Partitioning and stability of ionic, nano- and microsized zinc in natural soil suspensions

Science of the Total Environment 700 (2020) 134445

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Partitioning and stability of ionic, nano- and microsized zinc in natural soil suspensions Martin Šebesta a,⇑, Lucia Nemcˇek a, Martin Urík a, Marek Kolencˇík b,c, Marek Bujdoš a, Ivo Vávra d, Edmund Dobrocˇka d, Peter Matúš a a

Institute of Laboratory Research on Geomaterials, Faculty of Natural Sciences, Comenius University in Bratislava, Ilkovicˇova 6, 842 15 Bratislava, Slovakia Department of Soil Science and Geology, Faculty of Agrobiology and Food Resources, Slovak University of Agriculture in Nitra, Trieda A. Hlinku 2, 949 76 Nitra, Slovakia Nanotechnology Centre, VŠB Technical University of Ostrava, 17. listopadu 15/2172, 708 33 Ostrava, Czech Republic d Institute of Electrical Engineering, Slovak Academy of Sciences, Dúbravská cesta 9, 841 04 Bratislava, Slovakia b c

h i g h l i g h t s

g r a p h i c a l a b s t r a c t

 Micro and nano sized ZnO forms’

behavior was compared to Zn ions in various soils.  Soil pH plays major role in partitioning and size distribution of Zn forms in soils.  Partitioning of particulate ZnO and ionic Zn significantly differ in soil solutions.  ZnO nanoparticles form small aggregates in alkaline soil solutions.

a r t i c l e

i n f o

Article history: Received 4 July 2019 Received in revised form 10 September 2019 Accepted 12 September 2019 Available online 13 September 2019 Editor: Filip M.G. Tack Keywords: Zinc Stability Soil Environmental fate Partitioning Nanoparticle

a b s t r a c t Batch experiments aimed at solid-liquid distribution of 40 nm engineered zinc oxide nanoparticles (ZnONP), microparticles (bulk ZnO), and ionic Zn in ZnSO4 solution were conducted on eight field soil samples of different characteristics to identify how the form of Zn affects its distribution in soil. The concentration of Zn in different size fractions present in supernatant solutions obtained from centrifuged soil suspensions was also measured. The distribution between a liquid and a solid was different for the ionic Zn (ZnSO4) and particulate Zn (ZnO-NP and bulk ZnO). In acidic soil solutions, the partitioning coefficient (KdA) of the ionic Zn was in range of 14.7–15.9 compared to 133.4–194.1 for ZnO-NP and bulk ZnO. The situation was reversed under alkaline conditions resulting in a decreased retention of particulate forms of Zn by the solids, with ZnO-NP showing KdA of 8.5–23.4 compared to 160.0–760.1 of ionic Zn. Soil pH thus appears to be the predominant factor influencing the solid-liquid distribution of Zn in different forms. Even the distribution of Zn in different size fractions is heavily affected by the soil pH, causing dissolution of ZnO-NP and bulk ZnO in acidic soils. In alkaline soils, applied ionic Zn (ZnSO4) remained dissolved. This study shows that ZnO-NP are the most mobile of the three tested forms of Zn in alkaline soils. This may affect the spatial distribution of Zn in soil and potentially increase the effectivity of the application of Zn fertilizer when in nanoparticle form. Ó 2019 Elsevier B.V. All rights reserved.

⇑ Corresponding author at: Ústav laboratórneho vy´skumu geomateriálov, Prírodovedecká fakulta, Univerzita Komenského v Bratislave, Ilkovicˇova 6, 84215 Bratislava, Slovakia. E-mail address: [email protected] (M. Šebesta). https://doi.org/10.1016/j.scitotenv.2019.134445 0048-9697/Ó 2019 Elsevier B.V. All rights reserved.

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1. Introduction In the past two decades, engineered nanomaterials found use in numerous applications, e.g. in electronics, catalysts, ceramics, renewable energy, antimicrobial materials, pharmaceuticals, and agriculture (Piccinno et al., 2012). However, an extensive production and use of engineered nanoparticles (NP) have increased the risk of their unintentional release to the environment, which raises concerns about potential toxic effects on the environment and human health. Soils along with surface waters represent major sinks for released NP. Thus, it is important to gain knowledge about the processes governing their mobility and transformation in the soil environments (Cornelis et al., 2014; Peijnenburg et al., 2016). The soil comes in contact with NP in two ways. Unintentionally, engineered NP may be applied onto soil with activated sludge used as a fertilizer or they are deposited from the atmosphere. Intentional direct application is another pathway. Engineered NP are used in soil remediation, and there are plans to use engineered NP as carriers for agricultural active substances or use them directly as a source of important macro- and micronutrients for crops. With the rising interest in using nanotechnology in agriculture to enhance growth, productivity and protection of the crops, an intentional release of engineered NP may play a bigger role in soil contamination than unintentional ones in the future (Korˇenková et al., 2017; Prasad et al., 2017; Raliya et al., 2017). ZnO in both bulk and nano forms has been widely used in a broad range of industrial and commercial applications with estimated global annual production of 1377 kilotons in 2014 (MarketsandMarkets, 2015), of which nanosized ZnO has been produced in amounts of approximately 30 kilotons (Future Markets Inc., 2016). Agricultural land is at an ecological risk of ZnO-NP contamination. By estimate, up to 8.7 kilotons of ZnO-NP can end up in soils unintentionally, mainly through their release from activated sludge applied to land (Cornelis et al., 2014; Keller et al., 2013; Peijnenburg et al., 2016). These NP enter the soil either unchanged or transformed to some degree. During wastewater treatment, an anaerobic digestion of wastewater rich in phosphates and sulfide may result in the formation of ZnS and produced aged activated sludge may also show the presence of Zn phosphates and Zn bound to iron oxyhydroxides (Lombi et al., 2012; Ma et al., 2014). The future is likely to bring an increase in direct applications of ZnONP as they are viewed as a potential micronutrient nanofertilizer (Liu and Lal, 2015). Applied either directly to the soil or by foliar application they may pose potential danger, although at right concentrations they have been shown to enhance plant growth (Medina-Velo et al., 2017; Raliya et al., 2016). Generally, the mobility of Zn forms in soils, including ZnO-NP, is mostly affected by factors like pH and the content and quality of clay minerals, oxyhydroxides of Al, Fe, Mn, and organic matter (Kabata-Pendias and Szteke, 2015; Rajput et al., 2018; Šebesta et al., 2019). Other, specific processes affecting the mobility of Zn contained in ZnO-NP in the soil environment include (1) release of Zn by partial or full dissolution of ZnO-NP; (2) homoaggregation of ZnO-NP or heteroaggregation with natural colloids; and (3) surface transformation of ZnO-NP by humic acids or dissolved ions present in the soil solution. These three processes are affected by pH (Peng et al., 2017; Wang et al., 2013), concentration and type of dissolved organic matter (Mohd Omar et al., 2014; Tang et al., 2014), and by water chemistry (Bian et al., 2011; Odzak et al., 2014). The intrinsic properties of ZnO-NP also influence their mobility in soil and water environments, namely their particle size and shape (Bian et al., 2011), concentration (Yung et al., 2015), and surface coating (Sivry et al., 2014). In studies conducted on the transport and retention of ZnO-NP in soils, concentration of unbound Zn to soil was measured as the

