Impact of wastewater-borne nanoparticles of silver and titanium dioxide on the swimming behaviour and biochemical markers of Daphnia magna: An integrated approach

Victor Galhano; Sarah Hartmann; Marta S Monteiro; Richard Zeumer; Darya Mozhayeva; Benedikt Steinhoff; Katharina Müller; Kirsten Prenzel; Jan Kunze; Klaus-Dieter Kuhnert; Holger Schönherr; Carsten Engelhard; Christian Schlechtriem; Susana Loureiro; Amadeu M V M Soares; Klaudia Witte; Isabel Lopes

doi:10.1016/j.aquatox.2020.105404

Impact of wastewater-borne nanoparticles of silver and titanium dioxide on the swimming behaviour and biochemical markers of Daphnia magna: An integrated approach

Aquat Toxicol. 2020 Mar:220:105404. doi: 10.1016/j.aquatox.2020.105404. Epub 2020 Jan 9.

Authors

Victor Galhano¹, Sarah Hartmann², Marta S Monteiro³, Richard Zeumer⁴, Darya Mozhayeva⁵, Benedikt Steinhoff⁶, Katharina Müller⁷, Kirsten Prenzel⁸, Jan Kunze⁹, Klaus-Dieter Kuhnert¹⁰, Holger Schönherr¹¹, Carsten Engelhard¹², Christian Schlechtriem¹³, Susana Loureiro¹⁴, Amadeu M V M Soares¹⁵, Klaudia Witte¹⁶, Isabel Lopes¹⁷

Affiliations

¹ Department of Biology and Centre for Environmental and Marine Studies (CESAM), University of Aveiro, Campus Universitário de Santiago, 3810-193, Aveiro, Portugal. Electronic address: [email protected].
² Research Group of Ecology and Behavioural Biology, Institute of Biology, Department of Chemistry-Biology, University of Siegen, Adolf-Reichwein-Strasse 2, Siegen, 57076, Germany. Electronic address: [email protected].
³ Department of Biology and Centre for Environmental and Marine Studies (CESAM), University of Aveiro, Campus Universitário de Santiago, 3810-193, Aveiro, Portugal. Electronic address: [email protected].
⁴ Fraunhofer Institute for Molecular Biology and Applied Ecology IME, Auf dem Aberg 1, Schmallenberg, 57392, Germany; Institute of Environmental Research (Biology V), RWTH Aachen University, Worringer Weg 1, Aachen, 52074, Germany; Faculty of Agriculture/Environment/Chemistry, Dresden University of Applied Sciences, Friedrich-List-Platz 1, Dresden, 01096, Germany. Electronic address: [email protected].
⁵ Analytical Chemistry, Department of Chemistry-Biology, University of Siegen, Adolf-Reichwein-Strasse 2, Siegen, 57076, Germany. Electronic address: [email protected].
⁶ Physical Chemistry I, Department of Chemistry-Biology, University of Siegen, Adolf-Reichwein-Strasse 2, Siegen, 57076, Germany; Center of Micro- and Nanochemistry and Engineering (Cμ), University of Siegen, Adolf-Reichwein-Strasse 2, 57076, Siegen, Germany. Electronic address: [email protected].
⁷ Research Group of Ecology and Behavioural Biology, Institute of Biology, Department of Chemistry-Biology, University of Siegen, Adolf-Reichwein-Strasse 2, Siegen, 57076, Germany. Electronic address: [email protected].
⁸ Research Group of Ecology and Behavioural Biology, Institute of Biology, Department of Chemistry-Biology, University of Siegen, Adolf-Reichwein-Strasse 2, Siegen, 57076, Germany. Electronic address: [email protected].
⁹ Institute of Real-time Learning Systems, Department of Electrical Engineering and Computer Science, University of Siegen, Hoelderlinstrasse, 3, Siegen, 57076, Germany. Electronic address: [email protected].
¹⁰ Institute of Real-time Learning Systems, Department of Electrical Engineering and Computer Science, University of Siegen, Hoelderlinstrasse, 3, Siegen, 57076, Germany. Electronic address: [email protected].
¹¹ Physical Chemistry I, Department of Chemistry-Biology, University of Siegen, Adolf-Reichwein-Strasse 2, Siegen, 57076, Germany; Center of Micro- and Nanochemistry and Engineering (Cμ), University of Siegen, Adolf-Reichwein-Strasse 2, 57076, Siegen, Germany. Electronic address: [email protected].
¹² Analytical Chemistry, Department of Chemistry-Biology, University of Siegen, Adolf-Reichwein-Strasse 2, Siegen, 57076, Germany; Center of Micro- and Nanochemistry and Engineering (Cμ), University of Siegen, Adolf-Reichwein-Strasse 2, 57076, Siegen, Germany. Electronic address: [email protected].
¹³ Fraunhofer Institute for Molecular Biology and Applied Ecology IME, Auf dem Aberg 1, Schmallenberg, 57392, Germany; Institute of Environmental Research (Biology V), RWTH Aachen University, Worringer Weg 1, Aachen, 52074, Germany; Ecotoxicology Work Group, Institute of Biology, Department of Chemistry-Biology, University of Siegen, Adolf-Reichwein-Strasse 2, Siegen 57076, Germany. Electronic address: [email protected].
¹⁴ Department of Biology and Centre for Environmental and Marine Studies (CESAM), University of Aveiro, Campus Universitário de Santiago, 3810-193, Aveiro, Portugal. Electronic address: [email protected].
¹⁵ Department of Biology and Centre for Environmental and Marine Studies (CESAM), University of Aveiro, Campus Universitário de Santiago, 3810-193, Aveiro, Portugal. Electronic address: [email protected].
¹⁶ Research Group of Ecology and Behavioural Biology, Institute of Biology, Department of Chemistry-Biology, University of Siegen, Adolf-Reichwein-Strasse 2, Siegen, 57076, Germany. Electronic address: [email protected].
¹⁷ Department of Biology and Centre for Environmental and Marine Studies (CESAM), University of Aveiro, Campus Universitário de Santiago, 3810-193, Aveiro, Portugal. Electronic address: [email protected].

