Mechanisms of arsenic sequestration by Prosopis juliflora during

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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

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Mechanisms of arsenic sequestration by Prosopis

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juliflora during phytostabilization of metalliferous

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mine tailings

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

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

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Shantz 429, Tucson, AZ 85721

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

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imaging, phytoaccumulation

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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accumulation.


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1. INTRODUCTION

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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assisted direct planting during tailings phytostabilization has the goals of immobilizing

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

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

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

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

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resolved.

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

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

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

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

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

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

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

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

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

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

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

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

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deriving from arsenic-bearing mine tailings systems.

21, 33, 34

18-20

Arsenic

Among such plants studied

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

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

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

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

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

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

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

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

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phytostabilization.

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

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


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

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

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

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

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

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

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

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2. MATERIALS AND METHODS

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

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

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

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

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

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

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

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

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

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

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

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

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

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


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

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

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

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

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

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

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

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

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

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collection and tissue preparation is described in the SI.

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2.2 X-ray spectroscopy.

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

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

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

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

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

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

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

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

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temperature. Spectral processing was performed with SixPack

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correction) and Athena

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conducted with Athena and Artemis.

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reduction are provided in the SI.

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(average and deadtime

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

Additional details of bulk XAS collection and data

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

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


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

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

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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

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

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

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

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

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

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

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

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package SMAK.

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

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

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as above for bulk XAS.

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Speciation maps were fit by applying a matrix of normalized spectral

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3. RESULTS AND DISCUSSION

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

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

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

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

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

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

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

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

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


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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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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.


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

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

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

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

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

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

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

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

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

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

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

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


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

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

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

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

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

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

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the

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

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

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

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

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

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

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

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

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for the root-associated iron plaque.45, 46

ferric

sulfate

minerals

jarosite

[XFe3III(SO4)2(OH)6]

and

schwertmannite

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

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

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

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

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


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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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


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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

21, 24, 25, 36

For


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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


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Page 17 of 33


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.


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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.


17

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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


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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


19

Page 21 of 33


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


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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


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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


22


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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.


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