total concentration of Zn after digestion of the sample (Sun et al., 2015; Zhao et al., 2012). The form of an element, particulate or ionic, affects the mobility in soil and attachment to soil particles. Both ionic and particulate forms of an element can be cotransported with natural organic and inorganic colloids affecting the transport and bioavailability of the element in soils. This can lead to both underestimation or overestimation of the element’s mobility (Cornelis et al., 2013; Gavrilescu, 2014; Šimu˚nek et al., 2006). In soil solution, a distribution of an element in different size fractions thus provides a deeper understanding of behavior of the element under different environmental conditions. This knowledge can help with prediction of mobility and bioavailibility of the element in different physico-chemical forms. Our study examines the solid-liquid partitioning of ZnO-NP in eight soil samples and compares these experiments with partitioning of bulk ZnO and ionic Zn (ZnSO4). There were two main aims of the experiments: (1) To show the difference in partitioning of different physicochemical Zn forms and to (2) explain the solid-liquid partitioning between soil and soil solution and size partitioning of the studied Zn forms in soil solution as affected by soil characteristics. High concentrations were used to examine the difference in attachment of ionic vs particulate forms of Zn in soils and to provide information on particle size of the free forms or aggregates of ZnO-NP and bulk ZnO in soil solutions and attachment of ionic Zn to soil colloidal particles. Attachment of particles and ions to soil as well as the particle size play an important role in distribution of the constituent elements in soil and their bioavailability to soil organisms. We separated solutions into four size fractions in order to model different situations that lead to different scenarios occurring in the soil environment. Particles below 1000 nm belong to colloidal fraction with the ability to be transported in larger soil pores thus contributing to the spatial distribution of elements in the soil profile. Size below 450 nm is an operational divide. In older literature, materials passing through a 0.45-lm pore sized membrane filter were considered to be dissolved (Horowitz et al., 1992; Nowack and Bucheli, 2007). Size below 100 nm represents the nanoparticulate fraction easily accessible to soil organisms, and finally the dissolved fraction (below 1 nm) that is readily available to soil organisms. 2. Material and methods 2.1. Artificial rainwater All batch experiments were conducted in a background electrolyte with concentrations of ions typical for the Slovak rainwaters. The values of concentrations of mono- and divalent cations and anions were chosen based on the average of five-year measurements (2011–2015) made at five meteorological stations (SHMÚ, 2019). A thousandfold concentrated solution of artificial rainwater was prepared and the concentrations of chemicals added were as follows: 0.2705 g.L 1 of NaCl, 1.2397 g.L 1 of (NH4)2SO4, 0.3044 g.L 1 of NaNO3, and 1.5096 g.L 1 of Ca(NO3)2. 2.2. Soils used in the experiments The topsoil samples with different characteristics were collected from eight separate sites within wider Western Slovakia region at depth ranging between 5 and 15 cm. The soils were classified according to Morphogenetic Soil Classification System of Slovakia (Societas Pedologica Slovaca, 2014) and World Reference Base for Soil Resources (WRB) (IUSS Working Group WRB, 2015) as Cernozem kultizemna karbonatova/Calcic Chernozem (CH-cc), Ciernica kultizemna karbonatova/Calcaric Mollic Gleysol (GL-mo. ca), Fluvizem kultizemna karbonatova/Calcaric Gleyic Fluvisol

