Shape-Dependent Transformation and Translocation of Ceria

Aug 29, 2017 - Rod-like CeO2-NPs transformed to a degree greater than those of the other CeO2-NPs in solution simulating the plant exudates, indicatin...
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Shape-Dependent Transformation and Translocation of Ceria Nanoparticles in Cucumber Plants Peng Zhang,*,† Changjian Xie,† Yuhui Ma,† Xiao He,† Zhiyong Zhang,*,† Yayun Ding,† Lirong Zheng,‡ and Jing Zhang‡ †

Key Laboratory for Biological Effects of Nanomaterials and Nanosafety, Institute of High Energy Physics, Chinese Academy of Sciences, Beijing 100049, China ‡ Beijing Synchrotron Radiation Facility, Institute of High Energy Physics, Chinese Academy of Sciences, Beijing 100049, China S Supporting Information *

ABSTRACT: The association of physicochemical properties of CeO2-NPs (CeO2 nanoparticles) per se with their transformation is not well understood. This study for the first time compared the translocation and transformation of octahedral, cubic, rod, and irregularly shaped CeO2-NPs in hydroponic cucumber plants. Cerium contents in roots were close between different treatments, while the largest amount (153 mg/kg) of Ce accumulated in rod-like CeO2-NP treatments. Transmission electron microscopy and X-ray absorption near edge spectroscopy show that rod CeO2-NPs transformed faster and more than other CeO2-NPs, with nearly 40% of Ce in the form of Ce(III) species in roots (CePO4) and shoots (Ce carboxylates). Rod-like CeO2-NPs transformed to a degree greater than those of the other CeO2-NPs in solution simulating the plant exudates, indicating that rod-like CeO2-NPs have the highest chemical reactivity. These results suggest that the intrinsically different chemical reactivity of differently shaped CeO2-NPs resulted in their different transformation and translocation capacities in plants. This study provides new insight into plant−NP interaction, highlighting the significance of the shape of nanoparticles in assessing their environmental behavior and impacts. We suggest that the influence of shape should be also considered for other nanomaterials and systems in developing an accurate understanding of the nano−bio interactions.

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dissolution.12 Organic ligands such as ethylenediaminetetraacetic acid (EDTA) and citrate promote the dissolution by complexation with the surface Ce(III).10,12 Reducing substances such as Fe(II) and ascorbic acids (Vc) can reduce the Ce(IV) to Ce(III) and release Ce3+.10,12 Plant root exudates containing organic acids, reducing sugars, and phenols promote the dissolution and reduction of CeO2-NPs.10 Physicochemical properties of NMs also have significant impacts on their transformation. It was reported that smaller CeO2-NPs released more Ce3+ ions in Lactuca plant roots.11 Citrate-functionalized CeO2-NPs transformed less than pristine CeO2-NPs did in an activated sludge reactor because citrate functionalization may act as a barrier against the interaction of CeO2-NPs with bacteria.13 CeO2-NPs are usually manipulated into different shapes to achieve high catalytic capacity.14 However, how the shape of CeO2-NPs influences their transformation has not been studied. In fact, studies of other NMs have shown that a discrepancy in shape may result in different biological effects and behavior. Fan et al.15 found that octahedral Cu2O-NPs created more severe oxidative stress on Daphnia magna than

INTRODUCTION CeO2-NPs (CeO2 nanoparticles) are of great interest for industrial, agricultural, and biomedical applications because of their unique redox cycling between oxidation states Ce(III) and Ce(IV).1−3 It was estimated that the global production of CeO2-NPs will be 1000 t per year.4 The release of CeO2-NPs into the environment is inevitable and may affect the biota and environment. 5,6 Exposure modeling has suggested that terrestrial systems are important sinks for nanomaterials (NMs).7 As a result, NMs will interact with plants and may accumulate in plants and have adverse effects on plant growth.6 Furthermore, the transfer of NMs from plants to high-trophic level organisms through the food chain is also possible.8,9 CeO2-NPs were previously considered to be stable in the environment; however, recent studies have shown that CeO2NPs are prone to transformation in plants, releasing Ce3+ ions and further transforming into CePO4 or Ce carboxylates.10 Consequently, Ce will accumulate in plants in various forms rather than as only CeO2, and the transformation products may at least partially contribute to the toxic effects of CeO2.11 The transformation of CeO2-NPs is highly affected by their surroundings. CeO2-NPs can release a significant amount of Ce3+ ions in plant-free growth medium depending on the composition of the medium.12 The presence of organic matter such as arabic gum prevents agglomeration of CeO2-NPs and thus maintains a large reaction surface, which could promote © 2017 American Chemical Society

