, L., Sillanpää, M., & Schultz, E. (2017) · Journal of Nanoparticle Research · doi:10.1007/s11051-017-3916-5 · Cited by 35
“This adhesion phenomenon has been previously described by Baun et al. (2008) and Dabrunz et al. (2011).”
BackgroundLi, S., Wallis, L. K., Diamond, S. A., Ma, H., & Hoff, D. J. (2014) · Environmental Toxicology and Chemistry · doi:10.1002/etc.2583 · Cited by 34
“, mycosporine-like amino acids) [25–27].”
Titanium dioxide nanoparticles detoxify pirimicarb under UV irradiation at ambient intensities
Seitz, F., Bundschuh, M., Dabrunz, A., Bandow, N., Schaumann, G. E., & Schulz, R. (2011) · Environmental Toxicology and Chemistry · doi:10.1002/etc.1715 · Cited by 34
Kim, J., Lee, S., Kim, C.-M., Seo, J., Park, Y., Kwon, D., Lee, S.-H., Yoon, T. H., & Choi, K. (2014) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2014.01.002 · Cited by 33
Rosenfeldt, R. R., Seitz, F., Zubrod, J. P., Feckler, A., Merkel, T., Lüderwald, S., Bundschuh, R., Schulz, R., & Bundschuh, M. (2015) · Aquatic Toxicology · doi:10.1016/j.aquatox.2015.05.011 · Cited by 32
Significance of particle size and charge capacity in TiO2 nanoparticle-lipid interactions
Vakurov, A. V., Brydson, R., Ugwumsinachi, O., & Nelson, A. L. (2016) · Journal of Colloid and Interface Science · doi:10.1016/j.jcis.2016.03.045 · Cited by 32
“Toxicology and Environmental Health Science 3 1-6 [8] Dabrunz A Duester L Prasse C Seitz F Rosenfeldt R Schilde C Schaumann G E Schulz R”
BackgroundIndividual and binary toxicity of anatase and rutile nanoparticles towards Ceriodaphnia dubia
Iswarya, V., Bhuvaneshwari, M., Chandrasekaran, N., & Mukherjee, A. (2016) · Aquatic Toxicology · doi:10.1016/j.aquatox.2016.08.007 · Cited by 31
Li, D., Chen, H., Bi, R., Xie, H., Zhou, Y., Luo, Y., & Xie, L. (2017) · Chemosphere · doi:10.1016/j.chemosphere.2017.10.022 · Cited by 31
Ciocan, C. M., Kristová, P., Annels, C., Derjean, M., & Hopkinson, L. (2020) · Marine Pollution Bulletin · doi:10.1016/j.marpolbul.2020.111559 · Cited by 32
Metadata
- Authors
- Dabrunz, A., Duester, L., Prasse, C., Seitz, F., Rosenfeldt, R., Schilde, C., Schaumann, G. E., & Schulz, R.
- Affiliations
- University of Koblenz and Landau (DE)
- Technische Universität Braunschweig (DE)
- Corresponding author
- Schulz, Ralf
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2011-05-27
- Volume
- 6
- Issue
- 5
- Pages
- e20112
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC3103543
- OpenAlex
- W1971246481
- Cited by
- 208
- References
- 38
- Citations by year
- 2026: 4 · 2025: 4 · 2024: 7 · 2023: 9 · 2022: 12 · 2021: 10 · 2020: 14 · 2019: 15 · 2018: 17 · 2017: 13 · 2016: 26 · 2015: 22 · 2014: 22 · 2013: 13 · 2012: 14
- FWCI
- 12.45
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS ONE (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Topics
- Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Environmental Toxicology and Ecotoxicology
- Physical Sciences › Materials Science › Materials Chemistry › Nanoparticles: synthesis and applications
- Physical Sciences › Environmental Science › Pollution › Microplastics and Plastic Pollution
- Keywords
- titanium dioxide nanoparticles, nanoparticle toxicity, Daphnia magna, molting inhibition, particle size effects, freshwater zooplankton, ecotoxicology, long-term exposure
- MeSH terms
- Animals, Daphnia, Dose-Response Relationship, Drug, Particle Size, Suspensions, Time Factors, Titanium, Water, Molting, Nanoparticles
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