Trophic Transfer and Accumulation of Multiwalled Carbon Nanotubes

Dec 20, 2017 - Department of Chemical Engineering, Texas Tech University, ... Zhang, Du, Peralta-Videa, Gardea-Torresdey, White, Keller, Guo, Ji, and ...
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Article Environmental Science & Trophic transfer Technology is and published by the American Chemical accumulation Society. 1155of Sixteenth Street N.W., Washington, multi-walled carbon 20036 Subscriber accessDC provided by READING Published by American UNIV Chemical Society. Copyright © American Chemical Society.

nanotubes in the presence Environmental of copper Science & Technology is published by the American Chemical ions in Daphnia magna Society. 1155 Sixteenth Street N.W., Washington, 20036 by READING Subscriber accessDC provided Published by American UNIV Chemical Society. Copyright © American Chemical Society.

and fathead minnow (PimephalesEnvironmental promelas) Science & Technology is published

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J. Green, Amanda D. French, David M. Klein, Jordan Crago, Environmental Science & and Jaclyn E. Technology Cañas-Carrell is published by the American Chemical

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Page 1 ofEnvironmental 26 Science & Technology MWCNTs + Cu2+

MWCNTs

Cu2+

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Trophic transfer and accumulation of multi-walled

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carbon nanotubes in the presence of copper ions in

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Daphnia magna and fathead minnow (Pimephales

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promelas)

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Amanda M. Cano1, Jonathan D. Maul1, Mohammad Saed2, Fahmida Irin3, Smit A. Shah4, Micah

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J. Green4, Amanda D. French1, David M. Klein1, Jordan Crago1, Jaclyn E. Cañas-Carrell1*

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Department of Environmental Toxicology, The Institute of Environmental and Human Health,

Texas Tech University, Lubbock, TX, USA 2

Department of Electrical and Computer Engineering, Texas Tech University, Lubbock, TX,

USA 3

Department of Chemical Engineering, Texas Tech University, Lubbock, TX, USA

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Artie McFerrin Department of Chemical Engineering, Texas A&M University, College

Station, TX, USA

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*Email: [email protected]; Phone: 806-834-6217; Fax: 806-885-2132

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Abstract

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The increase in use of nanomaterials such as multi-walled carbon nanotubes (MWCNTs)

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presents a need to study their interactions with the environment. Trophic transfer was measured

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between Daphnia magna and Pimephales promelas (fathead minnow, FHM) exposed to

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MWCNTs with different outer diameter (OD) sizes (MWCNT1 = 8-15 nm OD and MWCNT2 =

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20-30 nm OD) in the presence and absence of copper. Pristine FHM were fed D. magna,

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previously exposed for 3 d to MWCNT1 or MWCNT2 (0.1 mg/L) and copper (0.01 mg/L), for

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7 d. D. magna bioaccumulated less MWCNT1 (0.02 µg/g) than MWCNT2 (0.06 µg/g), while

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FHM accumulated more MWCNT1 (0.81 µg/g) than MWCNT2 (0.04 µg/g). In the presence of

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copper, MWCNT bioaccumulation showed an opposite trend. Mostly MWCNT1 (0.03 µg/g)

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bioaccumulated in D. magna, however less MWCNT1 (0.21 µg/g) than MWCNT2 (0.32 µg/g)

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bioaccumulated in FHM. Bioaccumulation factors were higher for MWCNT1s than MWCNT2.

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However, an opposite trend was observed when copper was added. Plasma metallothionein-2

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was measured among treatments; however concentrations were not statistically different from the

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control. This study demonstrates that trophic transfer of MWCNTs is possible in the aquatic

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environment and further exploration with mixtures can strengthen the understanding of MWCNT

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environmental behavior.

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1. Introduction Due to their novel and distinct characteristics such as high tensile strength, conductivity,

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and surface area, carbon nanotube (CNT) use is predicted to increase. Specific applications for

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CNTs involve delivery systems for fertilizers and pesticides, consumer products and textiles, and

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waste water filtration.1-3 As such, the potential for environmental exposure can occur throughout

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the CNT lifecycle, yet little is known about bioaccumulation in the environment.4-8 CNT interactions in the aquatic environment are highly dependent on environmental

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conditions and CNT physicochemical properties. For example, in environments with high ionic

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strength or natural organic matter (NOM), CNTs may homoaggregate amongst themselves or

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heteroaggregate with other particles and settle in sediments.9 However, small CNT fractions

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may remain in the water column because of stabilizing agents used to prevent aggregation or by

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processes such as environmental transformation and sediment resuspension.6 Environmental

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CNT concentrations of 10-3 µg/L to 10-5 µg/L can occur in surface water and 1 µg/kg to 1 mg/kg

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in sediments.10, 11 Despite this, it is difficult to predict CNT concentrations at any given time.