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(FL-gl.ca), Kambizem luvizemna pseudoglejova/Dystric Stagnic Cambisol (CM-st.dy), Rendzina modalna/Dolomitic Rendzic Leptosol (LP-rz.do), and Kambizem modalna/Dystric Cambisol (CM-dy). For simplicity, samples are designated as S1–S8. The characteristics of the eight soils are shown in Table 1 and the soils are ordered from the most alkaline (S1) to the most acidic (S8). Total concentrations of Al, Fe, Mn and Zn were determined after decomposition of 1 g of soil by acid mixture of HF + HNO3 + HClO4 + H2O2 (4:3:4:1, 60 mL) in an open system at 200 °C. The oxalate extractable forms of Al, Fe and Mn in fine earth ground to a particle size <0.5 mm were extracted with 0.2 M ammonium oxalate at pH 3 (McKeague and Day, 1966) and their contents were measured using flame atomic absorption spectrometry (FAAS) (Perkin-Elmer 1100, Perkin-Elmer, Waltham, MA, USA). Total organic carbon (TOC) was determined according to Walkley and Black (1934). Soil pH was measured potentiometrically in 1 M KCl and in deionized water with a 1:2.5 soil to solution ratio. CaCO3 content was measured volumetrically using Janko’s calcimeter. A pipette method was used to determine the soil particle size distribution (Fiala et al., 1999). Based on the percentages of sand (2–0.05 mm), silt (0.05–0.002 mm) and clay (<0.002 mm), samples were then classified to textural types by reference to the USDAFAO soil-texture triangle (FAO, 2006). A method developed by Kononova and Belcˇikova (1962) was used to determine the amount of humic substances, humic acids, and fulvic acids. The soil cation exchange capacity (CEC) was measured by method of Kappen (1929).

dispersion and 250 mL of a thousandfold concentrated artificial rainwater into 250 mL volumetric flasks that were then diluted to the mark with distilled water to obtain NP suspensions with concentration of 65, 196, 327, 523 and 654 mg Zn.L 1, respectively. These NP suspensions were sonicated for 15 min in an ultrasonic bath. The time of sonication of 15 min was selected, since longer or shorter times led to increased aggregation. The preliminary experiments showed that during batch experiments with concentrations of ZnO-NP lower than 65 mg.L 1 nearly all of ZnO-NP were attached to the soil. For the purpose of observing size distribution of Zn forms in supernatant and to assess the attachment of different Zn forms to soil, concentrations above 65 mg Zn.L 1 were used, following the OECD Guidelines for the Testing of Chemicals, Test No. 106 with regards to selection of initial concentrations and solid to liquid ratio, where at least 20% of the applied element should remain in supernatant (OECD, 2000). Thus the range corresponding to 1 to 10 mmol Zn.L 1 was employed for all batch experiments. The ZnO-NP suspensions were prepared shortly before the batch experiments. A 0.1 mol.L 1 ZnSO4 stock solution was prepared by dissolving 7.189 g of ZnSO4
7H2O (p.a quality, CentralChem, Slovakia) in 250 mL of distilled water. Solutions of ZnSO4 with concentrations of 65, 196, 327, 523 and 654 mg Zn.L 1 were prepared by placing 7.5, 22.5, 37.5, 60 and 75 mL of 0.1 mol.L 1 ZnSO4 stock solution, respectively, into 250 mL volumetric flasks, then 250 mL of the thousand-fold concentrated artificial rainwater was added and the flasks were made up to the mark with distilled water.

2.3. ZnO nanoparticle suspensions and ZnSO4 solutions

2.4. Characterization of ZnO nanoparticles and the bulk ZnO

Zinc oxide nanoparticles (ZnO-NP) were purchased from Sigma Aldrich (product number 721077) in a form of aqueous dispersion. The obtained ZnO-NP dispersion was used to prepare NP suspensions by placing 102, 306, 510, 816 and 1020 mL of the ZnO-NP

Images, morphology and particle size of the ZnO-NP and bulk ZnO were obtained by means of Transmission Electron Microscopy (TEM) carried out on the JEOL 1200 EX (JEOL Ltd., Tokyo, Japan), operating at 120 kV. Samples were diluted in distilled water, then

Table 1 Characteristics of soil samples used in sorption experiments. Soil samples

S1

S2

S3

S4

S5

S6

S7

S8

Soil code (IUSS Working Group WRB, 2015) Location Land use Texture Sand [%] Silt [%] Clay [%] TOC [%] HS [%]a HA [%]b FA [%]c pHH2O pHKCl CaCO3 [%] Tot Al [mg.g 1]d Tot Fe [mg.g 1]d Tot Mn [mg.g 1]d Tot Zn [mg.g 1]d Ox Al [mg.g 1]e Ox Fe [mg.g 1]e Ox Mn [mg.g 1]e CEC [mmol.kg 1]f

CH-cc

GL-mo.ca

LP-rz.do

LP-rz.do

FL-gl.ca

CM-dy

CM-dy

CM-st.dy

Senec Crop loam 34.3 45.8 19.9 2.82 1.12 0.53 0.59 7.98 7.45 3.3 51.8 25.7 604 82.4 0.92 1.27 0.39 484

Saliby Crop sandy loam 68.2 14.4 17.4 1.66 0.45 0.31 0.14 7.82 7.09 3.3 58.2 28.0 465 99.7 1.10 2.95 0.23 500

Brezova pod Bradlom Forest loamy sand 84.2 12.6 3.2 6.20 2.00 0.19 1.81 7.82 7.30 41.6 26.2 14.0 632 47.4 3.21 1.51 0.39 480

Dobra Voda Forest loamy sand 84.8 12.6 2.6 7.47 2.70 0.17 2.53 7.61 7.16 59.0 12.1 6.3 612 49.0 2.49 1.26 0.38 499

Saliby Crop loam 33.0 42.8 24.2 1.65 0.73 0.37 0.36 7.58 7.32 18.1 65.6 32.7 457 95.5 1.06 2.14 0.11 494

Banska Stiavnica Grass loamy sand 57.7 27.3 15.0 3.00 0.76 0.20 0.56 5.02 3.69 0.1 80.5 58.3 1720 217.0 2.27 3.69 1.38 226

