Abstract
The progressive increase in nanoparticles (NPs) applications and their potential release into the environment because the majority of them end up in the soil without proper care have drawn considerable attention to the public health, which has become an increasingly important area of research. It is required to understand ecological threats of NPs before applications. Once NPs are released into the environment, they are subjected to translocation and go through several modifications, such as bio/geo-transformation which plays a significant role in determination of ultimate fate in the environment. The interaction between plants and NPs is an important aspect of the risk assessment. The plants growing in a contaminated medium may significantly pose a threat to human health via the food chain. Metal oxide NPs ZnO and CuO, the most important NPs, are highly toxic to a wide range of organisms. Exposure and effects of CuO and ZnO NPs on soil biota and human health are critically discussed in this study. The potential benefits and unintentional dangers of NPs to the environment and human health are essential to evaluate and expected to produce less toxic and more degradable NPs to minimize the environmental risk in the future.
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Introduction
Nanoparticles (NPs) refer to materials that have at least one dimension in the nanoscale and do not exceed 100 nm. Due to specific characteristics, physical and chemical properties, and high surface–volume ratio, their applications in the industry, for instance, consumer products, agriculture, coatings, cosmetics, chemicals, electronics, optics, environmental remediation, food and packing, fuel additives, energy, textile and paints, next-generation medicine, and plastics, are increasing (Rajput et al. 2017a, b). It is expected that hundreds of types of products are available in the market and many more could appear in the coming future with new characteristics and novel applications. Nano-era began in the late 1990s, and the application of nanomaterials to the environment reached $23.4 billion in 2014. The global market for nanocomposites totaled $2.0 billion in 2017 and is estimated to reach $7.3 billion by 2022, growing at a compound annual growth rate of 29.5% for the period of 2017–2022 (BBC 2018). There are more than 1600 nanotechnology-based consumer products (Vance et al. 2015), and an online database (www.nanodb.dk) lists 3000 products in different categories that contain NPs or nanomaterial (Hansen et al. 2016). The actual figure of the global production of NPs is still unavailable. A recent estimation indicated that more than 200 metric tons of nano-sized Cu and CuO were produced in 2010 and yearly 5500 tons of Zn NPs are produced in the form of a wide range of products (Connolly et al. 2016; Zuverza-Mena et al. 2015). The literature on the basis of data and modeling analysis indicates that production, use, and disposal of various NPs lead to release of thousands of tons of most common NPs (Ag, Al, Ce, Cu, Fe, Si, Ti, Zn) into the environment each year with the majority of them ending up in the soil, directly or through landfills from sludge and other waste (Bundschuh et al. 2018; Gottschalk et al. 2009; Keller et al. 2017; Keller and Lazareva 2013; McGillicuddy et al. 2017). Water and air also get a significantly high amount of share (Keller et al. 2013). The widespread applications of NPs increased scientific attention and became a priority research area in recent years (Keller et al. 2017; Keller and Lazareva 2013; Rajput et al. 2018a; Servin et al. 2017).
The applications of NPs are increasing that also raise the number of issues such as ethical, health and safety, technological, policy and regulatory, and issues related to purposefully releases of NPs into the environment (Bundschuh et al. 2018; Tiede et al. 2016). Even in the absence of acute toxicity, bioaccumulation and long-term exposure of NPs to the plants may have an impact on the food chain, which is unanswered (Tiede et al. 2008).
Metal oxide NPs ZnO and CuO, the most important NPs, possess a mixing characteristic of metal materials and NPs: essential elements with importance in metabolic and physiological processes in plant growth and human beings, wide use in antimicrobials, catalysis and skin products, semiconductors, plastic, glass, ceramics, cement, rubber materials, pigments, paints, food supplements, batteries, nonflammable material, agricultural industries, cosmetics, coatings, environmental remediation, fuel additives, textile industries, and wastewater treatments (Azizi et al. 2017; Rajput et al. 2017b, 2018c ; Sturikova et al. 2018). Applications of engineered NPs in agriculture and medical sectors are found to solve many problems as compared to the conventional approaches (Fernández-Luqueño et al. 2018; Rai et al. 2018; Raliya et al. 2017). Once NPs are released into the soil, they might impact soil physical and chemical properties, interact with other pollutants, form a new novel kind of toxic compounds, and disturb soil microbial functionality, plant growth, and performance (García-Gómez et al. 2018; Loureiro et al. 2018; Rajput et al. 2017b; Soni et al. 2015). Nanoparticles can exist for a long period of time in the soil and act as hazardous materials, which may impose a threat to human health (Assadian et al. 2018; Katsumiti et al. 2018; Mudunkotuwa et al. 2012).
