Mechanisms of Arsenic Sequestration by Prosopis juliflora during the

Dec 14, 2017 - Department of Soil, Water, and Environmental Science, University of Arizona, 1177 East Fourth Street, Shantz 429, Tucson, Arizona 85721...
7 downloads 11 Views 2MB Size
Subscriber access provided by Gothenburg University Library

Article

Mechanisms of arsenic sequestration by Prosopis juliflora during phytostabilization of metalliferous mine tailings Corin M Hammond, Robert Aubrey Root, Raina M Maier, and Jon Chorover Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.7b04363 • Publication Date (Web): 14 Dec 2017 Downloaded from http://pubs.acs.org on December 20, 2017

Just Accepted “Just Accepted” manuscripts have been peer-reviewed and accepted for publication. They are posted online prior to technical editing, formatting for publication and author proofing. The American Chemical Society provides “Just Accepted” as a free service to the research community to expedite the dissemination of scientific material as soon as possible after acceptance. “Just Accepted” manuscripts appear in full in PDF format accompanied by an HTML abstract. “Just Accepted” manuscripts have been fully peer reviewed, but should not be considered the official version of record. They are accessible to all readers and citable by the Digital Object Identifier (DOI®). “Just Accepted” is an optional service offered to authors. Therefore, the “Just Accepted” Web site may not include all articles that will be published in the journal. After a manuscript is technically edited and formatted, it will be removed from the “Just Accepted” Web site and published as an ASAP article. Note that technical editing may introduce minor changes to the manuscript text and/or graphics which could affect content, and all legal disclaimers and ethical guidelines that apply to the journal pertain. ACS cannot be held responsible for errors or consequences arising from the use of information contained in these “Just Accepted” manuscripts.

Environmental Science & Technology is published by the American Chemical Society. 1155 Sixteenth Street N.W., Washington, DC 20036 Published by American Chemical Society. Copyright © American Chemical Society. However, no copyright claim is made to original U.S. Government works, or works produced by employees of any Commonwealth realm Crown government in the course of their duties.

Page 1 of 33

Environmental Science & Technology

For Table of Contents Only 44x25mm (300 x 300 DPI)

ACS Paragon Plus Environment

Environmental Science & Technology

1

Mechanisms of arsenic sequestration by Prosopis

2

juliflora during phytostabilization of metalliferous

3

mine tailings

4

Corin M. Hammond, Robert A. Root, Raina M. Maier, Jon Chorover*

5

Department of Soil, Water and Environmental Science, University of Arizona, 1177 E 4th St,

6

Shantz 429, Tucson, AZ 85721

7

KEYWORDS: arsenic speciation, mine tailings, mesquite, Prosopis juliflora, XAS, XRF

8

imaging, phytoaccumulation

Page 2 of 33

9

ACS Paragon Plus Environment

1

Page 3 of 33

Environmental Science & Technology

10

ABSTRACT. Phytostabilization is a cost-effective long-term bioremediation technique for

11

immobilization of metalliferous mine tailings. However, the biogeochemical processes affecting

12

metal(loid) molecular stabilization and mobility in the root zone remain poorly resolved. Roots

13

of Prosopis juliflora grown for up to 36 months in compost-amended pyritic mine tailings from a

14

federal Superfund site were investigated by micro-scale and bulk synchrotron X-ray absorption

15

spectroscopy (XAS) and multiple energy micro X-ray fluorescence ((ME)-µXRF) imaging to

16

determine iron, arsenic, sulfur speciation, abundance, and spatial distribution. Whereas

17

ferrihydrite-bound As(V) species predominated in the initial bulk mine tailings, rhizosphere

18

speciation of arsenic was distinctly different. Root associated As(V) was immobilized on the root

19

epidermis bound to ferric sulfate precipitates and within root vacuoles as trivalent As(III)-SH3

20

complexes. Molar Fe:As ratios of root epidermis tissue was 2x times higher than the 15%

21

compost-amended bulk tailings growth medium. Rhizoplane associated ferric sulfate phases that

22

showed a high capacity to scavenge As(V) were dissimilar from the bulk tailings mineralogy as

23

shown by XAS and XRD, indicating a root surface mechanism for their formation or

24

accumulation.

ACS Paragon Plus Environment

2

Environmental Science & Technology

Page 4 of 33

25

1. INTRODUCTION

26

Arsenic is a metalloid of significant concern in the Earth’s critical zone because of its proven

27

toxic effects on humans and animals and disruption to plant metabolism.1-3 In base-metal mining

28

regions in the arid and semi-arid southwestern United States, arsenic is naturally abundant as

29

arsenopyrite (FeAsS). When exposed to oxygen and water by natural weathering, arsenopyrite

30

dissolves oxidatively, releasing arsenate (AsO43-) and protons to solution. This geochemical

31

transformation is observed at the legacy mine tailings located in the Iron King Mine and

32

Humboldt Smelter Superfund site (IKMHSS, EPA #: AZ0000309013) in central Arizona, USA.4

33

The surficial mineralogy of the IKMHSS tailings is dominated by high iron and sulfur content

34

with the major contaminant of concern being arsenic (ca. 2,100 mmol kg-1 Fe; 3,100 mmol kg-1

35

S; 40 mmol kg-1 As).4, 5 Under the oxidizing conditions of the surficial IKMHSS tailings, ferrous

36

sulfides naturally weather to form ferric (oxyhydr)oxides and (hydroxy)sulfates.4, 5 These arsenic

37

enriched secondary minerals have the potential for off-site transport as geo-dust in wind-driven

38

erosion.6-9 One potential low-cost, long-term remediation method proposed for such abandoned

39

mine tailings involves phytostabilization – i.e., the establishment of a sustainable vegetation

40

“cap” to effectively contain legacy tailings particles and the associated metal(loid)s including

41

arsenic, thereby diminishing contaminant exposure to adjacent communities.10-15 Compost-

42

assisted direct planting during tailings phytostabilization has the goals of immobilizing

43

contaminants against leaching or off-site particulate transport, establishing a positive feedback to

44

improved soil health and fertility, while decreasing contaminant leaching to groundwater.16,

45

However, the changes in metal(loid) speciation that occur as a result of root proliferation in the

46

porous tailings media, and that control stabilization at the molecular scale, remain poorly

47

resolved.

17

ACS Paragon Plus Environment

3

Page 5 of 33

48

Environmental Science & Technology

Prior studies have shown that both arsenate (HxAsO4x-3) and arsenite (HxAsO3x-3) may be

49

assimilated by plant roots with arsenate subsequently being reduced to arsenite.3,

50

observed within plant tissue has been characterized as As(III) bound by three thiol groups often

51

attributed to phytochelatins (PC), glutathione, or cysteine-like compounds.18, 19, 21-33 Prior work

52

proposes that arsenic-bound thiol complexes may be immobilized and sequestered in root cell

53

vacuoles as a detoxifying mechanism leading to potentially high localized accumulation in

54

arsenic tolerant species, but direct evidence is scant.2,

55

previously in laboratory systems is Prosopis juliflora (mesquite). This halophytic tree, tolerant to

56

growth in compost-amended IKMHSS tailings, is part of a field-scale experiment assessing long-

57

term feasibility of a direct planting phytostabilization.35 P. juliflora plants grown under stress in

58

arsenic spiked media 10 have been shown to exhibit both As(V) and As(III)-SH3 complexes either

59

associated with or in root tissue 19, but there are no prior studies of rhizosphere arsenic speciation

60

deriving from arsenic-bearing mine tailings systems.