Banska Stiavnica Grass loam 49.6 39.3 11.1 5.82 2.01 0.66 1.35 4.42 3.45 0.0 61.5 31.9 600 177.0 2.39 4.65 0.45 281

Stara Tura Forest loamy sand 79.2 16.4 4.5 4.73 2.48 0.79 1.69 4.10 3.40 0.4 44.6 16.2 318 142.0 1.56 2.97 0.32 291

CH-cc – Calcic Chernozem, GL-mo.ca – Calcaric Mollic Gleysol, FL-gl.ca – Calcaric Gleyic Fluvisol, LP-rz.do – Dolomitic Rendzic Leptosol, CM-st.dy – Dystric Stagnic Cambisol, CM-dy – Dystric Cambisol. a Humic substances. b Humic acids. c Fulvic acids. d Total concentration in the soil sample. e Oxalate-extractable phase of the element. f Cation exchange capacity.

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an appropriate amount of specimen suspension was placed on a carbon grid and examined using a TEM. Crystalline symmetry and structural parameters of ZnO-NP and bulk ZnO (p.a. quality, Chemapol, Prague, Czech Republic) were obtained by X-ray powder diffraction (XRD) using Bruker D8 DISCOVER diffractometer (Bruker, Billerica, MA, USA) equipped with X-ray tube with rotating Cu anode operating at 12 kW (40 kV, 300 mA). A parallel beam geometry with parabolic Goebel mirror in the primary beam was used in all measurements. Grazing incidence set-up with an angle of incidence a = 1.5° was used for recording the diffraction patterns in the angular range of 20–80° of 2h. Parallel plate collimator with the angular acceptance of 0.35° was inserted in the path of diffracted beam. The crystallite size was calculated using the Lvol-IB method (volume mean column height calculated from the integral breadth) (Uvarov and Popov, 2013). 2.5. Batch partitioning experiment with different concentrations and forms of Zn on S1, Calcic Chernozem (CH-cc) Batch experiment on S1 (characteristics shown in Table 1) was conducted using NP suspensions, bulk ZnO powder and solutions of ZnSO4 with initial concentration (C0) of 65, 196, 327, 523 and 654 mg Zn.L 1. A 790 mg of soil was placed into 15 mL centrifuge tubes and then 15.8 mL of either ZnO-NP suspension or ZnSO4 solution was added. When bulk ZnO was applied, 1.3, 3.9, 6.5, 10.4 or 13.0 mg of bulk ZnO was placed into centrifuge tube with soil and subsequently 15.8 mL of artificial rainwater was added. The tested soil to solution ratio was 1:20. The so-filled centrifuge tubes had little to no air space to diminish the effect of sorption on air-water interface. There was also a control experiment performed without any added Zn. Each concentration and form of Zn in soil was run in duplicate. Sealed centrifuge tubes were shaken on an overhead shaker at 5 rpm. After 24 h they were removed and sequentially centrifuged at 700g for 1 min, at 3500g for 1 min, and 3500g for 20 min to separate Zn particle aggregates into size fractions <1000 nm (A), 450 nm (B), and 100 nm (C), respectively. Selected centrifugal forces and times were calculated according to the Stokes’ law equation for particles made of ZnO (Gibbs et al., 1971; Schwertfeger et al., 2017). After each centrifugation, 1 mL of supernatant was collected to be analyzed for the concentration of Zn by FAAS. After the sequential centrifugation, 5 mL of supernatant were transferred to the centrifugal ultrafiltration units (Vivaspin 6 centrifugal concentrator, 3 kDa molecular weight cut off (MWCO) membrane, Sartorius, Germany) and were centrifuged at 3500g for 20 min. The selected cellulose membrane only passes particles below 1.2 nm in size, effectively letting only dissolved elements and small dissolved molecules pass through. A 1 mL of filtrate was taken to be analyzed for the concentration of Zn by FAAS to determine the dissolved fraction (D). From measured concentrations of Zn in size fractions A < 1000 nm (CA), B < 450 nm (CB), C < 100 nm (CC), and dissolved, D < 1 nm (CD), Zn concentrations in size fractions of 450–1000 nm (Ca = CA CB), 100– 450 nm (Cb = CB CC), 1–100 nm (Cc = CC CD) and the dissolved fraction <1 nm (Cd = CD) were calculated. The Zn bound to the soil (Sa) was calculated as a difference between the initial concentrations (C0) and fraction below 1000 nm (CA), SA = C0 CA. Size fraction C represents Zn bound to NP forms and follows the convention of NP having dimensions between 1 and 100 nm. Fractions a and b have a divide at 450 nm. This is the operational divide, since in older literature only those materials which pass through a 0.45lm pore-sized membrane filter were considered to be dissolved (Horowitz et al., 1992; Nowack and Bucheli, 2007). Centrifugal separation was chosen over filtration, as an excessive number of NP smaller than the pore size of selected membrane filters was found to be bound to them (Schwertfeger et al., 2017; Šebesta and Matúš,

