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.
“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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“, mycosporinelike amino acids, MAAs) (Dabrunz et al., 2011; Dunlap and Yamamoto, 1995; McClintock and Karentz, 1997).”
Wang, T., & Liu, W. (2022) · Environmental Science Nano · doi:10.1039/d2en00052k · Cited by 69 · see citing works
“36 Moreover, after 21 d of exposure, the longevity, growth, and reproduction of D. magna decreased significantly with increasing Al 2 O 3 NP concentration from 6.25 to 25 mg L − 1 .”
InfluentialPolydimethyl siloxane nanocomposites: Their antifouling efficacy in vitro and in marine conditions
Sankar, G. G., Sathya, S., Murthy, P. S., Das, A., Pandiyan, R., Venugopalan, V. P., & Doble, M. (2015) · International Biodeterioration & Biodegradation · doi:10.1016/j.ibiod.2015.05.022 · Cited by 66 · see citing works
“As the nanoparticles are embedded in the PDMS matrix and there is very little leaching taking place, only those organisms which come in to contact with the substratum get affected, and hence impact due to environmental release is minimal (Dabrunz et al., 2011).”
BackgroundDalai, S., Pakrashi, S., Chandrasekaran, N., & Mukherjee, A. (2013) · PLoS ONE · doi:10.1371/journal.pone.0062970 · Cited by 64 · see citing works
Carl, C., Poole, A. B., Vucko, M. J., Williams, M. R., Whalan, S., & de Nys, R. (2012) · Biofouling · doi:10.1080/08927014.2012.728588 · Cited by 64 · see citing works
“2012) and adhesion of aggregates to aquatic organisms (Dabrunz et al. 2011) is low because the nanoparticles are incorporated into the PDMS matrix.”
BackgroundNanoparticle toxicity in Daphnia magna reproduction studies: The importance of test design
Seitz, F., Bundschuh, M., Rosenfeldt, R. R., & Schulz, R. (2012) · Aquatic Toxicology · doi:10.1016/j.aquatox.2012.10.015 · Cited by 63 · see citing works
Fate, transport, and toxicity of nanoparticles: An emerging pollutant on biotic factors
Mishra, S., & Sundaram, B. (2023) · Process Safety and Environmental Protection · doi:10.1016/j.psep.2023.04.037 · Cited by 63 · see citing works
Lekamge, S., Miranda, A. F., Ball, A. S., Shukla, R., & Nugegoda, D. (2019) · PLoS ONE · doi:10.1371/journal.pone.0214398 · Cited by 62 · see citing works
Trinh, T. X., Seo, M., Yoon, T. H., & Kim, J. (2022) · NanoImpact · doi:10.1016/j.impact.2022.100383 · Cited by 62 · see citing works
Nano-pollution: Why it should worry us
Jan, N., Majeed, N., Ahmad, M., Lone, W. A., & John, R. (2022) · Chemosphere · doi:10.1016/j.chemosphere.2022.134746 · Cited by 63 · see citing works
Assessing the ecotoxicity of metal nano-oxides with potential for wastewater treatment
Nogueira, V. I. J. O., Lopes, I., Rocha‐Santos, T., Rasteiro, M. G., Abrantes, N., Gonçalves, F. J. M., Soares, A. M. V. M., Duarte, A. C., & Pereira, R. (2015) · Environmental Science and Pollution Research · doi:10.1007/s11356-015-4581-9 · Cited by 61 · see citing works
“Dabrunz et al. (2011) ob-”
BackgroundJovanović, B. (2015) · Environmental Toxicology and Chemistry · doi:10.1002/etc.2891 · Cited by 61 · see citing works
“In fact, surface attachment of nano-TiO2 to Cladocera carapace has been observed in previous studies [18,19], and the inner wall of the carapace is a major site of respiratory gas exchange for Cladocera [20].”
BackgroundAdam, N., Leroux, F. R., Knapen, D., Bals, S., & Blust, R. (2014) · Environmental Pollution · doi:10.1016/j.envpol.2014.06.037 · Cited by 59 · see citing works
Nanoparticle Surface Affinity as a Predictor of Trophic Transfer
Geitner, N. K., Marinakos, S. M., Guo, C., O’Brien, N., & Wiesner, M. R. (2016) · Environmental Science & Technology · doi:10.1021/acs.est.6b00056 · Cited by 59 · see citing works
Abdel‐Latif, H. M. R., Dawood, M. A. O., Menanteau‐Ledouble, S., & El‐Matbouli, M. (2020) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2020.110776 · Cited by 56 · see citing works
Noß, C., Dabrunz, A., Rosenfeldt, R. R., Lorke, A., & Schulz, R. (2013) · PLoS ONE · doi:10.1371/journal.pone.0080960 · Cited by 57 · see citing works
Zheng, M., Lü, J., & Zhao, D. (2017) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2017.12.018 · Cited by 56 · see citing works
Baumann, J., Sakka, Y., Bertrand, C., Köser, J., & Filser, J. (2013) · Environmental Science and Pollution Research · doi:10.1007/s11356-013-2094-y · Cited by 56 · see citing works
“The standard test duration of 48 h can underestimate the toxic effects of NMs. Dabrunz et al. (2011) have already shown increased toxicity and changed modes of action of TiO2 nanoparticles in a prolonged acute test with daphnids.”
