Trophic Transfer and Transformation of CeO2 Nanoparticles along a

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Ecotoxicology and Human Environmental Health

Trophic transfer and transformation of CeO2 nanoparticles along a terrestrial food chain: Influence of exposure routes Yuhui Ma, Yao Yao, Jie Yang, Xiao He, Yayun Ding, Peng Zhang, Junzhe Zhang, Guohua Wang, Changjian Xie, Wenhe Luo, Jing Zhang, Li-Rong Zheng, Zhi-Fang Chai, Yuliang Zhao, and Zhiyong Zhang Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.8b00596 • Publication Date (Web): 21 Jun 2018 Downloaded from http://pubs.acs.org on June 26, 2018

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Environmental Science & Technology

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Trophic transfer and transformation of CeO2 nanoparticles along a

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terrestrial food chain: Influence of exposure routes Yuhui Ma,a Yao Yao,a Jie Yang,a Xiao He,a Yayun Ding,a Peng Zhang,a Junzhe Zhang,a Guohua Wang,a Changjian Xie,a Wenhe Luo,a Jing Zhang,b Lirong Zheng,b Zhifang Chai,a Yuliang Zhao, Zhiyong Zhang,a, c, *

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a

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of High Energy Physics, Chinese Academy of Sciences, Beijing 100049, China.

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b

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Academy of Sciences, Beijing 100049, China.

Key Laboratory for Biomedical Effects of Nanomaterials and Nanosafety, Institute

Beijing Synchrotron Radiation Facility, Institute of High Energy Physics, Chinese

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c

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Beijing 100049, China.

School of Physical Sciences, University of the Chinese Academy of Sciences,

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* Corresponding author.

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E-mail address: [email protected]

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Tel: +86-10-88233215; Fax: +86-10-88235294

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ACS Paragon Plus Environment


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Abstract

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The trophic transfer and transformation of CeO2 nanoparticles (NPs) through

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a simulated terrestrial food chain were investigated using radiotracer technique and

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X-ray absorption near edge structure (XANES). Radioactive

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applied to head lettuce (Lactuca sativa), either treated with root exposure in its potting

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soil (5.5 or 11 mg/plant) for 30 d or foliar exposure (7.2 mg/plant, with half of leaves

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treated and the other half not) for 7 d. Subsequently, two groups of land snails

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(Achatina fulica) were exposed to 141Ce via either a direct (i.e., feeding on the lettuce

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leaves with surface

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lettuce leaves with systemically distributed

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exposure routes, the Ce contents in the lettuce, snail tissues and feces were

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determined by radioactivity measurements. The results show that both assimilation

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efficiencies (AEs) and food ingestion rates (IRs) of Ce are greater for the trophic

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(indirect) exposure. The low AEs indicate that the ingested CeO2 NPs by snails were

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mostly excreted subsequently, and those remained in the body were mainly

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concentrated in the digestive gland. XANES analysis shows that more than 85% of Ce

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was reduced to Ce(III) in the digestive gland under direct exposure, whereas Ce in the

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rest of the food chain (including feces) was largely in its original oxidized (IV) state.

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This study suggests that CeO2 NPs present in the environment may be taken up by

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producers and transferred to consumers along food chains and the trophic transfer

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may affect the food safety.

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Introduction

141

141

CeO2 NPs were

Ce-contaminated) or an indirect/trophic (i.e., feeding on the 141

Ce) route. To evaluate the influence of

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Nowadays, manufactured nanoparticles (NPs) are widely studied and used in

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many different fields. Throughout their life spans, these NPs are able to enter various

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compartments of the environment, such as air, soil, and water, etc., during the wear

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and destruction of a product containing NPs.1, 2 Because of their small sizes and high

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reactivities, NPs may interact with environmental media, releasing toxic by-products,

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which can cause harm to terrestrial species, including plants.