2018; Van Koetsem et al., 2017). A table of distribution coefficients and graphs of concentration in liquid phase vs in solid phase were calculated a constructed as detailed in the SI (Fig. SI1, Table SI1). 2.6. Batch partitioning experiment on selected soils of wider western Slovakia region A concentration of 196 mg Zn.L 1 as either bulk ZnO, ZnO-NP suspension or ZnSO4 solution was used to compare the solidliquid partitioning between Slovak soils of wider western region (S2–S8, see Table 1). Again, 0.79 g of each studied soil was placed into 15 mL centrifuge tube and then 15.8 mL of either ZnO-NP suspension or ZnSO4 solution was added. For bulk ZnO, 3.9 mg of bulk ZnO powder was mixed with soil and then 15.8 mL of artificial rainwater was added. A control with no Zn application was also included, prepared by placing 0.79 g of each soil treated with 15.8 mL of artificial rainwater into the centrifuge tube. The experiment and the analysis for the concentration of Zn were run the same way as described for batch experiment on S1 soil suspensions with different concentrations and forms of Zn (see Section 2.5). For each soil sample, a parallel control experiment without any added Zn was carried out simultaneously. Table of distribution coefficients was calculated and constructed in the same way as detailed in the SI for soil S1 (Table SI2). 2.7. Data processing SAS Studio (SAS Institute Inc., Cary, NC, USA) was used for analysis of variance (ANOVA) to evaluate differences in the retention or distribution of Zn in different size fraction in supernatant between different forms of Zn in the S1 soil. Normality of data was checked by Shapiro-Wilk’s test. When the data did not pass normality test, Kruskal-Wallis test was used. Levene’s test for homogeneity of variances was used. In case of violation of homogeneity of variances, Welch’s ANOVA was used. The source of significant mean differences was examined via Tukey’s post-hoc test for samples passing tests of normality and Dwass, Steel, Critchlow-Fligner Method for non-parametric data. Pearson’s correlation coefficients were calculated to find correlations between retention of applied Zn forms in soils or distribution of Zn in different size fractions in supernatant and soils parameters. 3. Results 3.1. Soil characteristics Physical and chemical properties of eight soil samples used in the experiments are presented in Table 1. Three samples, S1, S2, and S5, were taken from agricultural land that has been largely used for crop production. They contain the highest amounts of clay material. Samples S3 and S4 were collected in an oak-hornbeam forest in the Little Carpathians. These soils have a high content of CaCO3 and the highest content of total organic carbon among the soils. The soils from grassland sites (S6 and S7) were collected in Banska Stiavnica surrounding area. The bedrock underneath these soils is formed of andesite lava flows causing the overlying soils to have a naturally low pH. Soil S8 was collected in forested area on sandstone flysch bedrock and, thus, has a naturally low pH. 3.2. Characterization of ZnO nanoparticles and the bulk ZnO TEM images of bulk ZnO and ZnO-NP show the size difference between the two (Fig. 1). The size of the ZnO-NP corresponds to the size declared by the manufacturer with particle size distribution 10–70 nm. Bulk ZnO mainly comprises particles sized

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Fig. 1. TEM images of (A) ZnO-NP and (B) bulk ZnO.

between 100 nm and 500 nm, measured in the shortest dimension, with some particles with a diameter of well over 1000 nm. XRD diffractograms show that both bulk ZnO and ZnO-NP have a crystalline symmetry of the mineral zincite with wurtzite structure (Fig. 2). The calculated grain size Lvol-IB (volume mean column height calculated from the integral breadth) for well-defined crystalline grains of bulk ZnO and ZnO-NP was calculated to be 124 and 16 nm, respectively. The grain size of zinc oxide crystallite determined from XRD diffraction patterns appears smaller than in TEM images. 3.3. Batch partitioning experiment on Calcic Chernozem (S1), with different concentrations of Zn forms A batch experiment involving five different concentrations (65, 196, 327, 523 and 654 mg Zn.L 1) of three different forms of Zn (ZnSO4, ZnO-NP, bulk ZnO) was conducted on Calcic Chernozem (S1). This concentration range was applied to (1) identify the amount of initial Zn for at least one of the Zn forms that reaches

the retention value close to 50%, and to (2) see if the relative amount of Zn in different size fractions changes with initial concentration. The results of this experiment are summarized in Fig. 3A, showing the distribution of Zn between the solid and solution phases together with Zn concentration in different size fractions in the supernatant, with liquid phase divided into four sections representing the relative concentrations of Zn in four size fractions (Ca) 450–1000 nm, (Cb) 100–450 nm, (Cc) 1–100 nm, and (Cd) dissolved <1 nm. In Fig. 3B, only Zn concentration in different size fractions in supernatant is shown. Sorption isotherms where different size fraction (CA, CA, CC, or CD) is taken as the concentration of Zn in liquid phase and thus obtained distribution coefficients Kd can be viewed in the supplementary information (Fig. SI1, Table SI1). The highest relative contents of Zn in soil and also highest Kds were found at the lowest initial concentration (65 mg Zn.L 1) for all three forms of the element. All samples also show a similar trend of a continuous decrease of relative Zn content in solid phase

Fig. 2. X-ray diffraction patterns of bulk ZnO and ZnO-NP. The peaks are typical for the mineral zincite with wurtzite structure.

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Fig. 3. (A) Distribution of Zn between solid (S1, Calcic Chernozem (CH-cc)) and liquid after the batch experiment, with liquid phase classified into four different size categories. (B) Distribution of Zn in supernatant after the batch experiments. The part representing the liquid phase is sub-divided into four component bars representing the size fractions (Ca) 450–1000 nm, (Cb) 100–450 nm, (Cc) 1–100 nm, and (Cd) dissolved fraction below 1 nm. (SA) represents Zn bound to the soil complex and non-bound Zn sized over 1000 nm.

with an increasing concentration of the metal in the initial suspensions. The more efficient binding of bulk ZnO to soil compared to its nanosized form can be most likely attributed to the sedimentation of large particles the ZnO powder is largely comprised of. In the batch experiment with ZnSO4, ionic Zn has higher retention and KdA in soil compared to those either in ZnO-NP or bulk ZnO suspensions. Test for differences in variance has shown that the retention of the three forms of Zn is significantly different and the source of difference is between ZnSO4 vs. ZnO-NP and ZnONP vs bulk ZnO (Table SI3). Fig. 3B highlights that the supernatants obtained from suspensions of soils treated with three different forms of Zn show significant differences (Table SI2). In collected supernatant from ZnSO4 treatments, most of the applied Zn remained dissolved even after the batch experiment was over. Analysis of the bulk ZnO supernatant showed that major portion of suspended particles were in the size range of 450–1000 nm. This was to be expected, since most Zn in bulk ZnO is a part of particles that are larger than 450 nm.