Several studies suggest that CuO and ZnO NPs are highly toxic to a wide range of organisms, especially for plant growth (Adams et al. 2017; Assadian et al. 2018; Katsumiti et al. 2018; Rajput et al. 2018a, c; Servin et al. 2017), and the weathering of these NPs increases bioaccumulation within the terrestrial food chain (Rajput et al. 2018c; Servin et al. 2017). It is assumed that the CuO and ZnO NPs cause toxicity either by releasing ionic forms or by direct interactions with plant cells and tissues (Du et al. 2011; Perreault et al. 2014). However, the mechanism of NPs uptake is not well established. Like heavy metals, the varying impact of NPs on different plant species also depends upon the size, concentration, duration of exposure, plant genotypes, experimental conditions, and synthesis of NPs. CuO and ZnO NPs affected edible plants by inducing changes in seed germination, mineral uptake, modifications in cellular and subcellular organelles structure and ultrastructure, poor root and shoot growth, induce oxidative stress, cell death, increased activity of stress enzymes, photosynthesis, transpiration rate, and DNA damage (Adams et al. 2017; Rajput et al. 2018a, b, d; Zhang et al. 2018c). The accumulation of NPs in edible plant tissues is another concerning issue that could impact human health via the food chain. After interacting with plant roots, the NPs translocate to aerial parts and accumulate in cellular or subcellular organelles. Several microscopic studies exhibit the presence of NPs in different parts of plant tissues (Ahmed et al. 2018; Peng et al. 2015; Rajput et al. 2018a, d).
In the current overview, CuO and ZnO NPs toxicity on soil organism, plants, and human health is discussed, which could help to regulate the application of NPs in agriculture, food industry, and the medical sector. So the hazardous impacts on human health directly or via the food chain can be avoided.
Sources of soil contamination
The widespread use of NPs in a diverse range of products increases the chances to contaminate the environment. The NPs can be released accidentally or intentionally to the air, water, and soil system. Due to tiny size, nanoparticles can float into the air or get transported to another place through the water and ultimately accumulate for a long time in the soil. Tolaymat et al. (2017) suggested four main sources of NPs emission into the ecosystem, namely manufacturing of raw materials, nano-enabled products, product use, and waste management services. The modeling studies estimate NPs in sewage sludge in the range of 107 and 802 mg kg−1 and make up approximately 100 and 1000 t year−1 in Europe (Gottschalk et al. 2009; Piccinno et al. 2012). Anthropogenic and natural activities are the main sources of NPs in the environment (Fig. 1). Nanoparticles get into the cultivated soils due to their wide applications such as nano-fertilizers, pesticides, seed treatment, hydroponic solutions, and agro-films (Cornelis et al. 2014; Keller et al. 2013; Lowry et al. 2012; Mudunkotuwa et al. 2012; Nowack and Bucheli 2007; Strambeanu et al. 2015). Some applications in food ingredients and cosmetic products are the diffuse source of NPs in the soils. Nanoparticles usage in remediation technology can also lead to deliberate release into the environment. Waste treatment plants release NPs as concentrated sludge or water. Cu NPs are used as fungi- and bactericide in agriculture, which leads to toxic effects on aquatic life. It is predicted that more than 95% of Cu released into the environment will enter the soil and aquatic sediments and accumulate up to 500 μg L−1 (Keller et al. 2017). Similarly, Zn NPs are widely used in cosmetics industries, get released to aquatic system (Nowack and Bucheli 2007), and accumulate in sediments (1300 t a−1), in natural and urban soil (300 t a−1), as well as in landfills (200 t a−1) (Bundschuh et al. 2018).
