Bioavailability and translocation of metal oxide nanoparticles in the soil-rice plant system

Highlights

• Various MONPs altered the soil properties, especially the redox potential.

• DTPA was more suitable for evaluating the bioavailability of MONPs.

• DGT could hardly extract heavy metals from the MONP-amended soil.

• ZnO NPs caused much higher accumulation and translocation of Zn in the rice plants.

Abstract

To determine the bioavailability and translocation of metal oxide nanoparticles (MONPs) in the soil-rice plant system, we examined the accumulation and micro-distribution of ZnO nanoparticles (NPs), CuO NPs and CeO₂ NPs (50, 100 and 500 mg/kg) in the paddy soil and rice plants under flooded condition for 30 days using single-step chemical extraction and diffusive gradients in thin films (DGT) technique combined with micro X-ray fluorescence spectroscopy (μ-XRF). The results show that various MONPs changed the soil properties, especially the redox potential was enhanced to −165.33 to −75.33 mV compared to the control. The extraction efficiency of Zn, Cu and Ce in the paddy soil from high to low was EDTA, DTPA, CaCl₂ and DGT. Moreover, exposure to 500 mg/kg CuO NPs and CeO₂ NPs induced the primary accumulation of Cu and Ce elements in rice roots as high as 235.48 mg Cu/kg and 164.84 mg Ce/kg, respectively, while the Zn concentration in shoots was up to 313.18 mg/kg under highest ZnO NPs with a 1.5 of translocation factor. The effect of MONPs on the plant growth was mainly related to the chemical species and solubility of MONPs. Micro-XRF analysis shows that Zn was mostly located in the root cortex while Cu was primarily accumulated in the root exodermis and few Ce distributed in the root. Pearson correlation coefficients indicate that only DTPA-extracted metals in soil were significantly and well correlated to the Zn, Cu and Ce accumulation in rice seedlings exposed to MONPs. This work is of great significance for evaluating the environmental risks of MONPs in soil and ensuring the safety of agricultural products.

Introduction

Metal oxide nanoparticles (MONPs) have been extensively applied in medical treatment, solar cells, catalysts, semiconductors, wastewater treatment and environmental remediation due to their special physicochemical properties (Chen et al., 2018; Song et al., 2019). The global annual output of MONP production was estimated over 260000 tons (Tolaymat et al., 2017). The substantially increasing production of MONPs has forced people to concern their security issues. MONPs can enter the soil via atmospheric deposition, sewage irrigation, sludge farming, fertilizer application, pesticide spraying and environmental remediation (Hochella et al., 2019; Hong et al., 2013; Lead et al., 2018). Also, the nanoparticle exposure model predicted that >8–28% of MONPs were discharged into soils (Tolaymat et al., 2017). Thus, the soil, especially farmland soil, becomes the sink of nanomaterials in the environment.

Once MONPs are released into the soil, they may undergo a series of transformation, which ultimately determines the bioavailability and toxicity of nanoparticles (NPs). Despite that most of NPs may agglomierate in the soil, MONPs cannot only cause biological toxicity by releasing metal ions and generating reactive oxygen species (ROS), but also can be absorbed by plants, posing a potential threat to human health via transferring in the food chain (Priester et al., 2017; Servin et al., 2017). For instance, Bradfield et al. (2017) found that ZnO NPs and CuO NPs applied in the soil promoted the accumulation of Zn and Cu in sweet potato. Ma et al. (2018) reported that CeO₂ NPs were directly absorbed by the roots and leaves of head lettuce, and further translocated to the digestive gland of snails via the terrestrial food chain. In fact, the environmental risk of NPs largely depends on the bioavailability and chemical species of MONPs in the soil.

MONPs can be taken up by organisms in the soil as released metal ion state and nanoparticle state. How to rapidly and accurately evaluate the bioavailability of MONPs in soil is a critical issue that needs to be solved. Since the transformation of MONPs (such as ZnO NPs and CuO NPs) is significantly affected by pH (Peng et al., 2017a; Peng et al., 2017c), the classical Tessier sequential extraction method and the European Community Bureau of Reference (BCR) sequential extraction method may over-estimate the bioavailability of MONPs in soil. Hence, it is necessary to consider applying more neutral chemical reagents, such as CaCl₂ solution, ethylenediaminetetraacetic acid (EDTA) solution and diethylenetriamine pentaacetic acid (DTPA) mixture to extract heavy metals in the soil to characterize the mobility and bioavailability of MONPs in soil. Moreover, the technique of diffusive gradients in thin films (DGT) can well simulate the process of plant roots absorbing heavy metals, which can be used for in situ collection and determination of the bioavailable concentrations of heavy metals in soil (Wang et al., 2018). However, whether the chemical one-step extraction method combined with DGT can better evaluate the bioavailability of MONPs in soil remains unexplored.

Paddy soil is the most widely distributed agricultural soil in the world, which may suffer from MONP pollution. The hypothesis of this study was that the bioavailability and translocation ability of various MONPs in the soil-rice plant system could be characterized by a good linear correlation between extractable heavy metals from soil and metal concentrations in plants by various extraction methods. In this study, we analyzed the bioavailability of typical MONPs (ZnO, CuO and CeO₂ NPs) in paddy soil by one-step chemical extraction and DGT and investigated the translocation of these MONPs in the soil-rice plant system. Meanwhile, micro-X-ray fluorescence (μ-XRF) method was used to characterize the micro-distribution of elements in paddy soil and plant. The purposes of this study were to gain a rapid and suitable method for analyzing the transformation products of MONPs in soil and to explore the relationship between the physicochemical properties of MONPs and their bioavailability and translocation ability in the soil-rice plant system.