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Bioaccumulation of 14C-labled Graphene in an Aquatic Food Chain through Direct Uptake or Trophic Transfer Shipeng Dong, Tian Xia, Yu Yang, Sijie Lin, and Liang Mao Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.7b04339 • Publication Date (Web): 21 Dec 2017 Downloaded from http://pubs.acs.org on December 21, 2017
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Environmental Science & Technology
Table of Content
ACS Paragon Plus Environment
Environmental Science & Technology
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Bioaccumulation of 14C-labeled Graphene in an Aquatic Food Chain
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through Direct Uptake or Trophic Transfer
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Shipeng Dong†, Tian Xia‡,#, Yu Yang§, Sijie Lin┴ and Liang Mao†*
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†
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Nanjing University, Nanjing 210093, China
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‡
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Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing 100085, China
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#
Division of NanoMedicine, Department of Medicine, University of California, Los Angeles
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§
Department of Civil & Environmental Engineering, University of Nevada, Reno
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┴
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Control and Resource Reuse, Tongji University, Shanghai 200092, China
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Address correspondence to L. Mao, State Key Laboratory of Pollution Control and Resource
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Reuse, School of the Environment, Nanjing University, Nanjing 210093, P. R. China. E-mail:
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[email protected].
State Key Laboratory of Pollution Control and Resource Reuse, School of the Environment;
State Key Laboratory of Environmental Chemistry and Ecotoxicology, Research Center for
College of Environmental Science & Engineering, State Key Laboratory of Pollution
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ABSTRACT
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The growing applications of graphene materials warrant a careful evaluation of their
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environmental fate in aquatic food webs. Escherichia coli (Bacteria), Tetrahymena
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thermophila (protozoa), Daphnia magna (zooplankton) and Danio rerio (vertebrate) were used
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to build aquatic food chains to investigate the waterborne uptake and trophic transfer of
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14C-labeled graphene. Body burden factor (BBF) and trophic transfer factor (TTF) were
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analyzed for each organism and food chain to assess the bioaccumulation and
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biomagnification of graphene. The test organisms have high potential of accumulating
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graphene via direct uptake from culture medium with log-transformed BBF (log BBF) values
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of 3.66, 5.1, 3.9 and 1.62 for each organism, respectively. In the food chain from E. coli to T.
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thermophila, the calculated TTFs of 0.2 to 8.6 indicate the high trophic transfer potential in
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this aquatic food chain. However, the TTFs calculated for the food chain from T. thermophila
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to D. magna and from D. magna to D. rerio are much lower than 1, indicating that
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biomagnification was unlikely to occur in these food chains. Body burden measured for
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dietary uptake by T. thermophila, D. magna and D. rerio are higher than that via waterborne
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exposure in a similar nominal concentration, respectively, indicating that trophic transfer is a
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non-eligible route for the bioaccumulation of graphene in organisms.
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INTRODUCTION
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The growing industrial applications of graphene will lead to its inevitably releasing into
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the environment1,2 and potentially lead to negative ecological and human health effects3-9. As
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one of the essential parts in the environment and health risk assessment, the accumulation and
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elimination of graphene in organisms are limitedly investigated partly due to the lacking of
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effective quantification methods for graphene in complex environmental matrixes.10 Recently,
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with the using of a novel radioactive labeling technique, studies regarding exposure behavior
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of graphene in organisms were reported.7,11,12 When exposed to graphene suspension at
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similar concentration and exposure duration, the zooplankton daphnia had a much greater
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capability of accumulating graphene (body burden of ~8000 (µg graphene per g dry mass)11)
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compare to the vertebrate zebrafish (body burden of ~50 (µg graphene per g dry mass)12).
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These concentrations were both at least an order of magnitude higher than that for the
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oligochaete Limnodrilus hoffmeisteri (body burden of ~ 3 µg graphene per g dry mass)7.
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These difference may be attributable to the difference on body size, organs complexity and
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feeding behaviors.
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In addition to direct uptake of NPs suspended in the water, aquatic organisms in the
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environment could also accumulate NPs through trophic transfer from consumption of NPs
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associated with their prey. Most studies have concentrated on the exposure behavior of
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metallic nanoparticles in the single organism or short food chain.13-18 However, a stable
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microbial loop and a food web composed of multicellular organisms are usually regarded as
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two essential compartments of a productive aquatic ecosystem.19 Bacteria using organic
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matter as productive nutrition potentially ingested by protozoa like ciliates, along with the
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protozoa, constitute the simple microbial loop. The ingestion of protozoa by water-filter
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zooplankton (such as daphnia or rotifer) act as the connection between microbial loop and
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multicellular food web, which better simulates an aquatic ecosystem. Thus, in order to explore
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the exposure behavior of graphene in the aquatic ecosystem, it is reasonable to investigate the
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uptake and trophic transfer of nanoparticles from the organism belongs to lowest trophic level,
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like bacteria, to higher level organisms such as protozoa, zooplankton and fish.
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Bioconcentration factor (BCF) and biomagnification factor (BMF) have been used to
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assess the potential risk of traditional pollutants through direct exposure and trophic transfer, ACS Paragon Plus Environment
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respectively. However, the use of BCF for estimating bioaccumulation are not appropriate to
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measure the bioconcentration of nanomaterials because they do not reach equilibrium during
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test process.20 Furthermore, due to the property of carbon based nanoparticles (CNPs)
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including agglomerations, the CNPs gained access to the organisms may not penetrate
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through the intestinal epithelium and translocate to other tissues.21-25 The accumulation of
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CNPs is mainly in the intestinal tract, rather than distribution to the whole body, which may
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lead to the definitions of bioconcentration and biomagnification for CNPs being different to
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that of traditional pollutants.20 Thus, how to redefine the bioconcentration and
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biomagnification for NPs should be one of the essential issues in the CNPs exposure study.
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In the present study, Escherichia coli (Bacteria), Tetrahymena thermophila (protozoa),
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Daphnia magna (zooplankton) and Danio rerio (vertebrate) were used as model organisms to
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build an aquatic food chain to investigate the direct uptake and trophic transfer of graphene in
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the aquatic ecosystem, as summarized in Figure 1. The potential for graphene
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bioaccumulation and biomagnification in organisms at various trophic levels was assessed.
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This study provides the first evidence of graphene family nanomaterial undergoing trophic
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transfer in simplified food chains.
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EXPERIMENTAL SECTION
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Materials and Test Organisms. All reagents used are of analytical grade without further
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purification.
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0.59 mCi/g was synthesized according to our previous study11 and characters were presented
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in Supporting Information (SI). Modeling studies reported that the concentrations of
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carbon-based nanomaterials in surface water ranged from ppt to ppb26,27. Thus, the tested
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concentration of FLG in this study was set in the range of 1 to 1000 µg/L. A Gram-negative
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bacterial strain, Escherichia coli, purchased from BeNa Culture Collection (Beijing, China).
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Tetrahymena thermophila strain SB210E, daphnia magna and Danio rerio were obtained
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from the Institute of Hydrobiology (Chinese Academy of Science, Wuhan, China). The grown
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daphnia (~15 days old) was used as predator and daphnia neonates (
