The co-occurrence of Zn-and Cu-based engineered nanoparticles in soils: The metal extractability vs. toxicity to Folsomia candida
Graphical abstract
Introduction
Zn- and Cu-based engineered nanoparticles (ENPs) are among the most widely used ENPs applied in material engineering, electronics, medicine, and agriculture (Rajput et al., 2020). The extensively growing production of ENPs over the last decades has ultimately led to their release into the environment, including soils (Rajput et al., 2020). The fate of ENPs in soil has been widely addressed (Hadri et al., 2018), including their transformations e.g. oxidation, dissolution, aggregation and related implications for biota (Joo and Zhao, 2017; Lowry et al., 2012). The status of ENPs transformations was governed by the chemical nature of ENPs (Dimkpa et al., 2012), their concentrations (Rajput et al., 2021) as well as soil properties (García-Gómez et al., 2018a) and aging (Gao et al., 2017; Romero-Freire et al., 2017). Pristine or transformed ENPs may induce a different effect than their ionic counterparts, especially due to short-time exposure (Gao et al., 2018; Tatsi et al., 2018). Over time these differences between the fate of nanoparticulate and ionic metals may disappear (Sekine et al., 2017; Wang et al., 2013).
The effect of metal-based ENPs on biota is attributed to the activity of the particulate form and/or ions released from them (Qiu and Smolders, 2017). Thus, the numerous studies have estimated the predicting availability of metal component of ENPs in soil in addition to evaluation of ecotoxicological endpoints (García-Gómez et al., 2015; Romero-Freire et al., 2017; Tatsi et al., 2018). The approaches determining the pool of available metals in soils focus on the soil pore water collection (García-Gómez et al., 2018b; Kool et al., 2011) or batch extractions with different extractants e.g. H2O (Tatsi et al., 2018), salts (CaCl2, NaNO3) (Antisari et al., 2015) or chelating agents (aminopolycarboxylic acid (EDTA), diethylenetriamine pentaacetate (DTPA)) (Gao et al., 2018; Jośko et al., 2021a; Verma et al., 2021). These methods are characterized by different metal leaching capacity (Sahuquillo et al., 2003). In case of heavy metals, their leachability depends on their affinity for different soil components and strength of these bonds (Rao et al., 2008). For instance, Zn predominantly occupies cation-exchangeable sites based on electrostatic interactions, whereas Cu creates an inner-sphere complex with soil constituents by covalent bonds (Refaey et al., 2017). Upon exposure of metal-based ENPs, the extractability of metals is additionally affected by the above-mentioned transformations of ENPs, such as dissolution (García-Gómez et al., 2017; Rodrigues et al., 2020). The relationship between the toxicity towards soil organisms and the extractable concentration of metals in soil spiked with ENPs was dependent on the type of ENPs, endpoints and the extraction techniques (Gao et al., 2018; García-Gómez et al., 2017). Some studies have indicated no/weak correlation of Zn concentrations in pore water from soil with nano-ZnO and endpoints, concluding that there was ENPs-specific toxicity to soil invertebrates (Romero-Freire et al., 2017). In turn, comparative study by Gao et al. (2018) found that phytotoxicity was related with the CaCl2-extractable concentration of Cu in samples with nano-CuO, but that tendency was not observed for Cu extracted by DTPA.
Most of the studies on the fate of ENPs in soils have addressed individual exposure to ENPs (Gao et al., 2017; García-Gómez et al, 2018a, 2018b; Tatsi et al., 2018), whereas little is known about the scenario of co-existing ENPs in the soil system (Jośko et al., 2021b, 2021c). Similar applications of ENPs such as Zn- and Cu-based ones (e.g. agrochemicals) entail the mixed occurrence of ENPs in soils. The combined effects of mixtures of chemicals may be similar (addition), less (antagonism) or more (synergism) toxic than individual exposure (Amorim et al., 2012). As the studies about heavy metals show, the binary-metal system triggered the distinct effect on metal extractability relative to single application (Refaey et al., 2017). The sorption capacities of Zn and Cu were found to be 6-times lower for combined treatment in comparison to single application in sediments (Seo et al., 2008). In the case of the mixtures of ENPs characterized by different properties (e.g. oxidation state, solubility, surface charge), more complex interactions between ENPs as well as ENPs and soil constituents are expected than for individual treatment (Lopes et al., 2016). Moreover, the co-existence of ENPs may trigger specific co-ecotoxicity pattern (Deng et al., 2017). Our previous studies on the binary mixtures of ENPs in water (Jośko et al., 2017) and soil (Jośko and Oleszczuk, 2013) indicated the reduction of phytotoxicity compared to individual exposure. However, there is no data on the combined effect of ENPs on soil invertebrates such as collembolans, which are an important component of the soil system (Fountain and Hopkin, 2005). Folsomia candida, the abundant and widespread soil species participating in decomposition and mineralization process, is commonly used model organism in ecotoxicological studies examining wide range of chemicals including ENPs and heavy metals (Kool et al., 2011; Neves et al., 2019; Noordhoek et al., 2018; Vijver et al., 2001; Waalewijn-Kool et al., 2013a, 2013b; Oleszczuk et al., 2019). To date, the effect of individual ENPs on these springtails has been mostly evaluated at level of reproduction (Kool et al., 2011; Neves et al., 2019; Noordhoek et al., 2018). The half maximal effective concentration (EC50) of 1964 mg Zn kg−1 for nano-ZnO was measured (Kool et al., 2011), while no effect of nano-CuO on reproduction of F. candida was found at concentration up to 6400 mg kg−1 (Noordhoek et al., 2018). In turn, EC50 values was a few times lower for ZnCl2 and CuCl2 treatment (Kool et al., 2011; Noordhoek et al., 2018). Opposite to ENPs, the joint toxicity of Zn and Cu towards F. candida was evaluated in the previous studies (Renaud et al., 2020; Vijver et al., 2001), which reported additive or antagonistic effect of heavy metals. A question arises if the joint effect of ENPs will have the same direction as metal salts.
