Distribution, Bioaccumulation, Trophic Transfer, and Influences of

Apr 6, 2017 - In view of the final destination of nanomaterials, the water system would be an important sink. However, the environmental behavior of ...
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Distribution, bioaccumulation, trophic transfer, and influences of CeO2 nanoparticles in a constructed aquatic food web Xingchen Zhao, Miao Yu, Dan Xu, Aifeng Liu, Xingwang Hou, Fang Hao, Yanmin Long, Qunfang Zhou, and Guibin Jiang Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.6b05875 • Publication Date (Web): 06 Apr 2017 Downloaded from http://pubs.acs.org on April 13, 2017

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Distribution, bioaccumulation, trophic transfer, and influences of CeO2 nanoparticles in a constructed aquatic food web

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Xingchen Zhao1,2, Miao Yu1,2, Dan Xu1,2, Aifeng Liu1,2, Xingwang Hou1,2, Fang

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Hao1,2, Yanmin Long1,3, Qunfang Zhou1,2* and Guibin Jiang1,2

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Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing

State Key Laboratory of Environmental Chemistry and Ecotoxicology, Research

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100085, P.R.China, E-mail: [email protected], Fax/Tel: +86-10-62849334.

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University of Chinese Academy of Sciences, Beijing, 100049, P.R.China

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Institute of Environment and Health, Jianghan University, Wuhan, 430000, P. R.

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China

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Corresponding author:

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*

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Fax/Tel: +86-10-62849334

Dr. Qunfang Zhou, E-mail: [email protected]

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ABSTRACT

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In view of the final destination of nanomaterials, the water system would be the

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important sink. However, the environmental behavior of nanomaterials is rather

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confusing due to the complexity of the real environment. In this study, a fresh water

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ecosystem, including water, sediment, water lettuce, water silk, Asian clam, snail,

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water flea, the Japanese Medaka, and the Yamato shrimp, was constructed to study the

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distribution, bioaccumulation and potential impacts of CeO2 nanoparticles (CeO2 NPs)

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via long-term exposure. The results demonstrated most of the CeO2 NPs deposited in

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the sediment (88.7%) when the partition approached constantly 30 days later. The

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bioaccumulated Ce in 6 tested biota species was negatively correlated with its trophic

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level, showing no biomagnification of CeO2 NPs through this food web. CeO2 NP

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exposure induced visual abnormalities in hydrophytes including chlorophyll loss in

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water silk and water lettuce, ultrastructural changes in pyrenoids of water silk and root

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elongation in water lettuce. The generation of hydroxyl radical (⋅OH) and cell wall

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loosening induced by CeO2 NP exposure might mediate the increased root growth in

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water lettuce. The findings on the environmental behavior of CeO2 NPs in water

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system have provided useful information on the risk assessment of nanomaterials.

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KEYWORDS: CeO2 NPs, aquatic microcosm, bioaccumulation, trophic transfer,

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impact

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INTRODUCTION

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The development and application of engineered nanomaterials (ENMs) have rapidly

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increased in diverse fields during the past decade. Like other emerging chemicals,

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concerns have concomitantly arisen on their potential hazards ever since the

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appearance of ENMs. As the ultimate sink for all pollutants, the aquatic ecosystem

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plays important roles in the full life cycle of ENMs due to their intentional and

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unintentional release1, 2. The behavior of ENMs in the aquatic ecosystem has thus

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become an urgent issue in view of their risk assessment.

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Nanoparticles (NPs) may be accidently or intentionally released to the aquatic

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system via: (1) industrial discharges or domestic waste, (2) disposal of effluents, (3)

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indirect surface runoff from soils, and (4) precipitation carrying NPs3-6. Once released

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into the environment, manufactured nanomaterials can be transported or migrate in

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the ambient media. Due to the different properties of the media, like water, sediment,

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and biota, ENMs can be re-distributed and transformed biotically or abiotically, thus

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causing changes in the physical and chemical characteristics of the particles.

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Laboratory simulative experiments are widely used to investigate the aquatic

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toxicology of NPs. It has been reported that metal oxide nanomaterials can cause

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mechanical cell damage to algae through particle exposure and metal ion release7-9. In

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contrast to the biomagnifications of certain nanomaterials in terrestrial food chains10,

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relatively lower concentrations of nanomaterials in higher trophic organisms when

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compared to those in lower trophic ones12-14. The estuarine mesocosms were

, the aquatic animals can directly take up and transfer ENMs in food chains with

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constructed to study the fates and bioavailabilities of gold nanorods with different

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charges in natural system, but the duration only lasted for 12 days, which did not

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necessarily capture the chronic influences occurring in the natural environment15, 16.