21, 33, 34

18-20

Arsenic

Among such plants studied

61

Additional mechanisms of As detoxification have been reported. For example, the wetland

62

plant species rice and cattail, which translocate oxygen to the root zone in water-logged anoxic

63

paddy soils, have been shown to immobilize arsenic via root-associated ferric deposits or iron

64

plaques with high arsenate sorption affinity.32 This root-associated ferric iron37 has been

65

characterized as ferric (hydr)oxides similar to ferrihydrite and goethite.29, 32, 37-41 However, root

66

zone biogeochemical conditions in semi-arid and arid mine tailings are distinctly different from

67

paddies and wetlands, and there are no prior detailed investigations of the partitioning and

68

speciation of arsenic in root tissue of P. juliflora as it occurs in situ during mine tailings

69

phytostabilization.

70

Herein we report observation of Fe(III) sulfate plaques on root surfaces in a sulfate rich

71

environment and direct observation of As(III)-SH3 in root vacuoles using micro (1 µm2 pixel)

ACS Paragon Plus Environment

4

Environmental Science & Technology

Page 6 of 33

72

imaging technology. The aim of the present study was to determine the contribution of P.

73

juliflora root chemical activity to long-term phytostabilization of arsenic in pyritic mine tailings

74

in a semi-arid climate. By combining X-ray absorption spectroscopy (XAS), multiple energy

75

micro X-ray fluorescence ((ME)-µXRF) imaging, and bulk elemental analysis, this study reveals

76

long term (up to 3 years) stabilization of arsenic by P. juliflora. Arsenic sequestration is detected

77

in two distinct speciation pools spatially partitioned as As(V) associated with Fe(III) sulfate

78

plaques on root surface and thiol-bound As(III) in vacuoles of the root cortex.

79 80

2. MATERIALS AND METHODS

81 82

2.1 Sample Collection. Compost-amended and unamended tailings were collected at the

83

IKMHSS phytostabilization field site, which is described in SI and detailed elsewhere.4,5,10

84

Briefly, the federal Superfund site is a pyritic tailings pile containing bulk arsenic concentrations

85

of ca. 4 g kg-1 from arsenopyrite that has undergone oxidative weathering in the top 2 m over the

86

past 50 y since deposition. The site is now the focus of a large-scale phytostabilization trial. The

87

root systems of two field site mesquite (P. juliflora) plants were harvested at 1 and 3 years of

88

growth, transported on ice to the laboratory, and stored at -15 oC until analysis. Additionally, to

89

mimic early plant growth under field conditions, greenhouse plants were grown in surficial

90

tailings (0-20 cm depth) from IKMHSS with the same field site mixture of compost amendment

91

(Arizona Dairy Compost LLC, Anthem, AZ), at a mass concentration of 150 g kg-1. Following

92

previous work, P. juliflora seeds (Desert Nursery, Phoenix, AZ) were sown in four replicate pots

93

(30 each) at a depth of 0.5 cm.35 Quadruplicate pots produced 6 ± 3 plants, and 1 to 3 plants were

94

harvested from each pot on days 41, 76, and 102 for analysis of metal(loid) phytoaccumulation.

95

Greenhouse plant materials were segregated into roots, shoots, and leaves. All plant samples

ACS Paragon Plus Environment

5

Page 7 of 33

Environmental Science & Technology

96

were freeze-dried and sectioned using a stainless steel blade. For bulk analysis, tissue was hand-

97

ground by mortar and pestle (2013 field samples) or mechanically ground using a dedicated

98

KitchenAid® Blade Coffee Grinder (Model #BCG211OB) with the spice grinder attachment

99

(2015 field samples and greenhouse samples). Samples were stored at -15oC and transported on

100

ice leading up to analysis. Three grab samples of the tailings-compost mixture were freeze dried,

101

subjected to microwave-assisted digestion (CEM Corporation, MARS 6, Matthews, NC, USA)

102

following EPA Method 3051A, and analyzed for total metal(loid) content by ICP-MS (Perkin

103

Elmer, ELAN, Waltham, MA, USA) and total sulfur content by CHNSO analyzer (Costech

104

Analytical Tech, Inc., ECS 4010, Valencia, CA, USA). Additional detail regarding plant sample

105

collection and tissue preparation is described in the SI.

106

2.2 X-ray spectroscopy.

Root samples were analyzed with K-edge XAS for speciation of

107

arsenic, iron and sulfur. Spectra were collected at Stanford Synchrotron Radiation Lightsource

108

(SSRL) on beam line (BL) 11-2 for As and Fe and BL 4-3 for S. Beam energy was calibrated on

109

an As foil with the main edge inflection assigned 11,867 eV, Fe foil with the first edge inflection

110

assigned 7,112 eV, and sodium thiosulfate with the first peak (S-S) assigned 2,472.02 eV. At BL

111

11-2, fluorescence was quantified with a 100-element solid-state Ge detector with a LN2 cryostat

112

sample holder (∼ 77 K, see SI for XAS setup and analysis details). Sulfur XAS on BL 4-3 was

113

monitored under He(g) with a passivated implanted planar silicon (PIPS) detector at room

114

temperature. Spectral processing was performed with SixPack

115

correction) and Athena

116

conducted with Athena and Artemis.

117

reduction are provided in the SI.

43

42

(average and deadtime

(normalization and background subtractions), and spectral fitting was 43

Additional details of bulk XAS collection and data

118

2.3 µXRF Imaging Collection and Analysis. Two field-collected root segments were washed

119

and dried as described (see SI) prior to embedding in Paraplast Plus® wax with no fixing agent,

ACS Paragon Plus Environment

6

Environmental Science & Technology

Page 8 of 33

120

microtomed to 30 µm sections, and placed on quartz slides (Part No. CGQ-0640-01 Chemglass,

121

Inc.). Thin section were imaged and analyzed with µXRF, µXAS, and XANES at the SSRL BL

122

2-3 (As, Fe, K) with a step size of 2.5 µm2 a dwell time of 50 ms, and BL 14-3 (S) with a step

123

size of 5.0 µm2 and a dwell time of 75 ms. Speciation maps for As were collected at multiple

124

energies across the absorption edge and µXANES scans were collected at points of interest (See

125

SI for imaging details). Higher resolution As speciation maps were collected at Brookhaven

126

National Laboratory National Synchrotron Light Source II (NSLS-II) SRX beam line with a step

127

size of 1.0 µm2 and a dwell time of 300 ms. Data were collected at multiple energies across the

128

As edge and µXANES spectra were collected at select spots (see SI for details). Maps were

129

processed (deadtime corrected, normalized, PCA, and XANES imaging) using the software

130

package SMAK.

131

intensity of reference endmember spectra defined by LCF of µXANES spot analysis from the

132

root sample to the multiple energy stacked map. Data reduction of all µXANES was performed

133

as above for bulk XAS.