Received: Revised: Accepted: Published: 380

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2017 2017 2017 2017 DOI: 10.1021/acs.estlett.7b00359 Environ. Sci. Technol. Lett. 2017, 4, 380−385

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Environmental Science & Technology Letters cubic Cu2O-NPs did. Oh et al.16 found that the viability of human lung fibroblast (IMR90) and mouse alveolar macrophage (J774A.1) cells treated with poly(3,4-ethylenedioxythiophene) (PEDT) nanomaterials with an aspect ratio of 1.3 was nearly 20% lower than that of cells treated with PEDT with an aspect ratio of 4.5. Syu at al.17 found that decahedral silver NPs promoted Arabidopsis root growth, while spherical silver NPs showed no effects. All these studies suggest that shape is a critical factor that should be considered when assessing the environmental risk and safety of NMs. Here, we exposed hydroponic cucumber plants to octahedral, cubic, rod-like, and commercial irregularly shaped CeO2-NPs and compared their transformation and uptake in plants. The goal of this study was to provide deep insight into the behavior and fate of CeO2-NPs in plants and the link with their physicochemical properties and provide a basis for the design of safer CeO2-NPs.

Ce2(C2O4)3, and Ce(CH3COO)3, were also recorded. See details in part 1.3 of section 1 of the Supporting Information. Transformation of CeO2-NPs in Simulated Solutions. To compare the reactivity of differently shaped CeO2-NPs, CeO2-NPs were added to four solutions to a concentration of 2000 mg/L: KH2PO4 with citric acid (CA) and Vc, KH2PO4 with EDTA and Vc, KH2PO4 with CA and catechol, and KH2PO4 with EDTA and CAT. CA and EDTA represent organic acids, while Vc and CAT represent reducing agents, both of which simulate the key components of plant root exudates. After 21 days, levels of CePO4 and Ce3+ in the solutions were determined by Fourier transform infrared and ICP-MS. See details in part 1.4 of section 1 of the Supporting Information.

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RESULTS AND DISCUSSION As shown in Figure S1 and Table S1, S-CeO2-NPs show irregular shape and the average particle size was 26 ± 18 nm. The primary sizes of O-CeO2-NPs and C-CeO2-NPs were 25.2 ± 2.3 and 30.9 ± 12.4 nm, respectively. R-CeO2-NPs show uniform sizes with a diameter of 8.9 ± 0.9 nm and a length of 106 ± 9 nm. All the CeO2-NPs agglomerated fast in 1/4 Hoagland solution (Figure S2). Sizes of agglomerates for RCeO2-NPs were much larger than those of other CeO2-NPs. Figure S3 reveals that none of the CeO2-NPs showed adverse effects on shoot and root biomass. Ce contents in roots are not significantly different between different treatments (Figure 1).

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EXPERIMENTAL SECTION Synthesis and Characterization of CeO2-NPs. All the chemicals used were of analytical purity. Octahedral CeO2-NPs (O-CeO2-NPs) was synthesized by a precipitation method. Cubic and rod-like CeO2-NPs (C-CeO2-NPs and R-CeO2-NPs, respectively) were synthesized by hydrothermal methods. See details of CeO2-NPs syntheses in part 1.1 of section 1 of the Supporting Information. Commercial CeO2-NPs (S-CeO2NPs) were purchased from Sigma-Aldrich. The purity of the nanoparticles was determined by inductively coupled plasma mass spectrometry (ICP-MS). Primary particle sizes and morphology were determined by transmission electron microscopy (TEM) (JEM 200CX). The ζ potential and hydrodynamic sizes of CeO2 NPs were analyzed with a Zetasizer Nano ZS90 (Malvern). Seedling Culture and Application of CeO2-NPs. Cucumber seeds were purchased from the Chinese Academy of Agricultural Sciences. Seeds were sterilized, germinated, transferred into 250 mL beakers, and allowed to grow in 1/4 Hoagland solutions for 10 days in an artificial climate chamber. Each seedling was then exposed to 100 mL of a 2000 mg/L CeO2-NP suspension in nutrient solutions. After 14 days, the seedlings were harvested for further analyses (see details in part 1.2 of section 1 of the Supporting Information); 2000 mg/L was the maximum exposure concentration established by U.S. Environmental Protection Agency guideline.18 According to our previous work, the uptake of Ce in shoots of cucumber at exposure concentrations of 79% of the Ce remained as CeO2 in roots after S-CeO2-NP, O-CeO2-NP, and C-CeO2-NP treatments, while after R-CeO2-NP treatments, >40% of the Ce presented as Ce(III) species, most of which was CePO4 and a small part of which was carboxylates (Figure 3C). More than 80% of Ce remained as CeO2 in shoots after S-CeO2-NP, O-CeO2-NP, and C-CeO2-NP treatments, while only 62% remained as CeO2 after R-CeO2-NP treatment (Figure 3D). These results agree