The ZnO-NP form mainly homo- and/or heteroaggregates of 100–450 nm in size and, to a smaller degree, aggregates of 450–1000 nm in size. 3.4. Batch partitioning experiment on selected soils of wider western Slovakia region Based on the results obtained in the previous experiment, the concentration of 196 mg Zn.L 1 was used for the experiments with the remaining seven soil samples. This concentration was employed since the concentration of 65 mg Zn.L 1 had a too high retention (90%). Also, the relative amounts of Zn for ZnO-NP in different size fractions were very similar in concentration range 196–653 mg Zn.L 1. In Fig. 4A, the solid-liquid distribution of Zn is shown. The distribution of Zn in four different size fractions in supernatants collected from eight soil samples is shown in Fig. 4B. The soils are ordered from left to right according to decreasing pH.

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Fig. 4. (A) Distribution of Zn in solid and liquid phases and (B) in supernatant of eight soil samples after the batch experiments. The part representing the liquid phase is divided into four segments representing the size fractions (Ca) 450–1000 nm, (Cb) 100–450 nm, (Cc) 1–100 nm, and (Cd) dissolved fraction. (SA) represents the Zn bound to the soil complex and non-bound Zn sized over 1000 nm. The soils are ordered from left to right according to decreasing pH with S1 being the most alkaline and S8 the most acidic soil.

The batch experiments results show apparent difference in the retention of Zn between acidic and alkaline soils. In case of ZnSO4, representing the ionic form of Zn, greater attachment to soil particles was observed in alkaline soils compared to acidic soils and, hence, larger KdA were calculated for alkaline soils. For both ZnO-NP and bulk ZnO the trend was opposite to that of ZnSO4. Zn in these compounds was more prone to be adsorbed onto soil particles when soil pH was acidic with higher KdAs for acidic soils. Regarding ZnO-NP, retention of Zn in alkaline soils was inferior to that of bulk ZnO and ZnSO4, with lower KdAs, showing a similar trend as observed in experiments performed solely on Calcic Chernozem (S1) (Section 3.2). Differences in Zn concentration in different size fractions of suspended particles are discernible between different Zn forms. When Zn was applied in the ionic form of ZnSO4, Zn remained dissolved in all soil solutions at all soil pH values. In experiments with ZnO-NP, Zn was distributed differently in acidic soil suspensions compared to alkaline ones. In acidic soils, ZnO-NP were dissolved,

except for S6, the least acidic of the three cambic soils yet still classified as strongly acidic with soil pH of 5.2, in which most of the Zn formed large aggregates, bigger than 450 nm. In alkaline soils suspensions, Zn unbound to soil was present mainly in form of aggregates with a size distribution ranging from 100 to 450 nm. Fraction of particles between 450 and 1000 nm contained the second highest concentration of Zn in ZnO-NP experiments. Compared to the ZnO-NP particle size distribution, bulk ZnO in supernatants was present in form of large particles around 450 to 1000 nm in size, since the bulk ZnO is comprised mainly of particles larger than 450 nm. Batch experiment results of Zn retention in soils were compared with known soil parameters by Pearson’s correlation coefficient (Table SI3). Four soil characteristics met our fitting criteria, as they had absolute value of Pearson’s correlation coefficient above 0.5 for at least two Zn forms for retention and all size fractions and can be seen in Table 2. Regarding soil characteristics, the highest correlation was found for pH and CEC vs. the retention of ZnSO4, ZnO-NP

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Table 2 Selected correlations of soil characteristics with the retention of ZnSO4, ZnO-NP and bulk ZnO. The first line in each row presents Pearson’s correlation coefficient (r) and the second line shows p-value of significance. Ox Fea [mg.g Retention of ZnSO4 [%] Retention of ZnO-NP [%] Retention of bulk ZnO [%] ZnSO4, Ca, 450–1000 nm ZnO-NP, Ca, 450–1000 nm Bulk ZnO, Ca, 450–1000 nm ZnSO4, Cb, 100–450 nm ZnO-NP, Cb, 100–450 nm Bulk ZnO, Cb, 100–450 nm ZnSO4, Cc, 1–100 nm ZnO-NP, Cc, 1–100 nm Bulk ZnO, Cc, 1–100 nm ZnSO4, Cd, <1 nm ZnO-NP, Cd, <1 nm Bulk ZnO, Cd, <1 nm a b c

r p r p r p r p r p r p r p r p r p r p r p r p r p r p r p

1

]

0.840 0.009 0.710 0.049 0.681 0.063 0.781 0.022 0.297 0.476 0.721 0.044 0.200 0.635 0.718 0.045 0.678 0.065 0.711 0.048 0.137 0.747 0.659 0.075 0.833 0.010 0.254 0.544 0.722 0.043

HAb [%]

pHH2O

CECc [mmol.kg

0.568 0.142 0.585 0.128 0.479 0.230 0.530 0.177 0.665 0.072 0.586 0.127 0.482 0.227 0.639 0.088 0.590 0.123 0.871 0.005 0.449 0.265 0.871 0.005 0.565 0.145 0.081 0.848 0.792 0.019

