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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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1
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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] 1
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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