(Figure 2B4). The amount of CePO4 clusters on the root surface increased over time for all the treatments (Figure 2C1− C4 and Figure 2E1−E4). However, the amount of CePO4 in intercellular regions did not change significantly over time (Figure 2D1−D3 and Figure 2F1−F3) except for that after the R-CeO2-NP treatment, where a large amount of needlelike clusters were visible in the intracellular spaces on day 21 (Figure 2F4). The XANES spectra of roots subjected to S-CeO2-NP, OCeO2-NP, and C-CeO2-NP treatments show double white lines (Figure 3A), indicating that the Ce predominantly remained as CeO2. In contrast, spectra of roots after the R-CeO2-NP treatment presented a mixed feature of Ce(III) and Ce(IV), 383

DOI: 10.1021/acs.estlett.7b00359 Environ. Sci. Technol. Lett. 2017, 4, 380−385

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Environmental Science & Technology Letters with the TEM results, suggesting that R-CeO2-NPs transformed more than other CeO2-NPs did. We further calculated the absolute Ce(IV) and Ce(III) contents by multiplying their proportion by the total Ce contents. The smallest amount of Ce(IV) accumulated in roots during the R-CeO2-NP treatment, likely because R-CeO2-NPs formed large agglomerates and thus reduced the level of adsorption and/or absorption in roots. Ce(III) contents in roots were the highest after the R-CeO2-NP treatment, which agrees with the TEM and LCF results. Interestingly, Ce(IV) and Ce(III) contents in shoots were both higher after the RCeO2-NP treatment than after other treatments. Degradation of R-CeO2-NPs into small particles on root surfaces (Figure 2A4) may facilitate the movement of CeO2 and result in the high rate of Ce(IV) uptake in shoots. Because the transformation of CeO2-NPs occurs on the root surface rather than inside the plants,21 the high Ce(III) contents in shoots could be attributed to the high dissolving capacity of R-CeO2-NPs outside the roots. In a follow-up study, we incubated CeO2-NPs in simulated solutions that are composed of KH2PO4, reducing agents, and low-molecule organic acids. These components have been proven to have significant impacts on the transformation of CeO2-NPs.9,12,19 We found that the reactivity of CeO2-NPs decreases in the following order: R-CeO2-NPs > S-CeO2-NPs > O-CeO2-NPs > C-CeO2-NPs (see detailed results and discussion in part 2.5 of section 2 of the Supporting Information). The amount of CePO4 (Figure S5) or Ce3+ (Figure S6) transformed from R-CeO2-NPs was larger than those for other CeO2-NPs. CeO2-NPs with predominant facets of {100}/{110} planes are considered to be more catalytically active than those with {111} planes.22 In this study, O-CeO2-NPs enclosed by eight {111} planes are stable (Figure S7). S-CeO2-NPs exposed {111}, {200}, and {220} planes (Figure S8); however, S-CeO2NPs containing a large amount of small particles have a large surface area, thus also presenting high reactivity. C-CeO2-NPs exposed {100} or {111} planes (Figure S9); in addition, CCeO2-NPs are larger than the other CeO2-NPs. This may account for the low reactivity and transformation of C-CeO2NPs. R-CeO2-NPs were enclosed by six active planes, i.e., four {110} and two {100} planes (Figure S10), thus presenting the highest reactivity. Taken together, our results suggest that the shape of CeO2NPs determines their intrinsic chemical reactivity, thus affecting their transformation and translocation in plants. Studies of the particle shapes should be also performed with other NMs and systems. This is important not only for comprehensively understanding nano−bio interaction but also for the design of safer NMs.