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Plants are basic components of the ecosystem and vulnerable to NP exposure. It

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has been proved that some metal-based NPs can be taken up by plants and induce

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phytotoxicity, so it is reasonable to ask whether or not NPs can be transported to high

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trophic level consumers through food chains.3 However, the fate of NPs in the

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environment and their potential trophic transfer are rather poorly understood,

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especially in the terrestrial ecosystems and land food chains, which are more closely

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related to agricultural production, food safety and human health. Recently, Torre

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Roche et al. studied the transfer of bulk and NP La2O3 from soil through lettuce to

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crickets and then to mantises.4 They found that the La contents in the crickets and the

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mantises did not differ between bulk and NP-treatments after a longer depuration of 7

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d. However, it remains unknown whether the La was translocated in its ionic form or

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particulate form. In another study, was no Koo et al. fed insects with quantum dots

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(QDs)-contaminated Arabidopsis thaliana, and found that the different Cd and Se

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contents in the insects were likely derived from the ions released from QDs with

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different coatings.5 In general, the transfer of NPs in different trophic levels along

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land food chains is highly variable and depends on species investigated, NP

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compositions, and exposure conditions.

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Cerium oxide (CeO2) NPs are amongst the top 10 NPs produced worldwide and

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their annual global production was estimated to be 1000 tons/year by 2012.6, 7 The

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applications of CeO2 NPs include fuel additives, catalysts, polishing agents, and

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biomedical industry.8-11 Consequently these NPs have a high probability to enter the

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environment and have potential impacts on biota. Previous studies have shown that

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CeO2 NPs can be taken up by plants and translocated to the whole plant through the

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roots or leaves pathway.12-15 Once entering the plants, they might be transferred and

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accumulated in different tissues, especially in edible parts, and become available for

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higher level consumers. Therefore, investigation on the bioaccumulation and trophic

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transfer of CeO2 NPs within terrestrial food chains is of great importance. But

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unfortunately, this field is still in its infancy. Up to now, there are very few studies on

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the trophic transfer of CeO2 NPs along the terrestrial food chains.16 Hawthorne et al.



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compared the accumulation and transfer behavior of CeO2 from zucchini to crickets

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between bulk and nanoparticle forms.17 They found more CeO2 NPs accumulated in

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the zucchini than bulk materials, which resulted in more trophic transfer of CeO2 NPs

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in the crickets. However, whether or not CeO2 NPs can be transformed during the

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transfer process and how exposure pathways influence their transfer behaviors are

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almost completely unknown.

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In this study, the leafy vegetable lettuce (Lactuca sativa) was exposed to 141

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radioactive

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exposure scenarios from soil and air, respectively. The Ce-contaminated lettuce leaves

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were then fed to the land snails (Achatina fulica), which are a key component in

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terrestrial ecosystems and play a bridge role to connect plants and higher trophic level

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consumers. Ce contents in the plant and herbivore tissues were determined by

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radiotracer technique, which could detect the Ce uptake and transfer at

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environmentally relevant concentrations, regardless of the natural background levels.

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The transformation of CeO2 NPs in the primary producer and primary consumer was

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analyzed using X-ray absorption near edge structure (XANES). This study will

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provide significant information on the food chain transfer of CeO2 NPs under

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different exposure scenarios and on their environmental and human health risks.

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MATERIALS AND METHODS

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CeO2 NPs via root and foliar exposure routes, representing realistic

CeO2 NPs synthesis and characterization.

All the chemicals were analytical

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grade and obtained from Beijing Chemical Plant. Cerium-141 was produced by

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thermal neutron bombardments of

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Institute of Atomic Energy for 24 h at a thermal neutron flux of 2 × 1013 n/cm2∙s. After

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irradiation, CeO2 was chemically transformed into 141Ce(NO3)3 with H2O2 and HNO3.