54

Speciation maps were fit by applying a matrix of normalized spectral

134

3. RESULTS AND DISCUSSION

135

3.1 Elemental Distribution. Root tissue components (epidermis, cortex, and stele) of P.

136

juliflora plants grown in IKMHSS tailings media exhibited dissimilar concentrations of As, S

137

and Fe (Table 1), where components are morphologically defined in Figure S1. To gauge bulk

138

scale phytoaccumulation by P. juliflora, As, S, and Fe molar concentrations as well as molar

139

ratios (Fe:As and S:Fe) within plant tissue were compared to reference standard plant average

140

values,44 and relevant growth media for this study (i.e., compost, unamended tailings and 15%

141

compost-amended tailings) (Table 1). Notably, the total sulfur content of all root components

142

were within the range reported for plant averages with leaves, whole roots, epidermis, and cortex

143

exhibiting concentrations an order of magnitude higher than the shoot or root stele. The root

ACS Paragon Plus Environment

7

Page 9 of 33

Environmental Science & Technology

144

components of epidermis, cortex, and stele for larger roots (2-4 mm and 5-15 mm diameter) of

145

plants grown in field conditions in IKMHSS tailings exhibited preferential sequestration of As

146

and Fe in the following order: epidermis > cortex > stele (Table 1). Both arsenic and iron

147

exceeded the standard plant average values for whole roots and epidermis (Table 1). Arsenic was

148

preferentially phytoaccumulated in root tissue compared to shoots or leaves, signifying

149

subsurface arsenic sequestration. However Fe:As molar ratios increased with growth time in the

150

latter (Table 1). The Fe:As molar ratio of whole root tissue and epidermis were about the same or

151

slightly lower than those of bulk tailings and half the value of 15% compost-amended tailings

152

mixture that the plants were grown in indicating enrichment of As relative to Fe in the rhizoplane

153

(Table 1). While arsenic is enhanced with respect to iron in the epidermis compared to the 15%

154

compost amended tailings growth medium, the S:Fe molar ratio of the epidermis tissue is similar

155

to that of the growth medium. Sulfur and iron concentrations are both higher in the root

156

epidermis compared to the internal root and above ground biomass samples due to development

157

of iron and sulfur containing minerals strongly associated with the root surface (Table 1).

158

3.2 X-ray Fluorescence. Roots of P. juliflora were further investigated for arsenic microscale

159

phytoaccumulation mechanisms. A light micrograph of P. juliflora in thin section grown at the

160

IKMHSS tailings field site for 12 months displays epidermis, cortex, and stele external and

161

internal structure (Figure 1a). The water and nutrient transport channel of the stele is resolved by

162

a strong potassium fluorescence intensity (Figure 1b). The total sulfur K-edge μXRF imaging

163

reveals that sulfur is ubiquitous throughout the root cross section (Figure 1c). Gaussian peak

164

fitting of bulk S XANES collected on mesquite root samples 2-4 mm and 5-15 mm in diameter

165

exhibit a strong sulfate signal and co-localization of sulfate and organic thiol in all three root

166

components (epidermis, cortex, and stele) (Figure S2, Table S1).

167

ACS Paragon Plus Environment

8

Environmental Science & Technology

Page 10 of 33

168

ACS Paragon Plus Environment

9

Page 11 of 33

169

Environmental Science & Technology

Table 1. Total elemental concentrations for P. juliflora samples.

b

Whole Root Whole Rootb Whole Rootb Whole Rootc Whole Rootc Shootb Shootb Shootb Leavesb Leavesb Leavesb Epidermis 2-4 mm diameterc Epidermis 2-4 mm diameterc Epidermis 5-15 mm diameterc Epidermis 5-15 mm diameterc Cortex 2-4 mm diameterc Cortex 2-4 mm diameterc Cortex 5-15 mm diameterc Cortex 5-15 mm diameterc Stele 2-4 mm diameterc Stele 2-4 mm diameterc Stele 5-15 mm diameterc Stele 5-15 mm diameterc Standard Plant Averagee Bulk Tailings 0-20 cmf 15 wt% Compost Mixturef Compostf

170 171 172 173 174

Growth Time Months 1 2 3 12 36 1 2 3 1 2 3 12 36 12 36 12 36 12 36 12 36 12 36

Total Concentration (µmol g-1)a S 167 (53) 114 (38) 105 (32) 202 (1) 166 (6) 47 (1) 35 (7) 23 (5) 70 (4) 132 (26) 140 (27) 153 (22) 202 (6) 204 (12) 165 d 101 (0) 125 (32) 55 (23) 47 (2) 86 (17) 36 (2) 39 (1) 20 (4) 18.7 - 311.9 2,500 (300) 2,050 (80) 274 (26)

As 0.29 (0.14) 0.50 (0.31) 0.20 (0.11) 2.15 (0.33) 1.03 (0.47) 0.01 (0.00) 0.01 (0.00) 0.00 (0.00) 0.11 (0.04) 0.08 (0.03) 0.09 (0.03) 1.61 (0.21) 3.13 (0.34) 3.64 (0.76) 2.75 (0.13) 0.21 (0.04) 0.06 (0.02) 0.15 (0.03) 0.08 (0.01) 0.12 (0.04) 0.02 (0.01) 0.07 (0.03) 0.02 (0.01) 0.00 - 0.02 54 (6) 27.4 (0.4) 0.013 (0.004)

Fe 11 (4) 20 (13) 9 (5) 41 (6) 35 (14) 0.58 (0.14) 0.79 (0.44) 0.52 (0.18) 3.11 (0.87) 4.23 (0.44) 6.53 (1.68) 51.7 (6.7) 99.9 (9.8) 117.8 (18) 105 (8) 4.89 (1.44) 2.04 (0.11) 4.97 (1.34) 2.5 (0.2) 2.67 (0.5) 0.55 (0.09) 2.17 (0.35) 0.57 (.08) 0.09 - 3.58 1950 (200) 1589 (25) 65 (19)

Molar Ratio Fe:As 37 40 44 19 34 54 73 70 29 56 71 32 32 32 38 23 33 33 30 23 25 31 30 36 58 5,000

Molar Ratio S:Fe 15 6 12 5 5 81 45 44 23 31 21 3 2 1.7 1.6 21 61 11 19 32 65 18 36 1.3 1.3 4.2

a

Total elemental analysis by ICP-MS after microwave digestion of sub-sectioned components. b Greenhouse grown P. juliflora, average and standard deviation (in parentheses) of quadruplicate samples. c P. juliflora from IKMHSS field site, average and standard deviation reported from duplicate composite sample. d n=1 due to limited sample. e Range reported is the average content of elements expected to occur in tissue of a typical plant44. f Results from triplicate analysis.

ACS Paragon Plus Environment

10

Environmental Science & Technology

Page 12 of 33

175 176

Figure 1. Micro-scale XRF imaging analysis of P. juliflora root. Images depict μXRF maps and

177

(ME)-μXRF imaging for a 30 µm thick P. juliflora root thin section from a plant grown at the

178

IKMHSS tailings amended with 15% compost and lime for one year. Panels show (a) light

179

microscope image with dotted lines delineating the root epidermis, cortex, and stele, (b) total

180

potassium, (c) total sulfur, (d) total iron(e) As(V) (f) As(III)-SH3 (g) and a tricolor plot

181

overlaying Fe, As(V), and As(III)-SH3 in a 10:1:1 ratio of intensity scales. The inset shows (h)

182

total iron, (i) As(V), (j) As(III)-SH3, and (k) a tricolor plot overlaying Fe, As(V), and As(III)-SH3

183

collected with a 6.25x increase in spatial resolution. Circles identify regions of interest (ROIs)

184

that were probed by µXANES analysis (see Fig. 2). White dotted lines in h-k delineate the root

185

interior from the epidermis. Color intensity corresponds to the fluorescence signal of each

186

chemical component per volume in each pixel, mapped at 2.5 µm2 (b-g) and 1 µm2 (h-k). Micro

187

XRF maps were collected at 11,880 eV (K, Fe) and 2,487.5 eV (S). Arsenic speciation maps

ACS Paragon Plus Environment

11

Page 13 of 33

Environmental Science & Technology

188

were generated from μXANES matrix analysis from μXRF maps collected at 11,869 eV, 11,872

189

eV, 11,875 eV, and 11,880 eV (Table S2).

190 191

3.2.1 Fe Speciation. Iron μXRF imaging shows most Fe associated with the root epidermis

192

(Figure 1d). Regions of interest selected for Fe µXANES are identified by circles (Figure 1d).