To narrow the above-mentioned knowledge gaps, this study was designed to examine the potential metal availability and ecotoxicity under combined treatment of Zn- and Cu-based ENPs (metal and metal oxide). Ionic Zn and Cu (metal sulfates) treatments were tested for comparison. Because there is a lack of recommendations for the measuring of metal availability during ENPs exposure, four methods of metal extraction were tested. The potential available metal concentrations were determined in soil pore water as well as in soil using H2O, CaCl2 and DTPA as extractants. The used extraction methods allow to measure the concentration of dissolved (H2O), cation-exchangeable (CaCl2) or bound with carbonates and organic ligands (DTPA) metals in soil (Sahuquillo et al., 2003). The stronger extractants – CaCl2 and DTPA – mirror the soil chemistry considered as “readily available” (Gao et al., 2018) and correspond with the metal complex with soluble and solid ligands in soil environment (Jośko et al., 2021a), respectively. The potential availability of metals from ENPs and metal salts was compared with the toxicity towards the springtail Folsomia candida, which are recommended by the OECD for toxicity soil testing (Fountain and Hopkin, 2005). To investigate how soil properties may affect the potential effect (extractability, toxicity), two standard soils with contrasting properties were used. Considering that the fate of ENPs is time-dependent, the extractability and ecotoxicity were evaluated day after application of ENPs to soil and after 90 days of ENPs–soil incubation. Potential links between the metal extractability pattern and ecotoxicological endpoints may be helpful for risk evaluation of co-exposure of ENPs to soil biota.
Section snippets
Materials
Metal nanoparticles (nano-Cu; nano-Zn) and metal oxide nanoparticles (nano-CuO; nano-ZnO) (purity ≥95.5%) were purchased from Sigma-Aldrich (USA). ZnSO4 and CuSO4 (purity ≥95.5%) were also applied to compare effects of particulate (ENPs) and ionic compounds (metal salts). The primary particle size of ENPs determining with a transmission electron microscope (JEM–3010 TEM JEOL, Ltd., Japan) was and 25 ± 10 nm (nano-Cu), 40 ± 20 nm (nano-Zn), 50 ± 10 nm (nano-CuO), and 100 ± 25 nm (nano-ZnO). TEM
Changes of pH and ζ-potential values in soil after single or joint treatment with ENPs
Application of ENPs increased the soil pH to a level of 6.1–6.4 (LUFA 2.2.) and 6.2–6.7 (LUFA 2.3.) (Fig. 2A). Several studies have previously observed an increase in the pH value after application of ENPs to soil (Romero-Freire et al., 2017; Waalewijn-Kool et al., 2013a, 2013b) (Noordhoek et al., 2018) and it is associated with the consumption of H+ ions driven by the dissolution of ENPs (McManus et al., 2018). The pH did not differ significantly between single or joint treatment with ENPs (
Conclusions
The effect of co-existing ENPs on their metal component extractability and toxicity was here reported. Contrary to metal salts, the combined effect on Zn and Cu extractability for the ENPs mixtures was not unidirectional and depended on the extraction method, soil type and aging. Most of the joint effects on metal extractability occurred in aged samples using DTPA extraction. The direction of the combined effect on the extractability of Zn and Cu was also soil type-dependent. The joint effect
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgments
This study was supported by National Science Centre (Poland) in the frame of SONATA grant (2017/26/D/NZ9/00067).
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2023, Science of the Total EnvironmentCitation Excerpt :The stimulating effect of Zn on F. candida can be related to properties of Zn as an essential element responsible for many process in the living organisms (Sharma et al., 2013). This metal can be toxic in high concentration (Amorim et al., 2012) but in appropriate level may stimulate or regulate the organisms growth (Jośko et al., 2022). It was previously observed that Zn may improve the growth of F. candida, and their body size (Jośko et al., 2022).