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Both radioactive and nonradioactive CeO2 NPs were synthesized using a precipitation

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method as reported previously.18 Nonradioactive CeO2 NPs were used for

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characterization according to our previous report. The primary size of CeO2 NPs

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characterized by TEM was 6.9 ± 0.4 nm. The hydrodynamic size of the NP

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Ce (CeO2) in a swimming pool reactor at China


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agglomerates in deionized water were 40.2 ± 7.2 nm and zeta-potential was 32.9 ± 8.5

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mV, respectively.12

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Plant growth and CeO2 NPs application. The potting soil was obtained from Scotts

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Miracle-Gro Company and air dried at room temperature prior to use. Plastic boxes

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with 5×5 cm per cell were filled out with water-saturated of potting soil (11 g dry

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soil). Three seeds of head lettuce (Lactuca sativa) per cell were sown at about 1 cm

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beneath the potting soil surface. After germination, the seedlings were thinned to 1

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plant per cell with similar size. The seedlings were cultured in a climatic cabinate

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(PRX-450 C, Saifu, China) and the maximum/minimum temperature was 22/16 ℃

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during the test. The seedlings at the third or sixth leaf stage were separately exposed

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to

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deionized water or

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seedlings to obtain final concentrations of 0, 500, and 1000 mg NPs per kg dry soil

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(corresponding to 0, 5.5 or 11 mg NPs for each plant) with 6 replications. Each cell

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was supplied 10 mL of deionized water or 1/5 strength Hoagland’s solution14 every

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other day. At 7, 14, and 30 d, the relative chlorophyll contents in the leaves were

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measured using a chlorophyll meter (SPAD-502 Plus, Konic Minolta, Japan). After 30

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d of growth, the plants were harvested. 2) The six leaves were divided into two parts,

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with one part of four leaves on the adaxial side being dropped by 100 L of deionized

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water or

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part with the remaining two leaves being not dropped (untreated leaves) (Figure S1).

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19

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(approximately 1.2 mg NPs per g fresh weight). After 7 d, the chlorophyll contents in

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the leaves were measured. The treated leaves, untreated leaves and roots were

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separately harvested and quantified the Ce contents to determine the translocation of

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141

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Feeding experiment. Several dozen adult China white jade snails (Achatina fulica)

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were ordered from Green Agriculture Science and Technology Co., Ltd (Shanghai,

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CeO2 NPs through root or foliar exposure routes as the following: 1) 1.1 mL of

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CeO2 NP suspensions were applied to each cell around the

CeO2 NP suspensions (18 mg/mL) per leaf (treated leaves), and the other

This exposure corresponds to a final concentration of 7.2 mg NPs per plant

CeO2 NPs via foliar exposure.



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China) and were sorted by groups of 10 individuals into 24×15×15 cm polymethyl

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methacrylate containers amended with approximately 2 cm of sand. Acclimated snails

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were maintained without food for 48 h to ensure consumption upon feeding. One snail

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(six weeks old, 32.6 ± 1.9 g) was transferred to an acid-washed 16×9.5×12 cm

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polypropylene container served as an individual replicate. The snails were randomly

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assigned two group and fed on lettuce leaves via trophic/indirect (i.e., feeding on the

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lettuce leaves exposed to 1000 mg/kg

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feeding on the mixture of treated and untreated leaves from the foliar exposure)

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exposure. The leaves were cut into small pieces and mixed thoroughly, and then

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offered as diet at 1.5 g per day for per snail. There were five replicates for each

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treatment. During a 14-day exposure period, the residuals of unconsumed plant tissue

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were taken out from each replicate container for bulk analysis before feeding new

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leaves on the second day. The mass of Ce remaining in the tissues was subtracted

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from the individual snail’s dose. Feces produced by each snail were collected

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cumulatively and the Ce contents in each treatment were measured at 7 d and 14 d

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post exposure. During the feeding period, no snail was dead for all treatments. At the

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end of the experiment, snails were clean depurated individually for 48 h. After rinsing

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with deionized water, snails were euthanized and dissected into viscera (i.e., the

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visceral complex containing the posterior gut, digestive gland, kidney, mantle, and

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part of the reproductive tract), foot (containing the foot sensu stricto, anterior gut, and

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rest of the genital tract) and shell. All tissues were stored in a freezer (-20 0C) until

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further analysis.

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CeO2 NPs through the root) or direct (i.e.,

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Another experiment was performed with stable CeO2 NPs following the direct

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exposure for XANES analysis. After 7 or 14-days exposure, snails were euthanized

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and the digestive gland (DG) was isolated from the rest of the body. The samples

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were lyophilized with a freeze dryer and motor homogenized before XANES analyses.