193

The averaged Fe K-edge µXANES and the bulk Fe K-edge EXAFS reveal that the iron plaque

194

deposit at the epidermis from Figure 1d is well described by a linear combination fit (LCF) by

195

the

196

[(Fe8IIIO8(SO4)(OH)6] (Figure 2b, fit parameters reported in Table S3). The root bark Fe K-edge

197

EXAFS is well fit to jarosite (50.4%), schwertmannite (38.9%), and chlorite (5.9%), as are the

198

Fe K-edge normalized XANES and 1st derivative XANES data (Figure 2b, 2c). X-ray diffraction

199

(XRD) of the bulk root bark reveals amorphous or poorly crystalline morphology of the ferric

200

sulfate root plaque with a small crystalline contribution corresponding to the highest intensity

201

peaks for jarosite (Figure S5, see SI for XRD collection and data reduction). While a jarosite

202

signal in the XRD of the bark is evident, signal contribution from poorly-crystalline

203

schwertmannite and high arsenic content likely account for the amorphous morphology detected

204

for the root-associated iron plaque.45, 46

ferric

sulfate

minerals

jarosite

[XFe3III(SO4)2(OH)6]

and

schwertmannite

205

3.2.2 As Speciation. Principal components analysis (PCA) conducted on the As µXRF multiple

206

energy maps47, 48 revealed the existence of two unique arsenic component pools in the root thin

207

section sample. Arsenic K-edge µXANES performed with a 2.5 µm2 beam size were collected

208

from both pools according to regions of interest (ROIs) 1-10 shown (Figure 1e). Arsenic

209

speciation of two components As(V)-O and As(III)-SH3 was determined from LCFs using

ACS Paragon Plus Environment

12

Environmental Science & Technology

Page 14 of 33

210

endmember As K-edge µXANES spectra (Figure 2a) collected from the thin section sample.

211

Arsenic XANES maps for As(V) and As(III)-SH3 (Figure 1e and 1f) were produced from As

212

μXRF images collected at 11,869 eV, 11,872 eV, 11,875 eV, and 11,880 eV by applying a

213

XANES signal intensity matrix of normalized references (Table S2). The dominant arsenic

214

species associated with the root epidermis was As(V) (Figure 1e), whereas As(III)-SH3 was

215

concentrated in the cortex (Figure 1f). A tricolor plot of Fe, As(V), and As(III)-SH3 with color

216

intensity scales ranging from 0-500 counts for Fe (red) and 3-50 counts for As(V) (blue) and

217

As(III)-SH3 (green) was constructed from the µXRF maps and shows strong co-localization of

218

Fe and As(V) at the root epidermis, displayed as purple (Figure 1g, see Figure S3 for

219

quantification of co-localization ). Thiol-bound arsenic [As(III)-SH3] appears to be

220

compartmentalized in pockets located in the cortex at the 2.5 µm2 pixel size (Figure 1g). The

221

breakout images (Figure 1h-k) show that further probing of the root thin section by As µXANES

222

and µXRF imaging using the same method but with a 1 µm2 pixel size, confirmed the presence

223

of concentrated pockets of thiol-bound arsenic (green) in the cortex and strong co-localization

224

between As(V) (blue) and Fe(III) (red) in tricolor plot (Figure 1k) compiled from ROIs i-viii

225

(Figure 1i). Imaging with a 1 µm2 beam spot size provides ca. six-fold enhancement of spatial

226

resolution compared to the 2.5 µm2 beam spot maps. At this higher spatial resolution the As(III)-

227

SH3 is shown to be isolated in pockets of approximately 9 µm cross-sectional diameter and

228

isolated from the Fe(III) and As(V) concentrated at the root epidermis (indicated by dotted white

229

line) (Figures 1 i-k). At the lower resolution As(III)-SH3 could only be observed as diffused

230

throughout the cortex. Resolving these small structural features of isolated As(III)-SH3 storage

231

provides evidence for immobilization and detoxification. Plant vacuole size is highly variable but

232

it is commonly reported that they can take up to 80% of a plant cell’s volume where a plant cell

ACS Paragon Plus Environment

13

Page 15 of 33

Environmental Science & Technology

233

which has been shown to measure approximately 10 µm in diameter in mesquite roots.49 Arsenic

234

µXANES collected at the ROIs identified in Figure 1(e, i) were fit by linear combinations of end

235

member spectra collected from the thin section (Figure 2a, Table 2). Endmembers were

236

identified for As(III)-S (1, i) and As(V) (10, vii) (Figure 2a, Table 2). Semi-quantitative analysis

237

of As, Fe, and K concentrations of a mesquite root grown for one year at the tailings field-site

238

shows As 0-1 µg cm-2, Fe 0-100 µg cm-2, and K 0-100 µg cm-2 (Figure S4).

239

Arsenic K-edge bulk EXAFS data were collected for P. juliflora cortex tissue of roots 2-4 mm

240

in diameter from a plant grown at the IKMHSS field site to measure the oxidation state and

241

speciation of arsenic to confirm the presence and proportional abundance of As(III)-SH3

242

complexes (Figure 3). Shell-by-shell fit results indicate cortex tissue comprises a mixture of

243

63.5% As(III)-SH3 where arsenic is trigonally coordinated to sulfur and 36.5% As(V) with As

244

tetrahedrally coordinated with oxygen (Figure 3, fit in Table S4). Wavelet analysis of the shell

245

by shell fit of bulk P. juliflora root cortex tissue As k3 weighted EXAFS identifies two distinct

246

arsenic species contributions (As(V)-O and As(III)-S), and is provided in the SI (Figure S7).

247

FEFF path contributions are attributed to single scattering paths AsV-O (CN = 4, tetrahedral, 1.69

248

Å interatomic distance) and a multiple scattering contribution corresponding to the AsV-O-O

249

path (3.09 Å interatomic distance) within the arsenate tetrahedron and AsIII-S (CN = 3, trigonal,

250

2.28 Å interatomic distance) (Figure 3, fits shown in Table S3).

251

The observed interatomic distance of 2.28 Å between As(III) and S in the plant cortex is in

252

agreement with previous observations of As(III)-SH3 complexes found in plant tissue and

253

organic peat samples that have been reported to range from 2.24-2.34 Å.19,

254

validation, As-tris-DMSA, As-tris-cysteine, and As-tris-glutathione were synthesized21,

255

analyzed by As EXAFS, and fit by the same method to confirm the As-S single scattering shell

256

of the mesquite cortex sample. The chemical structures of DMSA, L-cysteine, and glutathione

21, 24, 25, 36

For

ACS Paragon Plus Environment

14

Environmental Science & Technology

Page 16 of 33

257

are provided in the SI along with the shell-by-shell fit of As-tris-glutathione and the

258

corresponding fit statistics (Figure S6, Table S5). Arsenic has been shown to coordinate with

259

three sulfhydryl groups of humic acid (As-S interatomic distances of 2.24-2.34 Å),24 and with

260

three organic sulfur groups in peat (As-S interatomic distances of 2.24-2.25 Å).25 Similar

261

arsenic-thiol interactions have been shown to occur within the tissue of plants grown in arsenic-

262

contaminated growth media. Previous studies of mesquite plants grown under stress of high

263

arsenic spiked agar medium21,

264

interior with an As-S interatomic distance of 2.24-2.26 Å.19 However, we show

265

distribution of As(III)-SH3 in discrete ~9 μm pockets, supporting the common claim that root

266

vacuoles serve as sinks for As(III)-SH3 compartmentalization and storage as a potential

267

detoxifying mechanism for high arsenic-containing environments.