BackgroundResultInfluentialWu, F., Bortvedt, A., Harper, B. J., Crandon, L. E., & Harper, S. L. (2017) · Aquatic Toxicology · doi:10.1016/j.aquatox.2017.06.021 · Cited by 56 · see citing works
Selmani, A., Ulm, L., Kasemets, K., Kurvet, I., Erceg, I., Barbir, R., Pem, B., Santini, P., Marion, I. D., Vinković, T., et al. (2020) · Chemosphere · doi:10.1016/j.chemosphere.2020.126265 · Cited by 55 · see citing works
Magro, M., Liguoro, M. D., Franzago, E., Baratella, D., & Vianello, F. (2018) · Scientific Reports · doi:10.1038/s41598-018-31483-6 · Cited by 54 · see citing works
Understanding the ecological impacts of nanoparticles: risks, monitoring, and mitigation strategies
Alizadeh, M., Qarachal, J. F., & Sheidaee, E. (2025) · Nanotechnology for Environmental Engineering · doi:10.1007/s41204-024-00403-7 · Cited by 52 · see citing works
Emergent Properties and Toxicological Considerations for Nanohybrid Materials in Aquatic Systems
Saleh, N. B., Afrooz, A. R. M. N., Bisesi, J. H., Aich, N., Plazas‐Tuttle, J., & Sabo‐Attwood, T. (2014) · Nanomaterials · doi:10.3390/nano4020372 · Cited by 52 · see citing works
Singh, A. K. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-801406-6.00008-x · Cited by 53 · see citing works
Surfactants decrease the toxicity of ZnO, TiO2 and Ni nanoparticles to Daphnia magna
Oleszczuk, P., Jośko, I. N., & Skwarek, E. (2015) · Ecotoxicology · doi:10.1007/s10646-015-1529-2 · Cited by 51 · see citing works
“Dabrunz et al. (2011) demonstrated that after a few hours most of nano-TiO2 sink to the bottom of the test beakers.”
BackgroundResultInfluentialRegulatory adequacy of aquatic ecotoxicity testing of nanomaterials
Hjorth, R., Skjolding, L. M., Sørensen, S. N., & Baun, A. (2017) · NanoImpact · doi:10.1016/j.impact.2017.07.003 · Cited by 50 · see citing works
“Case in point, in crustaceans, adsorption of CeO2, Pt and TiO2 MNs on the exoskeleton, cuticle and antenna is reported to influence mobility, molting, and swimming velocity (Artells et al., 2013; Cupi et al., 2015; Dabrunz et al., 2011; Gaiser et al., 2011; Noss et al., 2013).”
BackgroundRosenfeldt, R. R., Seitz, F., Senn, L., Schilde, C., Schulz, R., & Bundschuh, M. (2015) · Environmental Science & Technology · doi:10.1021/es506243d · Cited by 48 · see citing works
Lai, R. W. S., Kang, H.-M., Zhou, G., Yung, M. M. N., He, Y. L., Ng, A. M. C., Li, X.-Y., Djurišić, A. B., Lee, J., & Leung, K. (2021) · Environmental Science & Technology · doi:10.1021/acs.est.1c01300 · Cited by 48 · see citing works
Yang, Z., Lü, K., Chen, Y., & Montagnes, D. J. S. (2012) · PLoS ONE · doi:10.1371/journal.pone.0032285 · Cited by 47 · see citing works
“magna has been used to reveal the unexpected toxicity of fatty acids on zooplankton [40], the chronic toxicity of NOx to the crustacean [36], and the toxicity of nanoparticles on freshwater organisms [41].”
BackgroundSeitz, F., Lüderwald, S., Rosenfeldt, R. R., Schulz, R., & Bundschuh, M. (2015) · PLoS ONE · doi:10.1371/journal.pone.0126021 · Cited by 45 · see citing works
“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.”
BackgroundSeitz, F., Rosenfeldt, R. R., Schneider, S., Schulz, R., & Bundschuh, M. (2014) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2014.06.092 · Cited by 44 · see citing works
Role of molting on the biodistribution of CeO2 nanoparticles within Daphnia pulex
Auffan, M., Bertin, D., Chaurand, P., Paillès, C., Dominici, C., Rose, J., Bottero, J., & Thiéry, A. (2013) · Water Research · doi:10.1016/j.watres.2012.11.063 · Cited by 44 · see citing works
How to consider engineered nanomaterials in major accident regulations?
Nowack, B., Mueller, N. C., Krug, H. F., & Wick, P. (2014) · Environmental Sciences Europe · doi:10.1186/2190-4715-26-2 · Cited by 44 · see citing works
“8 [61]; other values (in mg/l): 1 [56], 3.”
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 · see citing works
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 · see citing works
Nasser, F., Davis, A., Valsami‐Jones, E., & Lynch, I. (2016) · Nanomaterials · doi:10.3390/nano6120222 · Cited by 43 · see citing works
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 · see citing works
AKSAKAL, F. İ. (2020) · Comparative Biochemistry and Physiology Part C Toxicology & Pharmacology · doi:10.1016/j.cbpc.2020.108830 · Cited by 42 · see citing works
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 · see citing works
Bundschuh, M., Seitz, F., Rosenfeldt, R. R., & Schulz, R. (2012) · PLoS ONE · doi:10.1371/journal.pone.0048956 · Cited by 41 · see citing works
“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 · see citing works
Nasser, F., & Lynch, I. (2019) · Safety Science · doi:10.1016/j.ssci.2019.05.045 · Cited by 41 · see citing works
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 · see citing works
“…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 · see citing works
“, 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 · see citing works
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 39 · see citing works
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 · see citing works
“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 · see citing works
“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 · see citing works
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 · see citing works
“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 · see citing works
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 · see citing works
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 36 · see citing works
“[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 · see citing works
Li, L., Sillanpää, M., & Schultz, E. (2017) · Journal of Nanoparticle Research · doi:10.1007/s11051-017-3916-5 · Cited by 35 · see citing works
“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 · see citing works
“, 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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
“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 · see citing works
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 · see citing works
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 · see citing works
- 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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