Data based on the modeling analysis indicate that the production, use, and disposal of various metal-based NPs lead to release of thousands of tons of most common metallic NPs into the environment each year with the majority of them ending up in the soil, directly or through landfills from sludge and other waste. Other components of the biosphere, water and air are also receiving the significantly high amount of NPs share (Keller et al. 2017; Keller and Lazareva 2013). Although the estimated concentration of NPs in the environment may not be entirely accurate as the values are indicated by predictive calculations (Sun et al. 2016). Thus, once entered into the environment, CuO and ZnO NPs are expected to undergo a series of bio/geo-transformation that ultimately decides their fates and toxicity. The predicted concentration of ZnO and CuO NPs in the soil and aquatic sediments is indicated in Table 1.
Bio/geo-transformation
Soil is a less dynamic component of the biosphere, has a relatively high capacity for pollutants accumulation than the water and air, and could be a depot for NPs. In soil, NPs pass through bio/geo-transformation. The process of bio/geo-transformation generally involves aggregation, dissolution, sulfidation, ad/absorption, and oxidation–reduction process (Gogos et al. 2017; Lowry et al. 2012; Ma et al. 2014). Aggregation and dissolution of CuO and ZnO NPs are generally influenced by a range of soil factors such as pH, organic matter, ionic species, and colloids (Feng et al. 2016; Peng et al. 2015, 2017). The process of aggregation largely impacts their colloidal stability that is one of the key factors controlling NPs fate and their toxic effects. However, the stability, mobility, and toxicity of ZnO NPs in soil depend on water chemistry, ionic strength, aggregation and sedimentation (Peng et al. 2017). The natural organic matter of soil influences the bioavailability of NPs in the soil through a diversity of mechanisms such as electrostatic interactions, ligand exchange, hydrophobic effect, hydrogen bonding, and complexation (Philippe and Schaumann 2014). Concentration, particle size, surface area, and surface coating are the properties of NPs which further affect dissolution (Peng et al. 2017).
CuO and ZnO NPs are often considered as insoluble, but the presence of organic acids such as citric acid and oxalic acid in soil enhances the dissolution of these NPs, which in turn increases their mobility and bioavailability to plants and soil organisms. These NPs have good solubility at low pH, whereas as the pH increases, its solubility decreases. In acidic/neutral medium, ZnO NPs showed ion-shedding ability which makes them more toxic (Liu et al. 2016). However, the presence of ligands including those with amine functional groups makes CuO NPs soluble at neutral pH also (Wang et al. 2013). The toxicity of these NPs greatly depends on soil pH (Ma et al. 2014; García-Gómez et al. 2018). The increases in toxicity of CuO NPs were observed at different pHs (4.8 and 5.8) of soils and affected root elongation of Hordeum vulgare (Qiu and Smolders 2017). In other study, a strong effect of ZnO NPs was observed in weak acidic (pH 6.0) soils on bacterial communities (Ge et al. 2011). Physicochemical properties such as size, surface area, and soil properties also affect ions dissolution from these NPs. The dissolution of CuO and ZnO NPs is often regarded as a passivation process which increases the solubility of Cu/CuO and Zn/ZnO NPs, resulting in enhanced bioavailability and toxicity (Ma et al. 2014). More dissolution of Cu NPs increases the likelihood that Cu is internalized as Cu2+ ions or in the form of organic complexes (Keller et al. 2017). However, the stability, mobility and toxicity of ZnO NPs in soil depend on water chemistry, ionic strength, aggregation and sedimentation (Peng et al. 2017). Various experiments associate relationship between ions releases and toxicity of these NPs (Chen et al. 2019; Rajput et al. 2017b).