36

and soil19,

26

exhibit As(III)-SH3 complexation in the root in situ

268 269

Figure 2. Speciation analysis of As and Fe in P. juliflora roots and IKMHSS tailings by XAS.

270

(a) Normalized arsenic μXANES are shown for regions of interest (ROIs) identified in Figure 1

ACS Paragon Plus Environment

15

Page 17 of 33

Environmental Science & Technology

271

and were collected with a 2.5 µm2 (1-10) and 1 µm2 (i-vii) beam. Linear combination fits (LCF)

272

depicted by red dotted lines were performed using ROI endmember spectra identified at the top

273

and bottom by solid black lines with no fit represented, values are tabulated in Table 2. The

274

“Bulk” As XANES of the surficial tailings amended with 15% compost is shown for reference to

275

the growth medium in panel (a). The significant contribution of both As(III)-SH3 (dark grey) and

276

As(V) (light grey) are highlighted for the As μXANES LCF of ROI (8) and (v). Iron XAS LCF

277

are shown for the root “Plaque” composite signal from the four thin section ROIs, the root

278

“Bark” collected using bulk XAS, and the “Bulk” amended IKMHSS tailings for (b) Fe K-edge

279

normalized and 1st derivative XANES, and (c) Fe K-edge k3-weighted EXAFS. Iron XAS LCF

280

values are reported in Table S3. Solid black lines are data; stippled red lines are least-squares

281

best fits. References provided for comparison include ferrihydrite (Fh.), hydronium jarosite,

282

(Jar.), schwertmannite (Sch.), chlorite (Chl.), and pyrite (Pyt.). Shaded grey panels are intended

283

to identify peak energies for As species (As(III)-SH3 and As(V)) and Fe minerals.

ACS Paragon Plus Environment

16

Environmental Science & Technology

Page 18 of 33

284

Table 2. Arsenic K-edge μXANES linear combination fit statistics. Samples correspond to ROIs

285

defined in Figure 1(e, i).

286 287 288

2.5 µm2 beam As K-edge normalized µXANES fit (%) ∑Asi As-XANES point As(III)-S As(V) total Red χ2 1 As(III)-S 100 0 100 na 2 96 3 99 0.002 3 95 3 98 0.002 4 94 3 97 0.003 5 94 4 98 0.002 6 87 11 98 0.002 7 81 17 98 0.002 8 41 55 96 0.001 9 9 85 94 0.003 10 As(V) 0 100 100 na 2 b. 1 µm beam As K-edge normalized µXANES fit (%) ∑ Asi As-XANES point As(III)-S As(V) total Red χ2 i As(III)-S endmember 100 0 100 na ii 100 2 102 0.001 iii 99 2 101 0.001 iv 93 7 100 0.001 v 72 28 100 0.001 vi 7 91 98 0.001 vii 1 97 98 0.001 viii As(V) endmember 0 100 100 na Percent fit (%) for contributing component species, total fit (∑Asi), and reduced chi squared (χ2) using endmember XANES collected from the thin section root sample are reported for spectra collected using (a) 2.5 µm2 (b) and 1.0 µm2 beam. a.

ACS Paragon Plus Environment

17

Page 19 of 33

Environmental Science & Technology

289

Ecosystem-scale impacts of these sequestration mechanisms can be evaluated based on

290

previous research on root biomass in a mature (mean parameters: 3.4 ± 0.1 m height, 5.1 ± 0.2 m

291

canopy diameter, 5.8 ± 0.4 basal stems) mesquite savanna of north Texas, USA (mean annual

292

precipitation of 665 mm).

293

volume of 25.44 m3 of soil as reported in that study indicates an approximate subsurface arsenic

294

phytostabilization capacity by P. juliflora roots of 11 mmol As per tree. The concentration of

295

arsenic in the IKMHSS tailings in the top half meter is 53 mmol kg-1 while the bulk density of

296

the IKMHSS tailings is about 3.4 kg m-3. 4, 10 Therefore, the total arsenic that would be contained

297

in the live mesquite root growth volume determined by Ansley et al. 55 represents ca. 0.2% of the

298

total arsenic in the bulk tailings. This value does not account for the high fractional fine root

299

turnover that occurs on an annual basis, and that could lead to an accumulation of the observed

300

arsenic species in senescent root tissue. This work reveals key features of arsenic

301

phytostabilization in mine tailings that have not been previously reported, including the

302

coexistence in close proximity of plant-root stabilized arsenic partitioned into distinct thiol- and

303

ferric-sulfate bound species whose formation was evidently promoted by root biogeochemistry

304

(Figure 1). Previous research on the IKMHSS tailings revealed that the limited water through-

305

flux at the semi-arid site leads to persistence of sulfate that, in turn, enhances the thermodynamic

306

stability of Fe(III)-sulfate minerals, dominantly jarosite, as products of pyrite (and arsenopyrite)

307

weathering (Figure 4).5

55

Assuming a total root biomass of 11 ± 3.6 kg tree-1 contained to a

308

Arsenic and iron K-edge XANES, EXAFS, and XRD data (Figure 2) suggest a disordered,

309

arsenic-enriched, schwertmannite-like ferric hydroxysulfate structure for root epidermis-

310

associated iron plaque that is distinct and chemically different from the surrounding growth

311

medium of 15% compost-amended IKMHSS mine tailings. Although previous research has

312

shown Fe strongly associated with root surfaces, as Fe-(oxyhydr)oxide minerals such as

ACS Paragon Plus Environment

18

Environmental Science & Technology

Page 20 of 33

313

ferrihydrite or goethite, a study of the binding affinity of As to schwertmannite found that under

314

acidic conditions (pH 3-4), such as those found in the IKMHSS tailings surface (pH 2-3), As(V)

315

introduction to the schwertmannite mineral structure can inhibit weathering of schwertmannite to

316

goethite and may explain the persistence of Fe(III)-sulfate minerals in the rhizosphere.50 While

317

iron uptake and internal biomineralization of jarosite by the plant Imperata cylindrical has been

318

reported,51 this study reports observation of a poorly-crystalline Fe(III)-sulfate root plaque that

319

sequesters arsenic during phytostabilization by P. juliflora (Figure 4).

320 321

Exterior 322 323 324 325 326 327 328 329 330 331 332 333 334

Figure 3. Molecular-scale characterization As stored in P. juliflora root cortex. Arsenic k3-

335

weighted EXAFS (inset), Fourier transformed (FT) EXAFS uncorrected for phase shift, and the

ACS Paragon Plus Environment

19

Page 21 of 33

Environmental Science & Technology

336

real FT components were fit using the shell by shell method. Solid black lines are data; stippled

337

lines are least-squares best fits (fit details and wavelet transform in SI, Table S4, Figure S7).

338

This investigation applied multi-element μXANES imaging to resolve spatial partitioning of

339

arsenic, iron, and sulfur spatial distribution and speciation in plant tissue to reveal two distinct

340

mechanisms of apparent arsenic detoxification in the P. juliflora rhizosphere. Ferric sulfate

341

plaques formed on root surfaces comprise elevated (relative to growth medium) concentrations

342

of co-precipitated arsenate substituting for sulfate in the mineral structure, effectively limiting

343

plant uptake of this toxic element in the above ground biomass. Arsenate that nonetheless

344

penetrates the root is reduced to As(III) and bound into As(III)-SH3 complexes in root vacuoles,

345

preventing interaction with root cellular metabolism. The latter mechanism had been postulated

346

but not confirmed by direct analysis prior to this study. These findings present new applications

347

for (ME)-μXANES imaging analysis for probing metal(loid) biogeochemistry relating to plant-

348

soil interactions.