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Therefore, a better understanding of the transport and effects of nanomaterials from

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long-term exposure is imperative.

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Cerium oxide nanoparticles (CeO2 NPs) have become one of the most popular

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nanomaterials in the past several years, and are currently being utilized in various

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fields as catalyst, cell electrolyte, semiconductor, antioxidant, coating and polishing

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chemical17-20. Its wide use would eventually cause the emerging exposure issue in real

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environmental scenario like some other metal oxide nanoparticles, e.g. TiO2 NPs21.

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The increasing concerns have been raised, regarding their potential adverse impacts.

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Currently-available data shows that CeO2 NPs are more toxic than bulk CeO2, and

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may induce cell death, oxidative stress and DNA damage22-24. Mesocosms were also

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introduced to assess the impact of CeO2 NPs in aquatic ecosystem, and it was found

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that CeO2 NPs were readily removed from the water column and partitioned between

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different organisms25. The distribution and accumulation characteristics of CeO2 NPs

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in various aquatic organisms were different26. The valence conversion from Ce (IV) to

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Ce (III) occurred in the digestive gland of benthic organisms for both bare and coated

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CeO2 NPs27. The size and surface modifications of CeO2 NPs obviously influenced

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the temporal partition behavior of nanoparticles in aquatic system, their

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bioavailability and toxicity to the biota species22, 23, 25. Nevertheless, previous studies

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with food chains containing no more than three species could not fully represent the 4

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situation of a complete ecosystem or mimic the real environmental scenario. It was

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thus of importance to study the long-term effect of CeO2 NP exposure in a water

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ecosystem constituted by multiple abiotic and biotic components to clarify their

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environmental fate and potential impacts.

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In this study, we conducted 10-month investigations on CeO2 NPs in a

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lab-constructed microcosm simulating real environmental scenario. CeO2 NPs were

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spiked in the simulated fresh water ecosystem, and their distribution among water

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column, sediments, water lettuce (Pistia stratiotes), water silk (Spirogyra borealis),

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Asian clam (Corbicula fluminea), snail (Physa acuta), water flea (Daphnia magna),

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Yamato shrimp (Caridina japonica), and Japanese medaka (Oryzias latipes) was

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monitored for 10 months. The carbon sources and trophic levels of the organisms

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were analyzed by the determination of stable isotopes of carbon (δ13C) and nitrogen

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(δ15N). Using trophic transfer factor calculations, the bioaccumulation and

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biomagnification behaviours of Ce in the tested food web were subsequently assessed.

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The biological hazardous effects were specifically addressed on two tested

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hydrophytes. This study has provided fundamental information on understanding the

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transport and fate of CeO2 NPs in aquatic environment, which helps the enactment of

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the related environmental management policies to reduce the potential negative

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impact.

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MATERIALS AND METHODS

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Reagents. Bare CeO2 NPs with diameters of around 50 nm were purchased from

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Sigma (St. Louis, MO). The working suspension (200 mg/mL) was freshly prepared 5

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by directly dispersing the NPs (10 g) in 50 mL of the ultrapure water (18.2 MΩ•cm,

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Millipore, Billerica, MA). N-Benzylidene-tert-butylamineN-oxid (Sigma, St. Louis,

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MO) was used in the radical generation analysis. 37% HCl was bought from Merck

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(Darmstadt, Germany). All the other chemicals were obtained from Sinopharm Co.,

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Ltd. (Beijing, China).

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Experimental setup and exposure design. The simulative aquatic system,

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including three main components (water, sediment, and biota), was established to

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compose the experimental microcosm in the glass tanks (40 cm in length × 20 cm in

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width × 25 cm in height). In each tank, about 9 L of water and 3 kg sediment were

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added, respectively. Three replicates were designed for both control and CeO2 NPs

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exposure groups. The charcoal-filtered tap water was supplemented every week to

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keep the constant volume (i.e. 9 L) of the established aquatic system. The temperature

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(°C), light intensity (lux) and pH of the water system were monitored at around 12

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a.m. every week and the data were shown in Figure S1, S2 and S3 (Supporting

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Information), respectively. The light/dark cycle was constantly kept 16 hr/8 hr.