PMID: 31954982
DOI: 10.1016/j.aquatox.2020.105404

Abstract

Due to their widespread use, silver (Ag) and titanium dioxide (TiO₂) nanoparticles (NPs) are commonly discharged into aquatic environments via wastewater treatment plants. The study was aimed to assess the effects of wastewater-borne AgNPs (NM-300 K; 15.5 ± 2.4 nm; 25-125 μg L^-1) and TiO₂NPs (NM-105; 23.1 ± 6.2 nm; 12.5-100 μg L^-1), from a laboratory-scale wastewater treatment plant, on Daphnia magna, at individual and subcellular level. For effect comparison, animals were also exposed to ASTM-dispersed NPs at the same nominal concentrations. The behaviour of D. magna was evaluated through monitoring of swimming height and allocation time for preferred zones after 0 h and 96 h of exposure. Biochemical markers of neurotransmission, anaerobic metabolism, biotransformation, and oxidative stress were subsequently determined. No 96-h EC₅₀ (immobilization ≤ 4 %) could be obtained with wastewater-borne NPs and ASTM-dispersed TiO₂NPs, whereas the ASTM-dispersed AgNPs resulted in an immobilization 96-h EC₅₀ of 113.8 μg L^-1. However, both wastewater-borne and ASTM-dispersed TiO₂NPs, at 12.5 μg L^-1, caused immediate (0 h) alterations on the swimming height. Allocation time analyses showed that animals exposed to ASTM-dispersed AgNPs spent more time on the surface and bottom at 0 h, and in the middle and bottom at 96 h. This pattern was not observed with ASTM-dispersed TiO₂NPs nor with wastewater-borne AgNPs and wastewater-borne TiO₂NPs. At the biochemical level, the more pronounced effects were observed with wastewater-borne AgNPs (e.g. induction of lactate dehydrogenase and glutathione S-transferase activities, and inhibition of catalase activity). This integrative approach showed that: (i) the behavioural and biochemical response-patterns were distinct in D. magna exposed to environmentally relevant concentrations of wastewater-borne and ASTM-dispersed NPs; (ii) the most pronounced effects on allocation time were induced by ASTM-dispersed AgNPs; and (iii) at the subcellular level, wastewater-borne AgNPs were more toxic than wastewater-borne TiO₂NPs. This study highlights the need for the assessment of the effects of wastewater-borne NPs under realistic exposure scenarios, since processes in wastewater treatment plants may influence their toxicity.

Keywords: AgNPs; Cladocera; Oxidative stress; TiO(2)NPs; Vertical migration; Wastewater treatment plants.

MeSH terms

Animals
Biomarkers / metabolism
Daphnia / drug effects*
Daphnia / metabolism
Metal Nanoparticles / toxicity*
Oxidative Stress / drug effects
Silver / toxicity*
Swimming
Titanium / toxicity*
Wastewater / chemistry*
Water Pollutants, Chemical / toxicity*

Substances

Biomarkers
Waste Water
Water Pollutants, Chemical
titanium dioxide
Silver
Titanium