It is revealed that CuO NPs get accumulated in epidermis and exodermis regions of the plants and get precipitated with citrate or phosphate ligands or get bound to amino acids forming Cu–cysteine, Cu–citrate, and Cu3(PO4)2 kind of products or get reduced to Cu(I) (Peng et al. 2015). Cu(I) is a highly redox active species capable of producing hydroxyl radical by Fenton-like reactions. The higher uptake of Zn by Glycine max was observed at 500 mg L−1 ZnO NPs due to lesser aggregation, and an increased aggregation was proposed at high concentrations (1000–4000 mg L−1) due to difficult passage through cell wall pores which reduced the uptake and accumulation of Zn (Lopez-Moreno et al. 2010). The mechanism of bio/geo-transformation of CuO and ZnO NPs passes through several chemical and biochemical processes with soil biota. Thus, NPs present in even smaller quantities have significant biological importance.
Effects on edible plants
Uptake, translocation, and bioaccumulation of CuO and ZnO NPs in plants depend upon the size, chemical composition, shape, and plant anatomy because xylem serves as the most important vehicle in the distribution and translocation of NPs to leaves (Rajput et al. 2018a). The size of CuO and ZnO NPs affects their toxicity by differences in ions dissolution and forms inside the cell, internalization efficiency, and ROS production (Adams et al. 2017; Rajput et al. 2018c). The phytotoxicity threshold concentration in plant tissues is in the range of 200-500 mg kg−1 for Zn and 20-30 mg kg−1 for Cu (Broadley et al. 2007; Marschner 1995). The accumulations of Cu and Zn in crops reduce food and feed quality, and transference to the food chain can cause a serious threat to human health (Rajput et al. 2018; Wang et al. 2017b). The high accumulation of Cu and Zn dissolute by Cu- and Zn-based NPs in roots was found (Da Costa and Sharma 2015; Rajput et al. 2018a). Da Costa and Sharma (2015) observed an increase of 76-fold in Cu content (190.14 mg kg−1) in the whole roots of rice treated with 1000 mg L−1 CuO NPs, whereas Rajput et al. (2018a) found 6.4-fold higher Cu content in leaves of barley than the control treatments. The recent studies on CuO and ZnO NPs accumulation and their toxic effects on plants are summarized in Table 2.
Seed germination is the beginning of a physiological process and is the first step toward the successful establishment of plants. The seed coat acts as a protector, and once it ruptures, the radicle is the first tissue to get direct contact with metals (Kranner and Colville 2011). CuO NPs significantly reduced seed germination in rice seedlings (78.6%), as compared to control (91.6%) (Shaw and Hossain 2013). CuO NPs affected seed germination and root elongation in Lactuca sativa, Raphanus sativus, and Cucumis sativus (Wu et al. 2012). Few studies were conducted to assess the effects of ZnO NPs on seed germination (Rajput et al. 2018c).
It is well understood that NPs enter plant tissues either via root tissues (root tips, rhizodermis, and lateral root junctions) or the aboveground organs and tissues (cuticles, trichomes, stomata, stigma, and hydathodes) as well as through the wounds and root junctions. Since the root is the first target tissue exposed to soil pollutants, it seems that the functional and structural disorders appear more often in root than in the aboveground tissues. The NPs are taken up by roots and could transport to the aboveground tissues through the vascular system, depending on the composition, shape, size of NPs, and anatomy of the plants (Rico et al. 2011). It has been suggested that the plants can accumulate NPs in their original form or as metal ions (Cota-Ruiz et al. 2018). In studies, CuO NPs showed 5% and 13% decrease in root and shoot lengths, respectively, of wheat and exhibited necrosis in roots, which as a result were thinner and more brittle compared to the control (Dimkpa et al. 2012). The lateral root growth of Arabidopsis thaliana a model plant was inhibited by CuO NPs (Xu 2018). The Cu NPs (15.6 mM) and Cu ions showed dose-dependent inhibitory effects on Triticum aestivum root growth decreasing by 60% and the formation of lateral roots was stimulated, possibly due to the enhancement of nitrogen uptake and accumulation of auxin in lateral roots (2018). Up to 80% of growth reduction was observed in A. thaliana treated with 300 mg L−1 ZnO NPs in soil pots (Wang et al. 2015). Similarly, 80% root and shoot biomasses of Medicago sativa were reduced by ZnO NPs at concentration ranging from 0 to 750 mg kg−1 soil (Bandyopadhyay et al. 2015). The elevated concentration (10–2000 mg L−1) of ZnO NPs revealed a biomass drop and damaged root surface cells of Fagopyrum esculentum at 2000 and 4000 mg L−1 (Lee et al. 2013). CuO NPs damaged the root tip and cap as well as the meristematic zone of A. cepa (Deng et al. 2016). Similarly, ZnO NPs also affected root tip and root morphology along with cortical cells, broke epidermis, vacuolated cortical cells, and shrank vascular cylinder of Lolium perenne (Lin and Xing 2008).