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biomass production (Figure S3), translocation factors of CeO2-NPs in plants (Figure S4), XANES spectra of reference compounds (Figure S5), complete results of simulation studies (Figures S6 and S7), and highresolution TEM spectra of CeO2-NPs (Figures S8− S11) (PDF)

AUTHOR INFORMATION

Corresponding Authors

*E-mail: [email protected]. Telephone: +86-10-88233215. Fax: +86-10-88235294. *E-mail: [email protected]. ORCID

Peng Zhang: 0000-0002-2774-5534 Yuhui Ma: 0000-0002-7031-4596 Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This work was financially supported by the National Natural Science Foundation of China (Grants 11405183, 11375009, 11575208, 11675190, and 21507153) and the Ministry of Science and Technology of China (Grant 2016YFA0201600).

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ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.estlett.7b00359. Additional materials and methods (CeO2-NP syntheses, seedling culture and CeO2-NP application, sample preparation for TEM, ICP-MS, and XANES analyses, and transformation of CeO2-NPs in simulated solutions), complete results of characterization of CeO2-NPs (Figure S1 and Table S1), photos of agglomeration of CeO2-NPs in nutrient solutions (Figure S2), effects of CeO2-NPs on 384

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Environmental Science & Technology Letters (13) Barton, L. E.; Auffan, M.; Bertrand, M.; Barakat, M.; Santaella, C.; Masion, A.; Borschneck, D.; Olivi, L.; Roche, N.; Wiesner, M. R.; Bottero, J.-Y. Transformation of pristine and citrate-functionalized CeO2 nanoparticles in a laboratory-scale activated sludge reactor. Environ. Sci. Technol. 2014, 48, 7289−7296. (14) Tana; Zhang, M.; Li, J.; Li, H.; Li, Y.; Shen, W. Morphologydependent redox and catalytic properties of CeO2 nanostructures: nanowires, nanorods and nanoparticles. Catal. Today 2009, 148, 179− 183. (15) Fan, W.; Wang, X.; Cui, M.; Zhang, D.; Zhang, Y.; Yu, T.; Guo, L. Differential oxidative stress of octahedral and cubic Cu2O micro/ nanocrystals to Daphnia magna. Environ. Sci. Technol. 2012, 46, 10255−10262. (16) Oh, W. K.; Kim, S.; Yoon, H.; Jang, J. Shape-dependent cytotoxicity andproinflammatory response of poly (3, 4-ethylenedioxythiophene) nanomaterials. Small 2010, 6, 872−879. (17) Syu, Y. Y.; Hung, J. H.; Chen, J. C.; Chuang, H. W. Impacts of size and shape of silver nanoparticles on Arabidopsis plant growth and gene expression. Plant Physiol. Biochem. 2014, 83, 57−64. (18) U.S. EPA Ecological effects test guidelines. OPPTS 850.4150 Terrestrial Plant Toxicity, Tier I (vegetative Vigor). EPA 712-C-96163 (Public Draft); Office of Prevention, Pesticides and Toxic Substances, U.S. Environmental Protection Agency: Washington, DC, 1996. (19) Schwabe, F.; Tanner, S.; Schulin, R.; Rotzetter, A.; Stark, W.; von Quadt, A.; Nowack, B. Dissolved cerium contributes to uptake of Ce in the presence of differently sized CeO2-nanoparticles by three crop plants. Metallomics 2015, 7, 466−477. (20) Rui, Y.; Zhang, P.; Zhang, Y.; Ma, Y.; He, X.; Gui, X.; Li, Y.; Zhang, J.; Zheng, L.; Chu, S.; Guo, Z.; Chai, Z.; Zhao, Y.; Zhang, Z. Transformation of ceria nanoparticles in cucumber plants is influenced by phosphate. Environ. Pollut. 2015, 198, 8−14. (21) Ma, Y.; Zhang, P.; Zhang, Z.; He, X.; Zhang, J.; Ding, Y.; Zhang, J.; Zheng, L.; Guo, Z.; Zhang, L.; Chai, Z.; Zhao, Y. Where does the transformation of precipitated ceria nanoparticles in hydroponic plants take place? Environ. Sci. Technol. 2015, 49, 10667−10674. (22) Zhou, K.; Wang, X.; Sun, X.; Peng, Q.; Li, Y. Enhanced catalytic activity of ceria nanorods from well-defined reactive crystal planes. J. Catal. 2005, 229, 206−212.

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DOI: 10.1021/acs.estlett.7b00359 Environ. Sci. Technol. Lett. 2017, 4, 380−385