0.977 <0.0001 0.936 0.0006 0.954 0.0002 0.775 0.024 0.558 0.151 0.969 <0.0001 0.302 0.467 0.940 0.001 0.968 <0.0001 0.874 0.005 0.453 0.260 0.862 0.006 0.977 <0.0001 0.269 0.519 0.903 0.002

0.977 <0.0001 0.937 0.0006 0.924 0.001 0.777 0.023 0.288 0.490 0.901 0.002 0.534 0.173 0.922 0.001 0.908 0.002 0.722 0.043 0.555 0.153 0.683 0.062 0.979 <0.0001 0.252 0.547 0.752 0.031

1

]

Oxalate-extractable phase of the element. Humic acids. Cation exchange capacity.

and bulk ZnO by soil. A strong positive correlation for pH and ZnSO4 retention and negative correlation for ZnO-NP and bulk ZnO retention was found. CEC was strongly correlated with the retention of all three forms of Zn in soils. The CEC is also strongly correlated with pH; therefore, it is not possible to easily distinguish which of these two factors may play a bigger role in retention of the three forms of Zn in studied soils. At least two Zn forms out of three had a statistically significant correlation between Zn retention and CEC, pH and oxalate-extractable Fe, and also between the distribution of Zn in different size fractions in supernatant and CEC, pH, and oxalate-extractable Fe (Table 2). Concentration of CaCO3 and oxalate-extractable Mn showed moderate correlation with the retention of Zn forms in soil, but these correlations did not meet the criteria of statistical significance at a = 0.05. 4. Discussion There is an apparent difference in Zn retention and size fractionation between acidic and alkaline soils (Fig. 4). Two attributes that have contributed to this observation are (1) a higher retention of ionic Zn in alkaline soils where binding sites available to ionic Zn are inaccessible to bulk or nanosized particles due to the surface roughness of soil particles and/or humic acid coating of particulate Zn which may change electrical charge of the particles and their binding site preferences (Šebesta et al., 2017; Treumann et al., 2014); and (2) the behavioral pattern of dissolved Zn has an opposite trend compared to that of ZnO-NP and bulk ZnO with regard to soil pH. It is well documented that the ionic Zn is less mobile at higher pH; it precipitates in the form of carbonates or hydroxides and creates strong bonds with soil oxyhydroxides (Anderson and Christensen, 1988). For particulate forms of Zn, it can be a less

prevalent process and their dissolution is necessary prior to precipitation or sorption. The dissolution is less likely to occur with increasing solution pH which stabilizes ZnO particles (Xu et al., 2016). Furthermore, the sorption of ionic Zn onto humic substances decreases with pH (Havelcová et al., 2009), thus, the contribution of humic substances to the Zn retention in acidic soils is low in comparison with alkaline ones. This is in good agreement with our observations (Fig. 4). The alkaline pH also promotes dissolution of humic substances; and since their affinity towards ZnO-NP and bulk ZnO surfaces is high, they form a surface layer which contributes to disaggregation of Zn particles and their stabilization in soil solutions (Mohd Omar et al., 2014). The newly formed surface layer gives the particles an overall negative charge (Mohd Omar et al., 2014; Šebesta et al., 2019). As soils have generally lower affinity towards negatively charged particles (Brady and Weil, 2008), the alteration of surface charge of Zn particles induces changes in the binding sites to which the particles are attached and decreases soil retention capacity. This results in a lower retention of particulate Zn compared to that of the ionic Zn in alkaline soils (Fig. 4). The experiments with complex matrices such as wastewater and sludge also support this conclusion as the presence of dissolved organic matter enhances ZnO-NP stability by reducing the aggregation of the particles countering the effect of high ionic strength (Zhou et al., 2015). Thus, ZnO-NP tend to be more stable and less reactive in soil suspensions. The stabilizing effect of humic substances on ZnO-NP is also highlighted in Fig. 3, where the size fraction of 100–450 nm particles is dominant in solution with concentration range between 196 and 654 mg.L 1 and it is relative stable regardless of the initial Zn concentration. This is also supported by the previous observations where ZnO-NP preferentially formed the homoaggregates that were around 200 nm in diameter (Šebesta et al., 2019). The