Nanoparticles affected ultrastructure of cellular and subcellular organelles: plastids, mitochondria, peroxisomes, plastoglobules, starch granules, protoplasm, vascular bundles, plasma membrane and cell wall (Rajput et al. 2018a, b). Decreased thylakoids number per granum, swollen intrathylakoidal space was observed in Oryza sativa treated with 1,000 mg L−1 CuO NPs (Da Costa and Sharma 2015). Increased periplasmic space of confluent parenchymal cells of Solanum lycopersicon was induced by CuO NPs (Ahmed et al. 2018). An increased number of plastoglobules, decreased size of starch grains, disrupted and irregular-shaped mitochondria, stroma displacing the grana, and dilation of the chloroplast membrane were observed in Landoltia punctata by CuO NPs (Lalau et al. 2015). Adams et al. (2017) found shorten zones of division and elongation and compressed epidermal cells in wheat by CuO NPs. ZnO NPs affected ultrastructure of chloroplasts of mesophyll cells, decreased the size, and increased the number of plastoglobules in Brassica napus L. (Mousavi et al. 2015). The highly collapsed cortical cells, broken epidermis and root cap, vacuolated cortical cells, and shrank vascular cylinder were observed in Lolium perenne treated with 1000 mg L−1 ZnO NPs.
These observations indicated a decline in seed germination, roots and shoots growth, and modifications in cell ultrastructure, especially in the photosynthetic apparatus, which could limit the surface area for water uptake and photosynthesis, respectively, and consequently affects the plant performance.
Effects on soil organisms
Nanoparticles are considered as a major cause of toxicity to both the pathogenic and beneficial microbes (Lofts et al. 2013) and very toxic to the native soil bacteria (Concha-Guerrero et al. 2014). The effects of NPs could be observed by measuring the soil respiration and enzymatic activities of soil microbial community (Simonin and Richaume 2015). A review indicates the NPs significantly affected enzymatic activities (invertase, urease, catalase, phosphatase, dehydrogenase), microbial community structure, bacterial diversity nutrient cycling, changes in humic substances, and biological nitrogen fixation (Rajput et al. 2017a).
In flooded paddy soil, CuO NPs decreased microbial biomass, enzymatic activities, and disturbed community structures (Xu et al. 2015). Similarly, ZnO NPs affected enzymatic activities of bacterial communities in saline–alkali and black soils (You et al. 2017). Concha-Guerrero et al. (2014) have also shown that CuO NPs were toxic for native soil bacteria, as observed from the formation of cavities, holes, membrane degradation, blebs, cellular collapse, and lysis in the cell of soil bacterial isolates. At 30–60 mg L−1, CuO NPs concentration affected the microbial enzymatic activity of activated sludge (Wang et al. 2017a). The study conducted on the effect of CuO on Saccharomyces cerevisiae shows increased toxicity over time due to increased dissolution of Cu ions from CuO (Kasemets et al. 2009). Bacterium Sphingomonas and Rhizobiales are well known for their importance in remediation and symbiosis with plant roots appeared susceptible to Cu NPs (Shah et al. 2016). CuO NPs were mostly bactericidal, while ZnO NPs had a bacteriostatic effect (Gajjar et al. 2009). ZnO NPs hindered the thermogenic metabolism, reduced the numbers of colonies of Azotobacter, P-solubilizing and K-solubilizing bacteria, and inhibited enzymatic activities such as urease, catalase, and fluorescein diacetate hydrolase activities (Chai et al. 2015). The effects of CuO and ZnO NPs on the soil microbial community are little explored. However, these results indicate the influence of CuO and ZnO NPs on soil microbial community structure and functionality which could impact biological nitrogen fixation.