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There were five replicates for each treatment.

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Radioactivity measurements. The activities of

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Ce (E=145.4 keV) in samples


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(contaminated lettuce, snails, and feces) were determined with a GWL series high

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purity germanium (HPGe) coaxial well photon detector system (EG&G-ORTEC,

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USA), with a resolution of 2.05 keV at the 1.33 MeV peak of

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crystal volume of 100 cm3. The data were expressed as mass concentration by

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comparing the radioactivity in the sample to the reference standard.

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Ce speciation analysis by XANES. The dry lettuce tissues and snail DG samples

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were ground to fine powders and pressed into thin slices with diameter of 10 mm and

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thickness of 2 mm for XANES analysis. XANES spectra were collected on 1W1B

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beamline of Beijing Synchrotron Radiation Facility (BSRF, China). The electron

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energy in the storage ring was about 2.5 GeV with a current about 50 mA. CeO2 and

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CePO4 (representing Ce(IV) and Ce(III)) were used as reference compounds. Ce

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(5723 eV) LIII-edge absorption spectra of reference compounds were obtained using

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transmission mode. Considering the low concentrations of Ce in samples, a

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19-element germanium array solid detector at fluorescence mode was used for the DG

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samples. The collected scans for samples were normalized using linear pre-edge and

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post-edge and the background was removed by spline fitting. The Ce XANES

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(-20~60 E, eV) spectra were analyzed by linear combination fit (LCF) using Athena

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software (Chicago, USA).

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Data analyses. Trophic transfer factors (TTFs), defined as the ratio of concentrations

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of Ce ([C]snails in g/g) in the snail tissue to that in the lettuce leaves ([C] lettuce in g/g),

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were calculated by the following equation (1).

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Co and total active

(1)

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The uptake of CeO2 NPs from food can be characterized by the Ce assimilation

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efficiency (AE, unitless) and the food ingestion rates (IR, g g-1 d-1).20 AE (%) can be

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calculated by the mass-balance of Ce in snails (Msnails in mg) and feces (Mfeces in mg)

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as the following equation (2), while food IR can be determined using Equation (3). (2)

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(3)

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where [C]lettuce represents total Ce concentration in the ingested lettuce (mg g-1), Wsnail is the dry weight of snail (g) and T is the exposure period (d).

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The results were expressed as mean±SD (standard deviation). One-Way ANOVA

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followed by Tukey’s HSD test was employed to examine the statistical differences

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among treatments. A 5% significance (p < 0.05) was used in all tests. All statistical

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analyses were conducted using Statistical Packages for the Social Sciences (SPSS)

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Version 18.0.

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RESULTS AND DISCUSSION

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Lettuce, with high germination rate, short vegetative cycle, and low genetic

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variability, has been specifically recommended for the determination of ecological

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effects from exposure to toxic substances.21 When grown in the media contaminated

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with NPs, this plant frequently transports NPs to its edible parts. Consequently, the

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consumption of fresh lettuce leaves by herbivores or humans may lead to the exposure

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to these NPs or their transformed metabolites.

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Plant biomass and relative chlorophyll contents in leaves

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The fresh and dry biomass of lettuce tissues under the root and foliar exposures is

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shown in Figure S2. Under root exposure, the total plant fresh/dry masses of lettuce

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from control, 500 and 1000 mg/L of CeO2 NPs exposures are 11.3 ± 2.4/1.58 ± 0.25,

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9.9 ± 1.0/1.48 ± 0.25 and 10.4 ± 1.8/1.47 ± 0.13, respectively. The total plant

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fresh/dry masses of lettuce from control and foliar exposure are 7.7 ± 1.0/1.0 ± 0.2

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and 8.0 ± 1.4/1.0 ± 0.2, respectively. The plant masses do not differ significantly

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relative to each control under both treatments. The results under the root exposure in

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this study are inconsistent with that previously reported by Gui et al., where they

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found that CeO2 NPs were phytotoxic to lettuce at a high concentration (1000

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mg/kg).22 The different effects might be attributed to at which growth stage CeO2 NPs

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was added, that is, lettuce is more sensitive to CeO2 NPs at germination stage than


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vegetable stage.