349

ACS Paragon Plus Environment

20

Environmental Science & Technology

Page 22 of 33

350 351

Figure 4. Modes of As immobilization by P. juliflora during growth in the oxidizing pyritic

352

IKMHSS tailings. Oxidation of the IKMHSS tailings weathers the mineral-bound Fe(II), As and

353

S deposited as pyritic mineral to As(V)-associated poorly crystalline ferric sulfate minerals

354

composed of Fe(III) and SO4. (a) Establishment of a vegetation cap on mine tailings provides a

355

physical barrier to erosion that aids in As (blue) and Fe (red) subsurface containment where the

356

paired accumulation is displayed in purple. (b) Externally, arsenic bearing ferric sulfate mineral

357

products of arsenopyrite oxidative weathering develop on the root epidermis, presumably as a

358

result of As(V) (blue) scavenging and immobilization from pore waters during ferric plaque

359

formation (red) where purple indicates a prominence of As(V) and Fe(III) spatial co-localization.

360

(c) Internally, reduced As(III), which was never detected in the bulk tailings or on the root

361

exterior, is immobilized by complexation with thiols such as phytochelatins that were modeled

362

by As(III)-(GLU)3 (green) and stored in vacuoles in the root cortex. Mineral structures were

363

taken from published models.52, 53

ACS Paragon Plus Environment

21

Page 23 of 33

Environmental Science & Technology

364

Associated Content

365

Supporting Information

366

This section includes a brief history of phytostabilization at Iron King Superfund Site,

367

description of greenhouse experiments, documentation of plant tissue and thin section

368

preparation (Fig. S1), detail of arsenic reference materials, summary of XAS data collection and

369

processing (for As, Fe, and S; Table 1, Fig. 2), description of µ-XRF image collection and

370

processing and µ-XANES fitting protocol (As: Table S2, Fe: Table S3), µ-XRF element and

371

species correlation plots (Fig. S3), semi-quantitative As, Fe, and K content in P. juliflora root

372

thin section (Fig. S4), description of XRD diffractogram collection and processing (Fig. S5),

373

details of non-linear least-squares fitting of As EXAFS in P. juliflora root cortex (Table S4) and

374

As(III)-tris-glutathione (Fig. S6, Table S5), 2D continuous Cauchy wavelet transform of

375

normalized As EXAFS. This material is available free of charge via the Internet at

376

http://pubs.acs.org.

377 378

Corresponding Author *

379

Jon Chorover, Department of Soil, Water and Environmental Science, University of Arizona,

380

1177 E 4th St, Shantz 429, Tucson, AZ 85721 Telephone: +1 520-626-5635, Fax: 520-626-1647,

381

E-mail: [email protected]

382

ACKNOWLEDGMENTS

383

This research was supported by NIEHS Superfund Research Program Grant 2 P42 ES04940.

384

We thank Steven Schuchardt, president of North American Industries, for providing access to the

385

IKMHSS site and help with irrigation and the weather station. Portions of this research were

ACS Paragon Plus Environment

22

Environmental Science & Technology

Page 24 of 33

386

carried out at Stanford Synchrotron Radiation Laboratory, a National User Facility operated by

387

Stanford University on behalf of the U.S. Department of Energy, Office of Basic Energy

388

Sciences. This research performed on NSLS-II Proposal #300145 used the SRX beam line of the

389

National Synchrotron Light Source II, a U.S. Department of Energy (DOE) Office of Science

390

User Facility operated for the DOE Office of Science by Brookhaven National Laboratory under

391

Contract No. DE-SC0012704. Special thanks to Scott White for extensive work in establishing

392

and maintaining the field site and greenhouse study and for supervising all field sampling efforts.

393

We recognize Juliana Gil-Loaiza who contributed invaluable assistance in organizing annual

394

field sampling, and Mon Bejar and Deseree Carrillo for mesquite sample processing. We thank

395

Guilherme Dinali for helping to set up the greenhouse experiment, and all volunteer students

396

from Environmental Microbiology, Environmental Biochemistry, and Contaminant Transport

397

Labs at the University of Arizona for their help during field sampling trips from 2010 to 2015.

398

Gratitude is expressed to Sam Webb for his expert advice on µXRF and arsenic storage in plants,

399

and to Mary Kay Amistadi, Kelsie Lasharr and Shawn Pedron for ICP-MS analyses of Fe, As,

400

and S content of samples performed at the Arizona Laboratory for Emerging Contaminants

401

(ALEC) at the University of Arizona. The views of authors do not necessarily represent those of

402

the NIEHS, NIH.

403 404

ABBREVIATIONS

405

XRF, X-ray fluorescence; XAS, X-ray absorption spectroscopy; ROI, region of interest.

ACS Paragon Plus Environment

23

Page 25 of 33

Environmental Science & Technology

406

REFERENCES

407

1. Carlin, D. J.; Naujokas, M. F.; Bradham, K. D.; Cowden, J.; Heacock, M.; Henry, H. F.; Lee,

408

J. S.; Thomas, D. J.; Thompson, C.; Tokar, E. J.; Waalkes, M. P.; Birnbaum, L. S.; Suk, W.

409

A., Arsenic and Environmental Health: State of the Science and Future Research

410

Opportunities. Environmental Health Perspectives 2016, 124, (7), 890-899.

411 412 413 414

2. Clemens, S.; Ma, J. F., Toxic Heavy Metal and Metalloid Accumulation in Crop Plants and Foods. Annual Review of Plant Biology, Vol 67 2016, 67, 489-512. 3. Finnegan, P. M.; Chen, W. H., Arsenic toxicity: the effects on plant metabolism. Frontiers in Physiology 2012, 3.

415

4. Root, R. A.; Hayes, S. M.; Hammond, C. M.; Maier, R. M.; Chorover, J., Toxic metal(loid)

416

speciation during weathering of iron sulfide mine tailings under semi-arid climate. Applied

417

Geochemistry 2015, 62, 131-149.

418

5. Hayes, S. M.; Root, R. A.; Perdrial, N.; Maier, R. M.; Chorover, J., Surficial weathering of

419

iron sulfide mine tailings under semi-arid climate. Geochimica et Cosmochimica Acta 2014,

420

141, 240-257.

421

6. Youn, J. S.; Csavina, J.; Rine, K. P.; Shingler, T.; Taylor, M. P.; Saez, A. E.; Betterton, E.

422

A.; Sorooshian, A., Hygroscopic Properties and Respiratory System Deposition Behavior of

423

Particulate Matter Emitted By Mining and Smelting Operations. Environmental Science &

424

Technology 2016, 50, (21), 11706-11713.

425 426

7. Csavina, J.; Taylor, M. P.; Felix, O.; Rine, K. P.; Saez, A. E.; Betterton, E. A., Size-resolved dust and aerosol contaminants associated with copper and lead smelting emissions:

ACS Paragon Plus Environment

24

Environmental Science & Technology

Page 26 of 33

427

Implications for emission management and human health. Science of the Total Environment

428

2014, 493, 750-756.

429

8. Stovern, M.; Felix, O.; Csavina, J.; Rine, K. P.; Russell, M. R.; Jones, R. M.; King, M.;

430

Betterton, E. A.; Saez, A. E., Simulation of windblown dust transport from a mine tailings

431

impoundment using a computational fluid dynamics model. Aeolian Research 2014, 14, 75-

432

83.

433

9. Csavina, J.; Field, J.; Taylor, M. P.; Gao, S.; Landazuri, A.; Betterton, E. A.; Saez, A. E., A

434

review on the importance of metals and metalloids in atmospheric dust and aerosol from

435

mining operations. Science of the Total Environment 2012, 433, 58-73.