Effects on human health
The CuO and ZnO NPs possibly enter the human cells via oral and skin exposure. Due to smaller size, NPs can easily penetrate through cell wall and membranes (Anreddy 2018). The schematic presentation of soil contamination by NPs and their possible impacts on human health is presented in Fig. 2. The studies on direct exposure of Cu NPs to human beings have not been reported; however, different human cell lines experiments demonstrate ill effects. CuO NPs treatment boosted the accumulation of mitochondrial superoxide anions and caused mitochondrial dysfunction in human umbilical vein endothelial cells (HUVECs) (Zhang et al. 2018b). It has also been observed in HUVECs that CuO NPs are deposited within the lysosomes and released Cu ions. Further, a caspase-independent cell death pathway is suggested in NPs-based cytotoxicity (Zhang et al. 2018a). CuO NPs damaged the mitochondria and lysosomes in human blood lymphocytes and increased ROS (reactive oxygen species) level (Assadian et al. 2018).
Increasing production and contamination of soil means higher chances of CuO and ZnO NPs to enter human body either accidently or by food chain; thereby, NPs can reach gastrointestinal tract. A concentration-dependent decrease in cell viability was observed in undifferentiated Caco-2 cells. Impacts including cell morphology, tight junction integrity, translocation, and IL-8 production were comparable to CuSO4, suggesting NPs release ions inside the cells (Ude et al. 2017). Cytotoxicity of Cu-based NPs for breast cancer cells was more selected than for normal cells lines at a higher concentration. Nanoparticles were able to induce ROS leading to oxidative stress (Azizi et al. 2017). Intracellular ROS may proceed with epigenetic changes that alter DNA methylation patterns affecting genome (Lu et al. 2016). Membrane blebbing and reduced cell viability were observed in breast cancer cell lines by ZnO NPs in concentration-dependent manner and were suggested to be a result of ROS, metal ions (Zn+2) (Umar et al. 2019). Cytotoxicity of ZnO NPs was induced by oxidative stress and inflammatory response, which depended on the size and concentration of NPs with the release of Zn2+ (Chen et al. 2019). Intracellular ROS was also associated with an increase in Zn ions in human aortic smooth muscle cells treated with ZnO NPs. An increase in endoplasmic reticulum stress biomarkers and occurrence of vacuolation of cells were related to NPs (Wang et al. 2018). The results highlighting damages to in vitro models signify the investigation of toxic effects of CuO and ZnO NPs.
Conclusion and future perspective
The CuO and ZnO NPs are the most extensively used nanoparticles.. These NPs are proven to pass through various chemical and biochemical reactions which could affect biological nitrogen fixation, damage a plant cell, and may cause a serious threat to human health. Therefore, the series of safety evaluation and toxicological risk assessment standards must be formulate, including exposure route and the safe exposure doses of ZnO and CuO NPs. Another way to reduce the release of NPs into the environment is to match their quantities with the stage of crop growth with the greatest response. An example, the appropriate application of small amounts of NPs had maximum benefits to crops when it applied to the seeds in a pre-germinative manner. Future studies should address some questions such as very less is known about the effects of NPs on food quality and threshold limits should be defined. Real-time data should be generated because most of the reported studies have been performed in hydroponics, potting soil, or synthetic soil and are little known about the interactions of NPs with plants in soils with different physicochemical properties. Based on these studies, the application of nanomaterials in field conditions will not be feasible until we reach a complete understanding of the phytotoxic effects and impacts on soil organisms and human health.
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This work was supported by the Ministry of Education and Science of Russia, Project No. 5.948.2017/PCh and joint projects: RFBR No. 18-55-05023 and SCS No. 18RF-077.
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Rajput, V., Minkina, T., Sushkova, S. et al. ZnO and CuO nanoparticles: a threat to soil organisms, plants, and human health. Environ Geochem Health 42, 147–158 (2020). https://doi.org/10.1007/s10653-019-00317-3
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DOI: https://doi.org/10.1007/s10653-019-00317-3