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The relative chlorophyll contents of lettuce exposed to CeO2 NPs through roots

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are displayed in Figure S3. Statistically significant differences are only shown

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between the control and the concentration of CeO2 NPs at 1000 mg/kg. At 7 d after

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treatment, the relative chlorophyll contents increase significantly, while decrease at 30

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d with respect to each control (p < 0.05). In contrast, there is no significant difference

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between the treated group and control under the foliar exposure for 7 days (data not

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shown).

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Ce accumulation in plants

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Under the root exposure, concentrations of Ce in the roots/leaves of lettuce plants

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grown in potting soil amended with 500 and 1000 mg/kg CeO2 NPs are 44.5 ±

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20.7/0.09 ± 0.04 and 79.5 ± 62.0/0.3 ± 0.17 g/g, respectively (Figure 1A). A number

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of studies have demonstrated the accumulation and translocation of CeO2 NPs in

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various plant species in hydroponic or soil media.23-25 Most of these studies observed

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a dose-dependent increase of Ce in the root tissues and translocation factors of Ce

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from roots to shoots were usually less than 1%.26, 27 Similar to these, the majority of

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CeO2 NPs in this study is accumulated in the roots and Ce contents in the shoots are at

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least two order of magnitude below that in the roots. The calculated translocation

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factors of Ce are respectively 0.22 ± 0.13% and 0.46 ± 0.16% at the CeO2 NP

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concentrations of 500 and 1000 mg/kg (p < 0.05), which are comparable to the

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previous reports.17, 26

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Under the foliar exposure, Ce concentrations in the treated leaves (with CeO2

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dropped on them), untreated leaves (without CeO2), and roots of lettuce are 982.4 ±

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341.7, 8.1 ± 3.4, and 2.7 ± 0.4 g/g, respectively (Figure 1B). Considering that the

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relatively high background Ce levels in potting soil (86.2 ± 26.8 mg/kg in this study)

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may confuse the quantitative detection of Ce contents, it is beneficial to use

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radioactive tracers since they are not susceptible to the interference from endogenous



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substances. Therefore, the Ce contents detected in the untreated leaves and roots are

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definitely transloacted from those treated leaves, indicating that CeO2 NPs could be

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taken up by leaves and transported to the whole plant. This result is in line with a

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previous work, where CeO2 NPs can be taken up through the leaves and distributed

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within cucumber plant tissues. 28

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Figure 1. Ce contents of the roots and shoots of lettuce plants exposed to CeO2 NPs through root

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(A) or foliar (B) exposure treatments. The values were given as mean ± SD (n = 5). The different

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letters indicate significant difference at p < 0.05 among the different treatments.

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Ce in the consumer snails

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In the present study, “trophic exposure” meant feeding snails with lettuce exposed

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to CeO2 NPs via their roots, in which NPs had been taken up and incorporated into

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plant tissues. In contrast, “direct exposure” meant feeding snails with lettuce exposed

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to CeO2 NPs via their leaves, in which the majority of NPs was adsorbed on the leaf

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surface. After the experiments, no mortality of snails was observed and the weight of

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snails increased by 5.6 ± 1.8% for trophic exposure and 2.5 ± 1.3% for direct

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exposure (p > 0.05), respectively (Figure S4). The concentrations of Ce within snails

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under different exposures are listed in Table 1. For a 48 h depuration period, the Ce

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content in the visceral organ of snails fed on lettuce exposed by roots is 0.011 ± 0.003

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g/g, while those in the foot and shell are below the limit of quantification (LOQ, 3.5

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ng Ce). In contrast, Ce contents in the foot, shell, and visceral organ of snails


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consuming foliar-exposed lettuce leaves are 0.015 ± 0.006, 0.081 ± 0.041 and 0.51 ±

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0.12 g/g, respectively. In both trophic and direct exposures, the accumulations of Ce