436

10. Gil-Loaiza, J.; White, S. A.; Root, R. A.; Solis-Dominguez, F. A.; Hammond, C. M.;

437

Chorover, J.; Maier, R. M., Phytostabilization of mine tailings using compost-assisted direct

438

planting: Translating greenhouse results to the field. The Science of the Total Environment

439

2016, 565, 451-461.

440

11. Heckenroth, A.; Rabier, J.; Dutoit, T.; Torre, F.; Prudent, P.; Laffont-Schwob, I., Selection of

441

native plants with phytoremediation potential for highly contaminated Mediterranean soil

442

restoration: Tools for a non-destructive and integrative approach. Journal of Environmental

443

Management 2016, 183, 850-863.

444

12. Fernandez, Y. T.; Diaz, O.; Acuna, E.; Casanova, M.; Salazar, O.; Masaguer, A.,

445

Phytostabilization of arsenic in soils with plants of the genus Atriplex established in situ in

446

the Atacama Desert. Environmental Monitoring and Assessment 2016, 188, (4).

ACS Paragon Plus Environment

25

Page 27 of 33

Environmental Science & Technology

447

13. Sanchez-Lopez, A. S.; Gonzalez-Chavez, M. D. A.; Carrillo-Gonzalez, R.; Vangronsveld, J.;

448

Diaz-Garduno, M., Wild Flora of Mine Tailings: Perspectives for Use in Phytoremediation of

449

Potentially Toxic Elements in a Semi-Arid Region in Mexico. International Journal of

450

Phytoremediation 2015, 17, (5), 476-484.

451

14. Cuevas, J. G.; Silva, S. I.; Leon-Lobos, P.; Ginocchio, R., Nurse effect and herbivory

452

exclusion facilitate plant colonization in abandoned mine tailings storage facilities in north-

453

central Chile. Revista Chilena de Historia Natural 2013, 86, (1), 63-74.

454

15. Clemente, R.; Walker, D. J.; Pardo, T.; Martinez-Fernandez, D.; Bernal, M. P., The use of a

455

halophytic plant species and organic amendments for the remediation of a trace elements-

456

contaminated soil under semi-arid conditions. Journal of Hazardous Materials 2012, 223, 63-

457

71.

458

16. Mendez, M. O.; Maier, R. M., Phytostabilization of mine tailings in arid and semiarid

459

environments - An emerging remediation technology. Environmental Health Perspectives

460

2008, 116, (3), 278-283.

461 462 463

17. Mendez, M. O.; Maier, R. M., Phytoremediation of mine tailings in temperate and arid environments. Reviews in Environmental Science and Bio/Technology 2008, 7, (1), 47-59. 18. Kopittke, P. M.; de Jonge, M. D.; Wang, P.; McKenna, B. A.; Lombi, E.; Paterson, D. J.;

464

Howard, D. L.; James, S. A.; Spiers, K. M.; Ryan, C. G.; Johnson, A. A. T.; Menzies, N. W.,

465

Laterally resolved speciation of arsenic in roots of wheat and rice using fluorescence-

466

XANES imaging. New Phytologist 2014, 201, (4), 1251-1262.

ACS Paragon Plus Environment

26

Environmental Science & Technology

Page 28 of 33

467

19. Lopez, M. L.; Peralta-Videa, J. R.; Parsons, J. G.; Duarte-Gardea, M.; Gardea-Torresdey, J.

468

L., Concentration and biotransformation of arsenic by Prosopis sp grown in soil treated with

469

chelating agents and phytohormones. Environmental Chemistry 2008, 5, (5), 320-331.

470

20. Delnomdedieu, M.; Basti, M. M.; Otvos, J. D.; Thomas, D. J., Reduction and binding of

471

arsenate and dimethyl arsenate by glutathione - a magnetic-resonance study. Chemico-

472

Biological Interactions 1994, 90, (2), 139-155.

473

21. Pickering, I. J.; Prince, R. C.; George, M. J.; Smith, R. D.; George, G. N.; Salt, D. E.,

474

Reduction and coordination of arsenic in Indian mustard. Plant Physiology 2000, 122, (4),

475

1171-1177.

476

22. Mishra, S.; Wellenreuther, G.; Mattusch, J.; Staerk, H.-J.; Kuepper, H., Speciation and

477

Distribution of Arsenic in the Non-hyper accumulator Macrophyte Ceratophyllum

478

demersum. Plant Physiology 2013, 163, (3), 1396-1408.

479

23. Bluemlein, K.; Raab, A.; Meharg, A. A.; Charnock, J. M.; Feldmann, J., Can we trust mass

480

spectrometry for determination of arsenic peptides in plants: comparison of LC-ICP-MS and

481

LC-ES-MS/ICP-MS with XANES/EXAFS in analysis of Thunbergia alata. Analytical and

482

Bioanalytical Chemistry 2008, 390, (7), 1739-1751.

483

24. Hoffmann, M.; Mikutta, C.; Kretzschmar, R., Bisulfide Reaction with Natural Organic

484

Matter Enhances Arsenite Sorption: Insights from X-ray Absorption Spectroscopy.

485

Environmental Science & Technology 2012, 46, (21), 11788-11797.

486 487

25. Langner, P.; Mikutta, C.; Kretzschmar, R., Arsenic sequestration by organic sulphur in peat. Nature Geoscience 2012, 5, (1), 66-73.

ACS Paragon Plus Environment

27

Page 29 of 33

488

Environmental Science & Technology

26. Castillo-Michel, H.; Hernandez-Viezcas, J. A.; Servin, A.; Peralta-Videa, J. R.; Gardea-

489

Torresdey, J. L., Arsenic Localization and Speciation in the Root-Soil Interface of the Desert

490

Plant Prosopis juliflora-velutina. Applied Spectroscopy 2012, 66, (6), 719-727.

491

27. Castillo-Michel, H.; Hernandez-Viezcas, J.; Dokken, K. M.; Marcus, M. A.; Peralta-Videa, J.

492

R.; Gardea-Torresdey, J. L., Localization and Speciation of Arsenic in Soil and Desert Plant

493

Parkinsonia florida Using mu XRF and mu XANES. Environmental Science & Technology

494

2011, 45, (18), 7848-7854.

495

28. Liu, W. J.; Wood, B. A.; Raab, A.; McGrath, S. P.; Zhao, F. J.; Feldmann, J., Complexation

496

of Arsenite with Phytochelatins Reduces Arsenite Efflux and Translocation from Roots to

497

Shoots in Arabidopsis. Plant Physiology 2010, 152, (4), 2211-2221.

498

29. Seyfferth, A. L.; Webb, S. M.; Andrews, J. C.; Fendorf, S., Defining the distribution of

499

arsenic species and plant nutrients in rice (Oryza sativa L.) from the root to the grain.

500

Geochimica et Cosmochimica Acta 2011, 75, (21), 6655-6671.

501 502 503

30. Zhao, F. J.; Ma, J. F.; Meharg, A. A.; McGrath, S. P., Arsenic uptake and metabolism in plants. New Phytologist 2009, 181, (4), 777-794. 31. Lombi, E.; Scheckel, K. G.; Pallon, J.; Carey, A. M.; Zhu, Y. G.; Meharg, A. A., Speciation

504

and distribution of arsenic and localization of nutrients in rice grains. New Phytologist 2009,

505

184, (1), 193-201.