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CNT bioaccumulation has been measured in Gambusia holbrooki (mosquitofish) and Pimephales

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promelas (fathead minnow, FHM).12, 13 This accumulation can hinder normal function, as CNTs

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can form physical blockages which lead to the organism’s inability to absorb nutrients.10-12, 14 Physiochemical properties of multi-walled carbon nanotubes (MWCNTs) such as outer

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diameter (OD) and length can influence bioavailability and toxicity in the aquatic environment.15, 16

Increased toxicity due to shading effects caused by aggregation was observed in Chlorella

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vulgaris (green algae) exposed to MWCNTs with larger ODs.17 Exposure to shorter MWCNTs

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(median length 0.17 µm) in zebrafish embryos led to severe developmental toxicity when

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compared to longer MWCNTs (median length 0.7 µm).18 When ingested, MWCNTs are known

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to bioaccumulate in the digestive tract of aquatic organisms such as D. magna and fish species.13, 14, 16, 19, 20

At the community level, MWCNTs impacted productivity and structure in freshwater

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food chains.21 Given these observed effects, the need exists to investigate trophic transfer of

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MWCNTs between individual species.

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The large surface area of MWCNTs allows components such as metals, polycyclic

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aromatic hydrocarbons (PAHs), NOM, and other compounds to bind to MWCNTs which are

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then ingested by aquatic organisms.9, 22, 23 Synergistic effects in D. manga have been measured

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with hydroxyl-functionalized MWCNTs at varying pH levels when combined with lead or

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nickel.24, 25 No studies have measured MWCNT exposure between trophic levels. Meanwhile,

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public use of copper in pesticides and herbicides in both agricultural and urban settings allow for

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a potential mixture with MWCNTs during runoff events. Particularly, nanocopper has been

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suggested as an emerging concern for use in pesticide applications.26 Copper II, the most

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abundant form of copper in surface water, can induce effects in fish such as decreased immune

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system function, increased metallothionein (MT) production, and olfaction impairment at trace

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concentrations.27-29 MT production is one of several coping mechanisms for metal toxicity in fish

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and can serve as a biomarker for metal exposure, as this protein is involved in metal regulation.30

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Specifically, metallothionein-2 (MT-2) participates in metal homeostasis stabilization, free

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radical scavenging, and expression regulation.27-30 MT-2 is detectable in liver, gill, and kidney

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tissues, but also resides at trace concentrations in blood, because plasma proteins serve as a

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vehicle for metal transport between organs.

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The present study evaluated the effect of OD size on MWCNT trophic transfer and bioaccumulation in the presence and absence of copper ions between two model aquatic species,

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D. magna and FHM, at environmentally relevant concentrations. Further, this study aimed to

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enhance the understanding of MWCNT toxicity and behavior in the aquatic food web.

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2. Materials and methods

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2.1 MWCNT characterization

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Non-functionalized MWCNTs of different outer diameters, 8-15 nm OD (MWCNT1, >95

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wt% purity, 95 wt%

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purity, Cu2+> Cd2+.39 Therefore, it is

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possible MWCNTs may have served as a vehicle for organism dietary exposure of copper. This

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has been demonstrated with increased EC50s in D. magna exposed to nickel suspensions

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containing oxidized-MWCNTs.24 Similarly, a trend was observed in the present study between

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MWCNT and copper in FHM exposed to MWCNT2s with the larger ODs, (Figures 2 and 3,

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Supplemental Data, Figure S6). In addition to dietary exposure, free-floating copper eliminated

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by D. magna may have been transported into FHM through their gills, though at a minimal level

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(< 3.5 µg/L).

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Figure 2. Average MWCNT concentrations in D. magna (n = 30 per treatment) and fathead

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minnow (FHM, n = 5 per treatment) for study II. D. magna were exposed for 3 d to MWCNTs

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(0.1 mg/L) and copper concentrations (0.01 mg/L). FHM were fed D. magna previously exposed

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to MWCNTs and copper. Treatments included a control, MWCNTs with 8-15 nm OD

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(MWCNT1+Cu), and MWCNTs with 20-30 nm OD (MWCNT2+Cu). Significant differences

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were compared between treatments of the same species using nonparametric statistical tests (p