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in the visceral organ are much higher than those in the foot and shell, indicating that

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feeding is the major route of transfer of Ce into the snails. It has been reported that

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viscera of snails have strong organizational retention capacity for metals, such as Cd,

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Pb and Zn.29 Likewise, the digestive system is also the main retention organ of NPs

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for higher level consumers. For instance, high concentrations of corresponding metals

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were found to be accumulated in the midgut of insects after eating Au, Ag or TiO2

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NPs-contaminated plant leaves.30-33 The highest total Ce concentrations were

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observed in the dissected DG of adult Planorbarius corneus which were grown in

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CeO2 NPs-contaminated aquatic mesocosms.34 These results are consistent with our

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current research. It has been reported that significantly greater amounts of Ce can be

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accumulated in plants and thus their consumers when exposed to CeO2 in nanoparticle

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form than bulk one.17 In this study, it definitely proved that CeO2 NPs can be

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transmitted from plants to herbivores by trophic transfer through a terrestrial food web

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and have a risk of biological transmission, though the concentration of Ce in snails is

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very low. However, the food borne lettuce does not lead to a strong Ce accumulation

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in the part of the snail foot, which is the edible part of snails when they are as a kind

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of food. This shows that the potential risk of transferring of Ce to human beings

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through the food chain is less evident.

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The combined 7/14 d dry weights of feces are 0.5 ± 0.15/0.95 ± 0.18 g and 0.56 ±

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0.22/1.06 ± 0.21 g for trophic and direct exposed snails, respectively. There is no

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significant difference in feces weights between the two treatments (p > 0.05).

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However, the combined 7/14 d fecal Ce contents are 6.4 ± 2.4/7.2 ± 1.5 g/g and 5.7

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± 1.5/6.0 ± 1.2 mg/g for trophic and direct exposed snails, respectively (Table 1). It is

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not surprising to find that the Ce contents in feces are over 10 times higher than the

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leaf contents, given that the amount of feces is dry weight. It is interesting to find that

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Ce contents in feces collected during 14 d of exposure are slightly greater than during

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7 d for both exposures, suggesting the accumulation of Ce in the snails is close to



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saturation. The high excretion efficiency (see below AEs) indicates relatively low

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element accumulation within the consumers on consumption of contaminated plant

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leaves. These results are comparable to some recent studies. Conway et al. illustrated

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that approximately 99% of CeO2 NPs that captured by marine mussels was excreted

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in pseudofeces whether through direct or trophic exposure.35 In another study,

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Kubo-Irie et al. investigated the effects of TiO2 NPs-contaminated food on larval

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growth and found limited bio-concentration of TiO2 in the midgut epithelium of the 2

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nd instar larvae.32 The above results imply that captured NPs in the higher level

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consumers can be depurated through the processes of digestion and excretion.

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Table 1. Ce concentrations in different tissues (fresh weight) of the snails fed on CeO2

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NPs-contaminated lettuce and feces (dry weight). The values were given as mean ± SD (n = 5).

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The different lower- and upper-case letters indicate significant difference at p < 0.05 among the

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tissues and feces, and between the two treatments, respectively.

Ce Contents (g/g) Trophic exposure

Direct exposure

foot

n.d.x, A

0.015 ±0.006a, B

shell

n.d.x, A

0.081 ±0.041b, B

viscera

0.011 ±0.003y, A

0.51 ±0.12c, B

feces 7d

6.4 ±2.4z, A

5663 ±1508d, B

feces 14d

7.2 ±1.5z, A

6011 ±1200d, B

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n.d. = not determined.