506

32. Seyfferth, A. L.; Webb, S. M.; Andrews, J. C.; Fendorf, S., Arsenic Localization, Speciation,

507

and Co-Occurrence with Iron on Rice (Oryza sativa L.) Roots Having Variable Fe Coatings.

508

Environmental Science & Technology 2010, 44, (21), 8108-8113.

ACS Paragon Plus Environment

28

Environmental Science & Technology

509 510 511

Page 30 of 33

33. Schmoger, M. E. V.; Oven, M.; Grill, E., Detoxification of arsenic by phytochelatins in plants. Plant Physiology 2000, 122, (3), 793-801. 34. Lombi, E.; Zhao, F. J.; Fuhrmann, M.; Ma, L. Q.; McGrath, S. P., Arsenic distribution and

512

speciation in the fronds of the hyper-accumulator Pteris vittata. New Phytologist 2002, 156,

513

(2), 195-203.

514

35. Solis-Dominguez, F. A.; White, S. A.; Hutter, T. B.; Amistadi, M. K.; Root, R. A.; Chorover,

515

J.; Maier, R. M., Response of Key Soil Parameters during Compost-Assisted

516

Phytostabilization in Extremely Acidic Tailings: Effect of Plant Species. Environmental

517

Science & Technology 2012, 46, (2), 1019-1027.

518

36. Aldrich, M. V.; Peralta-Videa, J. R.; Parsons, J. G.; Gardea-Torresdey, J. L., Examination of

519

arsenic(III) and (V) uptake by the desert plant species mesquite (Prosopis spp.) using X-ray

520

absorption spectroscopy. Science of the Total Environment 2007, 379, (2-3), 249-255.

521

37. Blute, N. K.; Brabander, D. J.; Hemond, H. F.; Sutton, S. R.; Newville, M. G.; Rivers, M. L.,

522

Arsenic sequestration by ferric iron plaque on cattail roots. Environmental Science &

523

Technology 2004, 38, (22), 6074-6077.

524

38. Liu, W. J.; Zhu, Y. G.; Hu, Y.; Williams, P. N.; Gault, A. G.; Meharg, A. A.; Charnock, J.

525

M.; Smith, F. A., Arsenic sequestration in iron plaque, its accumulation and speciation in

526

mature rice plants (Oryza sativa L.). Environmental Science & Technology 2006, 40, (18),

527

5730-5736.

ACS Paragon Plus Environment

29

Page 31 of 33

Environmental Science & Technology

528

39. Hossain, M. B.; Jahiruddin, M.; Loeppert, R. H.; Panaullah, G. M.; Islam, M. R.; Duxbury, J.

529

M., The effects of iron plaque and phosphorus on yield and arsenic accumulation in rice.

530

Plant and Soil 2009, 317, (1-2), 167-176.

531

40. Frommer, J.; Voegelin, A.; Dittmar, J.; Marcus, M. A.; Kretzschmar, R., Biogeochemical

532

processes and arsenic enrichment around rice roots in paddy soil: results from micro-focused

533

X-ray spectroscopy. European Journal of Soil Science 2011, 62, (2), 305-317.

534

41. Khan, N.; Seshadri, B.; Bolan, N.; Saint, C. P.; Kirkham, M. B.; Chowdhury, S.; Yamaguchi,

535

N.; Lee, D. Y.; Li, G.; Kunhikrishnan, A.; Qi, F.; Karunanithi, R.; Qiu, R.; Zhu, Y. G.; Syu,

536

C. H., Root Iron Plaque on Wetland Plants as a Dynamic Pool of Nutrients and

537

Contaminants. Advances in Agronomy 2016, 138, 1-96.

538 539

42. Webb, S. M., SIXpack: a graphical user interface for XAS analysis using IFEFFIT. Physica Scripta 2005, T115, 1011-1014.

540

43. Ravel, B.; Newville, M., ATHENA, ARTEMIS, HEPHAESTUS: Data analysis for X-ray

541

absorption spectroscopy using IFEFFIT. Journal of Synchrotron Radiation 2005, 12, 537-

542

541.

543

44. Markert, B., Presence and significance of naturally-occurring chemical-elements of the

544

periodic system in the plant organism and consequences for future investigations of inorganic

545

environmental chemistry in ecosystems. Vegetatio 1992, 103, (1), 1-30.

546

45. Carlson, L.; Bigham, J. M.; Schwertmann, U.; Kyek, A.; Wagner, F., Scavenging of as from

547

acid mine drainage by schwertmannite and ferrihydrite: A comparison with synthetic

548

analogues. Environmental Science & Technology 2002, 36, (8), 1712-1719.

ACS Paragon Plus Environment

30

Environmental Science & Technology

549 550 551

46. Savage, K. S.; Bird, D. K.; O'Day, P. A., Arsenic speciation in synthetic jarosite. Chemical Geology 2005, 215, (1-4), 473-498. 47. Mayhew, L. E.; Webb, S. M.; Templeton, A. S., Microscale Imaging and Identification of Fe

552

Speciation and Distribution during Fluid-Mineral Reactions under Highly Reducing

553

Conditions. Environmental Science & Technology 2011, 45, (10), 4468-4474.

554

Page 32 of 33

48. Root, R. A.; Fathordoobadi, S.; Alday, F.; Ela, W.; Chorover, J., Microscale speciation of

555

arsenic and iron in ferric-based sorbents subjected to simulated landfill conditions.

556

Environmental Science & Technology 2013, 47, (22), 12992-13000.

557

49. Arias, J. A.; Peralta-Videa, J. R.; Ellzey, J. T.; Ren, M. H.; Viveros, M. N.; Gardea-

558

Torresdey, J. L., Effects of Glomus deserticola inoculation on Prosopis: Enhancing

559

chromium and lead uptake and translocation as confirmed by X-ray mapping, ICP-OES and

560

TEM techniques. Environmental and Experimental Botany 2010, 68, (2), 139-148.

561 562

50. HoungAloune, S.; Hiroyoshi, N.; Ito, M., Stability of As(V)-sorbed schwertmannite under porphyry copper mine conditions. Minerals Engineering 2015, 74, 51-59.

563

51. Fuente, V.; Rufo, L.; Juarez, B. H.; Menendez, N.; Garcia-Hernandez, M.; Salas-Colera, E.;

564

Espinosa, A., Formation of biomineral iron oxides compounds in a Fe hyperaccumulator

565

plant: Imperata cylindrica (L.) P. Beauv. Journal of Structural Biology 2016, 193, (1), 23-32.

566

52. Bindi, L.; Moelo, Y.; Leone, P.; Suchaud, M., Stoichiometric arsenopyrite, FeAsS, from La

567

Roche-Balue Quarry, Loire-Atlantique, France: crystal structure and Mossbauer study.

568

Canadian Mineralogist 2012, 50, (2), 471-479.

ACS Paragon Plus Environment

31

Page 33 of 33

569

Environmental Science & Technology

53. Bishop, J. L.; Murad, E.; Dyar, M. D., Akaganeite and schwertmannite: Spectral properties

570

and geochemical implications of their possible presence on Mars. American Mineralogist

571

2015, 100, (4), 738-746.

572

54. Webb, S. M., The MicroAnalysis Toolkit: X-ray Fluorescence Image Processing Software.

573

The 10th International Conference on X-ray Microscopy AIP Conf. Proc. American Institute

574

of Physics 2011, 1365, 196-199.

575

55. Ansley, R. J.; Boutton, T. W.; Jacoby, P. W., Biomass and Distribution Patterns in a Semi-

576

Arid Mesquite Savanna: Responses to Long-Term Rainfall Manipulation. Rangeland

577

Ecology & Management, 67,(2), 206-218.

578

ACS Paragon Plus Environment

32