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homoaggregation of ZnO-NP and the stabilization of aggregates by humic acids both significantly affect the condition of particulate ZnO in a solution, thus influencing retention performance. The role of pH in retention and size distribution was the most discernible in our experiment (considering that pH highly correlates with CEC; these two factors are for clarity of discussion taken as an influence of pH, since pH affects CEC). As discussed above, the pH not only directly affects the dissolution of ZnO-NP and bulk ZnO, but also the attachment of particles, sorption of ionic Zn in soils, the surface charge and aggregation of ZnO-NP (Peng et al., 2017). In soils of lower, acidic pH, ZnO-NP can be readily dissolved, and the behavior of released Zn is similar to that of the ionic Zn directly applied to land (Wang et al., 2013). In our experiment, this was preceded by the dissolution of the material and its reprecipitation or sorption on soil surfaces (Zhao et al., 2012), or the ZnO particles experienced an extensive level of homo- and heteroaggregation which resulted in their translocation from suspension to the sedimented phase (Mohd Omar et al., 2014). This behavior is strongly influenced by pH, with higher pH values decelerating the dissolution and transformation of ZnO-NP (Xu et al., 2016), which was clearly visible in soil S6, compared to more acidic soils S7 and S8 (Fig. 4). Higher amount of Zn colloids and a lower content of the ionic Zn in solution may have also resulted from the high content of oxalate-extractable Fe and Mn, which was highest in soil S6. The correlation between oxalate-extractable Fe, Mn and retention of Zn forms cannot be easily explained; it could partially be a result of a moderate positive relationship between oxalateextractable Fe, Mn and pH (Table SI4). Nevertheless, studies conducted on wastewaters highly concentrated with Fe oxyhydroxides reveal that ZnO-NP are bound to the Fe oxyhydroxide surfaces and the resulting complexes are less soluble (Ma et al., 2014, 2013; Rathnayake et al., 2014). The positive correlation of CaCO3 may correspond with formation of ZnCO3 on the surface of the soil’s solid phase (Ma et al., 2014, 2013; Rathnayake et al., 2014). Compared to other commonly studied NP, like Ag-NP, Au-NP and CeO2-NP, the ZnO-NP are affected by the changes in solution pH to greater extend. This is partly because of ZnO-NP’s higher solubility which largely affects its ecotoxicity due to release of Zn ions (Bundschuh et al., 2018). Ag-NP only ever undergo partial dissolution in most of the soil environments and solubility of Au-NP and CeO2-NP is mostly negligible (Cornelis et al., 2011; El Hadri et al., 2018; Van Koetsem et al., 2018). Attachment of Au-NP did not significantly differ at the range of concentrations used, a behavior different from ZnO-NP of this work, though a much lower concentration was used in experiments with Au-NP (0.01–5 mg. kg 1 Au compared to 65–654 mg.L 1 Zn in this work) (El Hadri et al., 2018). Also, since the used concentrations were lower, heteroaggregation was the prevalent form of aggregation compared to ZnO-NP being probably homoaggregated at 196–654 mg.L 1 Zn. Still, at lower concentration (65 mg.L 1 Zn), the heteroaggregation is expected to be more dominant (Fig. 3). Ag-NP and CeO2-NP attached to soil particles to less degree compared to their ionic counterparts, similarly to the behavior of ZnO-NP in more alkaline soils with pH, CEC and organic matter playing important role in attachment of nanoparticles to soil (Van Koetsem et al., 2018). The results implicate that different forms of Zn exhibit different behavior in soil, thus, selection of an appropriate form is significant for their optimal use in agriculture. ZnO-NP may function as a more mobile form of Zn with different distribution in soil compared to the ionic Zn. Hence, they might be a more bioavailable source of Zn in neutral to alkaline soils, with expected slow release of Zn ions by dissolution, rendering ZnO-NP stabilized by soil’s humic acids a preferred form for continuous release of Zn micronutrient to enhance crop growth (Waalewijn-Kool et al., 2013).

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5. Conclusions Processes governing stability and solid-liquid distribution in complex matrices like soils are important to consider when conducting environmental risk assessment of nanomaterials. In this study, the solid-liquid partitioning of Zn in different forms, (ionic Zn, ZnO-NP and bulk ZnO) and the size distribution of Zn in suspended phase was examined to advance our understanding of ZnO-NP behavior and its fate in complex environmental matrices, such as soil and soil solutions. The partitioning in eight soil samples was conducted and there were significant differences in partitioning between ZnO-NP and their ionic counterparts (ZnSO4). ZnO-NP were binding more efficiently to acidic soils (KdA between 133.4 and 194.1) than to alkaline soils (KdA between 8.5 and 23.4). The behavior of ionic Zn was clearly opposite, displaying higher binding to alkaline soils (KdA between 160.0 and 760.1) compared with acidic ones (KdA between 14.7 and 15.9). In acidic soils, ZnONP and bulk ZnO dissolved showing the same size distribution as the ionic Zn. In alkaline soils the size distribution of particles was different for all three forms of Zn, with ZnO-NP mainly forming aggregates of 100–450 nm in size. Ionic Zn remained dissolved fraction (<1 nm) in all soil solutions. Findings of this work contribute to the knowledge of the distribution of NP in soils, and to the growing research documenting how the physico-chemical forms of Zn affect the contamination. It enlarges information for theoretical studies of ZnO-NP behavior, namely aggregation and dissolution in soils that may assist during evaluation of Zn speciation in soil environments. Conducting other, more complex sorption experiments, such as column experiments may provide a better insight into mechanisms of ZnO-NP attachment to soil and how these mechanisms differ from ionic Zn species. Also, the suspended material still has to be studied in more detail with respect to its composition. 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 work has been financially supported by Scientific Grant Agency of the Ministry of Education, Science, Research and Sport of the Slovak Republic and the Slovak Academy of Sciences under the contracts Nos. VEGA 1/0153/17, VEGA 1/0146/18, and Comenius University in Bratislava under the contract No. UK/23/2019. Appendix A. Supplementary data Supplementary data to this article can be found online at https://doi.org/10.1016/j.scitotenv.2019.134445. References Anderson, P.R., Christensen, T.H., 1988. Distribution coefficients of Cd Co, Ni, and Zn in soils. J. Soil Sci. 39, 15–22. https://doi.org/10.1111/j.1365-2389.1988. tb01190.x. Bian, S.-W.W., Mudunkotuwa, I.A., Rupasinghe, T., Grassian, V.H., 2011. Aggregation and dissolution of 4 nm ZnO nanoparticles in aqueous environments: influence of pH, ionic strength, size, and adsorption of humic acid. Langmuir 27, 6059– 6068. https://doi.org/10.1021/la200570n. Brady, N.C., Weil, R.R., 2008. The Nature and Properties of Soils. Pearson Prentice Hall, Upper Saddle River, NJ. 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? Environ. Sci. Eur. 30, 6. https://doi.org/10.1186/ s12302-018-0132-6.

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