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Trophic transfer of Ce

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TTFs are used to assess Ce trophic availability along the food chain from lettuce

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to snails. After a 48 h depuration period, the TTF values for CeO2 NPs through the

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trophic and direct exposure are 0.037±0.007 and 0.0012±0.0004, respectively (Table

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2). TTFs under the two treatments are both far below 1, indicating that it has less


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possibility for this element to be biomagnified through the trophic transfer. However,

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the value of trophic exposure is significantly higher than that of direct exposure (p
0.05), with 94.8 ± 1.4% for the trophic exposure and

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85.9 ± 11.2% for the direct exposure, respectively (Table 2). Further, the uptake of Ce

321

is characterized by AEs and food IRs. After 48 h of depuration, only a low amount of

322

Ce is present in the snail tissues and AEs are estimated at 5.0 ± 1.4% for the trophic

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exposure and 0.17 ± 0.02% for the direct exposure, indicating that the elimination is

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very easy and the weak biodistribution of Ce in the internal organs. The low AEs in

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this study are compared with those reported previously, where the AE of TiO2 NPs in

326

mussels was 3.0% quantified by the stable isotope

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in freshwater and land snails were reported to be over 60% and even up to 100%.38, 39

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Therefore, nanomaterial composition, terrestrial species and exposure routes may

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influence the estimation of AEs.

47

Ti.37 However, AEs for Ag NPs

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The average IRs in snails through the trophic and direct exposures are 0.20 ± 0.05

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and 0.10 ± 0.02 g/g/d, respectively (Table 2). Similar to TTFs and AEs, a significant

332

difference in IRs is shown between the two treatments (p < 0.05). As mentioned

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above, the weight enhancement of the snails and the amount of feces had no

334

significant difference under the two treatments at the end of experiment. However, the

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amount of residual leaves was significantly different, with all of food being consumed



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336

by the trophic exposed snails while approximately 15% of food unconsumed by the

337

direct exposed snails. The reduction of food ingestion under direct exposure treatment

338

might be attributed to the avoidance of food for snails when there is high

339

accumulation of NPs in the food. Likewise, lower IRs were observed in snails feeding

340

Ag NPs-amended diatoms than those exposed to diatoms pre-exposed to Ag+.40 The

341

current and other previous studies reveal that it has greater bioavailability for NPs

342

when systemically distributed in the tissues than only adsorbed on surface of a prey

343

species. Several possible explanations are listed as following:31,

344

ingested NPs remain longer in the consumers through dietary exposure; 2)

345

modification of NPs surfaces occurs during uptake into the initial trophic level and

346

trophic filtering; 3) drying of NPs onto the leaf surface results in aggregation and thus

347

reduced their bioavailability; 4) the palatability of the food is reduced and some

348

avoidance of food occurred when there are NPs in the food.

349

Table 2. TTFs, recovery (%), AEs (%), and IR (g/g/d) of snails fed on CeO2 NPs-contaminated

350

lettuce. The values were given as mean ± SD (n = 5). The different lower-case letters indicate

351

significant difference between the two treatments (p < 0.05).

352

32, 36, 37, 40

Trophic exposure

Direct exposure

TTFs

0.037 ±0.007a

0.0012 ±0.0004b

Recovery (%)

94.8 ±1.4a

85.9 ±11.2a

AEs (%)

5.0 ±1.2a

0.17 ±0.05b

IR (g/g/d)

0.20 ±0.05a

0.10 ±0.02b

1) the

Transformation of CeO2 NPs in lettuce and snails

353

To investigate by which form CeO2 is accumulated in plants and transferred to

354

herbivores, chemical species of Ce in the plants, snails DG, and feces at the end of the

355

experiments are analyzed using XANES and LCF. The results are shown in Figure 2

356

and Table 3. The low R-factors indicate the good quality of all the LCFs of the

357

experimental data. The difference for Ce(IV) and Ce(III) is characterized by two


Page 15 of 22


358

absorption peaks at 5730.0 and 5737.2 eV for Ce(IV) while only one absorption peak

359

at 5725.7 eV for Ce(III) reference compounds. It can be seen that the spectra of Ce in

360

the lettuce roots through root exposure, as well as in the treated and untreated leaves

361

through foliar exposure are all similar to that of initial CeO2 NPs (Figure 2A). The Ce

362

contents in the root-exposed leaves and leaf-exposed roots are too low (< 5 ppm) to be

363

analyzed by XANES. The quantitative results of LCF show that Ce in plant tissues is

364

mainly present as Ce(IV) (Table 3), indicating that the NPs are limited reduced, if any.