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These ecosystems were constructed by natural water and sediment collected from

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the dragon-shaped river of the Olympic Park, Beijing. The basal concentrations of Ce

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in the sediment (below ng/g) were negligible. The microcosms were allowed to

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equilibrate for 2 months prior to the start of CeO2 NP exposure. The species, including

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water lettuce (P. stratiotes), water silk (S. borealis), Asian clam (C. fluminea), snail (P.

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acuta) and water flea (D. magna), were commonly found in lakes or rivers in China.

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The Japanese Medaka (O. latipes) was bred in our lab for generations, and the Yamato 6

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shrimp (C. japonica) was bought from the local aquarium market. These organisms

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comprise a food web naturally occurring in Asia.

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The microcosm system in exposure group was gently spiked with 50 mL of 200

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mg/mL CeO2 NP solution by stirring water for 10 s for the good dispersion. The

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spiking was performed carefully to ensure the upper surface of the floating water

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lettuce leaves free from NP solution splash. The exposure was lasted for 10 months,

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and the volume of the water (9 L) and the amount of soil (3 kg) were approximately

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kept the same during the whole study. All the samples including water, sediments, P.

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stratiotes, S. borealis, C. fluminea, P. acuta, D. magna, C. japonica and O. latipes

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were harvested when the exposure was terminated. Partial sampling was also

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performed for two hydrophytes (i.e. P. stratiotes, and S. borealis) after 9-month

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exposure for chlorophyll measurement, pathological observation and hydroxyl radical

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analysis.

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CeO2 NP and Ce analysis. A JEOL 2100F microscopy (JEOL, Tokyo, Japan)

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equipped with Oxford INCA energy dispersive x-ray spectroscopy suite was used to

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measure the morphology and dimension of the CeO2 NPs. X-ray photoelectron

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spectroscopy (XPS) was measured using an X-ray photoelectron spectrometer

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(Thermo escalab 250Xi, USA) with a monochromatic X-ray source of Al Ka. The

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spectra were collected at the pass energy of 20 eV in the fixed analyzer transmission

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mode.

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For Ce concentration analysis, the samples, including sediments, P. stratiotes, S.

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borealis, C. fluminea, P. acuta, D. magna, C. japonica and O. latipes were collected, 7

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rinsed with ultrapure water for more than 5 times, and freeze-dried for 4 days, after

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which they were ground to powder. The digestion protocol for the biota (0.2 g) and

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water (1 mL) samples were performed using a mixture of HNO3 and H2O2 (2 mL; 3:2,

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v/v) at 95 °C in 15 mL Teflon tubes for 4 hrs. The digestion protocol for the sediment

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samples (0.2 g) was similar except that the acid mixture of HNO3, H2O2 and HF (2

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mL; 1:1:1, v/v/v) was used. The resultant solutions were evaporated to about 0.5 mL.

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The residue solutions were then diluted to 10 mL using ultrapure water. Ce

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concentrations in the sample solutions were measured on an Agilent 8800 inductively

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coupled plasma mass spectrometer (ICP-MS, USA).

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Trophic level and food source descriptors. In order to determine the food web

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structure and trophic levels of the organisms tested in the present study, we applied

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the classic stable-carbon (δ13C) and stable-nitrogen (δ15N) isotope methods28-32. The

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stable carbon (δ13C) and nitrogen (δ15N) isotopic ratios of all samples were

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determined at Chinese Academy of Forestry (Beijing, China) using a flash 2000

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EA-HT elemental analyzer interfaced with a DELTA V advantage isotope ratio mass

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spectrometer (Thermo Fisher Scientific Inc., Waltham, MA). The isotope ratio was

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standardized against atmospheric nitrogen or Pee Dee Belemnite (National Institute of

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Standards

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δ15Nsample=(Rsample-Rstandard)/Rstandard×1000‰, where R is the ratio of 15N/14N or 13C/12C.

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Trophic levels (TLs) were determined based on the results of δ15N using Eq 1:

&

Technology,

Gaithersburg,

MD)

using

δ13Csample

or

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TL consumer =2+(δ 15 N consumer -δ 15 N plankton )/∆N

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where ∆N is the trophic enrichment factor (3.4 ‰). Trophic levels were assigned

(1)

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relative to zooplankton (D. magna) which was assumed to occupy trophic level 2. The

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trophic magnification factors (TMFs) based on the entire food chain were derived

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from the slope of the plots of natural log concentrations (lipid normalized) versus TL:

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Log[Concentrations]=a+bTL (2)

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TMF=e b (3)

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TMF > 1 indicates that the NPs are biomagnified, whereas TMF