Trophic transfer and accumulation of multi-walled carbon nanotubes in

1 hour ago - The increase in use of nanomaterials such as multi-walled carbon nanotubes (MWCNTs) presents a need to study their interactions with the ...
2 downloads 13 Views 596KB Size
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

Amanda Marie Cano, Jonathan by the American Chemical Society. 1155 Sixteenth D Maul, Mohammad A. Saed, Street N.W., Washington, DC 20036 Fahmida Irin,access Smit A. Shah, Micah Subscriber provided by READING Published by American UNIV Chemical Society. Copyright © American Chemical Society.

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

Environ. Sci. Technol., Just Society. 1155 Sixteenth Accepted Manuscript DOI: Street N.W.,• Washington,

20036 by READING Subscriber accessDC provided Published by American UNIV Chemical Society. Copyright © American Chemical Society.

10.1021/acs.est.7b03522 • Publication Date (Web): 20 Dec 2017 DownloadedEnvironmental from http://Science & Technology is published pubs.acs.org on December 23,Chemical 2017 by the American Society. 1155 Sixteenth Street N.W., Washington, 20036 by READING Subscriber accessDC provided Published by American UNIV Chemical Society. Copyright © American Chemical Society.

Just Accepted

Environmental Science & “Just Accepted” manuscripts have been pee Technology is published online prior to technical editing, formatting fo by the American Chemical Sixteenth as a fre Society provides Society. “Just 1155 Accepted” Street N.W., Washington, dissemination of scientific material as soon a DC 20036 by Subscriber access provided READING Published by American UNIV Chemical Society. Copyright © American Chemical Society.

appear in full in PDF format accompanied by a fully peer reviewed, but should not be conside Environmental ScienceObject & readers and citable by the Digital Iden Technology is published to authors. Therefore, the “Just Accepted” W by the American Chemical Society. 1155 Sixteenthis technica in the journal. After a manuscript Street N.W., Washington, Accepted” Web site and as an ASA 20036published Subscriber accessDC provided by READING Published by American UNIV Chemical Society. Copyright © American Chemical Society.

changes to the manuscript text and/or grap and ethical guidelines that apply to the jou Science or consequences Environmental arising from the &use of info Technology is published by the American Chemical Society. 1155 Sixteenth Street N.W., Washington, 20036 by READING Subscriber accessDC provided Published by American UNIV Chemical Society. Copyright © American Chemical Society.

Page 1 ofEnvironmental 26 Science & Technology MWCNTs + Cu2+

MWCNTs

Cu2+

ACS Paragon Plus Environment

Environmental Science & Technology

1

Trophic transfer and accumulation of multi-walled

2

carbon nanotubes in the presence of copper ions in

3

Daphnia magna and fathead minnow (Pimephales

4

promelas)

5

6

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

7

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

8 9 10 11 12 13 14 15

1

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

4

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

Station, TX, USA

16 17 18 19

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

ACS Paragon Plus Environment

Page 2 of 26

Page 3 of 26

Environmental Science & Technology

2

20

Abstract

21

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

22

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

23

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

24

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

25

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

26

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

27

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

28

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

29

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

30

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

31

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

32

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

33

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

34

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

35

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

36

environmental behavior.

37

ACS Paragon Plus Environment

Environmental Science & Technology

Page 4 of 26

3

38

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

39 40

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

41

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

42

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

43

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

44 45

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

46

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

47

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

48

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

49

processes such as environmental transformation and sediment resuspension.6 Environmental

50

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

51

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

52

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

53

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

54

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

55 56 57

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

58

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

59

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

60

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

ACS Paragon Plus Environment

Page 5 of 26

Environmental Science & Technology

4 61 62

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

63

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

64

MWCNTs between individual species.

65

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

66

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

67

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

68

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

69

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

70

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

71

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

72

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

73

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

74

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

75

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

76

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

77

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

78

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

79

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

80

vehicle for metal transport between organs.

81 82

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,

ACS Paragon Plus Environment

Environmental Science & Technology

Page 6 of 26

5 83

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

84

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

85 86

2. Materials and methods

87

2.1 MWCNT characterization

88

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

89

wt% purity, 95 wt%

90

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

273

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

274

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

275

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

276

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

277

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

ACS Paragon Plus Environment

Page 15 of 26

Environmental Science & Technology

14 278

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

279

(< 3.5 µg/L).

280 281

282 283

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

284

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

285

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

286

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

287

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

288

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