365

It has been reported that the release of Ce3+ ions from CeO2 NPs played a key role in

366

their phytotoxicity to Lactuca plants.41, 42 Considering the lower bioavailability of

367

NPs in soil than in aqueous media and less transformation, the nontoxicity of CeO2

368

NPs to lettuce in this study is reasonable.

369

Interestingly, XANES spectra of the snails DG for the direct exposure resemble

370

that of Ce(III) in appearance, while those of feces still resemble Ce(IV) reference

371

(Figure 2B). LCF results indicate that more than 85% of Ce(IV) is reduced to Ce(III)

372

in DG after staying in snails for 7 d and 14 d (Table 3). It seems that the strong

373

reduction of Ce is only occurred in the snails DG after ingestion, for Ce(IV) species

374

are predominated in the plant tissues and feces. The reduction of CeO2 NPs has been

375

observed in several species, such as E. coli,43 plants,12 nematodes,44 earthworm,45 and

376

also freshwater snails.34 Moreover, we have demonstrated natural reducing substances

377

and organic acids in root exudates play important roles for the reduction of CeO2 NPs

378

in plants.12, 46 As for snails, the DG is the main site for nutrient metabolism and

379

detoxification, which can produce various enzymes (e.g., digestive cysteine

380

proteinase)47 and metalloproteins.48 These reductive groups and low pH value36 in the

381

DG might be responsible for the reduction and/or dissolution of CeO2 in the snails.

382

The released ions might enter into internal organs and induce oxidative stress,34 which

383

need further investigation.



Page 16 of 22

384 385

Figure 2. The XANES spectra of the plant tissues exposed to CeO2 NPs (A), and snail DGs and

386

feces (B) treatments under direct exposure (B). Solid and dashed lines indicate the white line

387

position of Ce(III) and Ce(IV), repectively.

388 389

Table 3. Summary of LCF results of the XANES spectra for CeO2 in the lettuce tissues, snail DGs and feces under trophic exposure route.

390

Ce(III) (%)

Ce(IV) (%)

R-factor

Treated shoot

3.8

96.7

0.00023

Untreated shoot

4.8

98.4

0.00022

Root

3.1

100

0.00037

Dg-7d

89.2

12.2

0.0023

Dg-14d

85.3

14.8

0.0059

Feces-7d

5.2

96.0

0. 000063

Feces-14d

4.6

98.2

0.00024

Environmental significance

391

This study provides the first report about the accumulation of CeO2 NPs from soil

392

and air to plant tissues, with subsequent trophic transfer and biotransformation along a

393

terrestrial food chain via different exposure pathways. The results suggest that CeO2

394

NPs can be transmitted from plants to terrestrial herbivores by trophic transfer and

395

snails assimilate Ce more efficiently through the trophic exposure. Furthermore, the

396

biotransformation of CeO2 NPs almost does not occur in the plants and snail feces,


Page 17 of 22


397

but only in the snail DGs. The question that remains to be answered is whether the

398

reduction of Ce(IV) to Ce(III) induces an oxidative stress to the model organism and

399

the potential risk for human through the food supply.

400

401

402

Conflict of Interest The authors declare no competing financial interest.

403

404

405 406

Supporting Information The Supporting Information is available free of charge on the ACS Publications website.

407

Photographs of foliar exposure by control and CeO2 NPs treatments (Figure S1).

408

Fresh weight and dry weight biomass of roots/shoots from lettuce plants exposed to

409

CeO2 NPs through root or foliar exposure (Figure S2). Chlorophyll contents in the

410

leaves of lettuce plants grown for 30 days in potting soil, treated with 0, 500, and

411

1000 mg/kg CeO2 NPs (Figure S3). Snail weight at the beginning and end of the

412

experiments (Figure S4).

413

414

Acknowledgments

415

This work was financially supported by National Natural Science Foundation of

416

China (Grant No. 11575208, 11375009, 11405183, and 11675190) and the Ministry of

417

Science and Technology of China (Grant No. 2016YFA0201604).

418



419

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Trophic Transfer and Transformation of CeO2 Nanoparticles along a

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