In Vivo Synchrotron Study of Thallium Speciation and

MIKE J. MCLAUGHLIN ‡. LRPCD, NRML, ORD, U.S. Environmental Protection Agency,. 5995 Center Hill Avenue, Cincinnati, Ohio 45224, and. CSIRO Land ...
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Environ. Sci. Technol. 2004, 38, 5095-5100

In Vivo Synchrotron Study of Thallium Speciation and Compartmentation in Iberis intermedia K I R K G . S C H E C K E L , * ,† E N Z O L O M B I , ‡ STEVEN A. ROCK,† AND MIKE J. MCLAUGHLIN‡ LRPCD, NRML, ORD, U.S. Environmental Protection Agency, 5995 Center Hill Avenue, Cincinnati, Ohio 45224, and CSIRO Land and Water, Centre for Environmental Contaminant Research, PMB2 Glen Osmond, SA 5064 Australia

Thallium (Tl) is a metal of great toxicological concern and its prevalence in the natural environment has steadily increased as a result of manufacturing and combustion practices. Due to its low natural abundance and increasing demand, Tl is the fourth most expensive metal, thus, recovery and reuse could be a profitable endeavor. The hyperaccumulator Iberis intermedia was examined via in vivo micro-X-ray absorption near edge (µ-XANES) and microX-ray fluorescence (µ-XRF) spectroscopies to determine the speciation and distribution of Tl within leaves of the plant. I. intermedia plants were cultivated under controlled conditions in 0, 10, and 20 mg Tl kg-1 soil leading to a shoot concentration of up to 13 430 mg Tl kg-1 dry weight plant mass during 10 weeks of growth. Live plant leaves were examined by µ-XANES and µ-XRF which determined aqueous Tl(I) to be the model species distributed primarily throughout the vascular network. A direct relationship of vein size to Tl concentration was observed. The high uptake of Tl and high potential biomass of I. intermedia, combined with knowledge of Tl speciation and compartmentation within the plant, are discussed in terms of accumulation/tolerance mechanisms, consequences for potential food chain contamination, and phytomining strategies to reclaim Tl-contaminated soils, sediments, and waters.

Introduction Thallium (Tl) is an element with greater toxicity to mammals than Hg, Cd, Pb, or Cu (1-3) and is listed among the USEPA’s 13 priority metals (4). The toxicity of Tl was clearly recognized immediately after its discovery. The majority of toxicological studies that have been conducted are in the context of forensic and occupational medicine (5). Small doses (8 mg kg-1) can be lethal to man (6) and the narrow margin between toxicity and therapeutic benefits stopped its original use in treating ringworm and other skin infections. Recently, more attention has been given to the occurrence of elevated concentrations of Tl in the environment (7). Environmental accumulation of Tl is the result of both geogenic and anthropogenic inputs * Corresponding author tel: 513-487-2865; fax: 513-569-7879; e-mail: [email protected]. † U.S. Environmental Protection Agency. ‡ CSIRO Land and Water, Centre for Environmental Contaminant Research. 10.1021/es049569g CCC: $27.50 Published 2004 by the American Chemical Society Published on Web 09/03/2004

(1, 3). Thallium may be accidentally released into the environment during the manufacturing of crystals, dyes, pigments, electric and electronic equipment, semiconductors, optical and infrared systems, and fiberglass cables, or following mining, combustion of coal, and cement production (1). In the past, Tl was widely used as rodenticide until it was banned in the United States in 1972. Detrimental effects of Tl in the aquatic environment are well documented (8-11). In the terrestrial environment, Tl concentrations in soils and plants, which are of concern for animal and human health, have been reported by various authors (12-15). Epidemiological studies in Europe have found significant positive correlations between Tl concentrations in the environment and the incidence of diseases of the circulatory system (5), and between Tl in soil and garden vegetables and a number of nonspecific health effects for a study conducted in Germany (16). The major pathway of exposure to humans is the ingestion of vegetables grown in Tl-contaminated soils. Thallium can be readily taken up by plants because it is generally present in soil as thermodynamically stable Tl(I) and, as such, is an analogue of potassium. Normal concentration ranges of Tl in crops are low as observed for corn (0.78-3.1 mg kg-1 DW) and rice (1-5.2 mg kg-1 DW); however, carrot (22 mg kg-1 DW) and green cabbage (15-495 mg kg-1 DW) may pose health concerns if grown on Tl enriched soils (17). Little is known regarding the chemical speciation of Tl in plants (1). However, this information is important because Tl has two oxidation states, monovalent Tl(I) and trivalent Tl(III), which differ in terms of toxicity and chemical reactivity. Trivalent Tl is approximately 50 000 times more toxic than Tl(I) and 43 000 times more toxic than Cd on a free-ion basis (18). Thallium(III) is reported to be the most abundant Tl species in sea and lake waters (19-21). Oxidation of Tl(I) to Tl(III) has been observed in freshwater and was reported to be due to the activity of planktonic bacteria by Twining et al. (9), who suggested that the advantages of this oxidation may be related to the possible formation of stabilized complexes with inorganic and organic ligands. In this work we investigated in vivo Tl speciation and distribution in leaves of the Tl hyperaccumulator Iberis intermedia. This knowledge is valuable in view of the large potential of this plant for phytoremediation of Tlcontaminated soils as reported by Anderson et al. (22). The ability of I. intermedia to accumulate extremely large concentration of Tl in the above ground biomass (up to 13 429 mg kg-1) makes this plant interesting in terms of phytomining. Currently, Tl is the fourth most expensive metal after Pt, Au, and Pd. Determining the oxidation state of Tl in this plant is essential to assess disposal options and/or recycling possibilities of the metal-loaded plant biomass. Only one recent study, from Nolan et al. (23), has assessed Tl speciation in this plant using ion or sizeexclusion chromatography coupled on-line to inductively coupled plasma mass spectroscopy (ICP-MS), or electrospray mass spectroscopy. However, the analytical techniques used by Nolan et al. (23) required an aqueous extract of the leaves to be prepared prior to instrumental analyses, raising uncertainties regarding changes in speciation during this sample preparation step. In our work we assessed both Tl speciation and compartmentation in I. intermedia leaves using an innovative in vivo synchrotron technique. Our research provides useful information regarding the potential toxicity and the detoxification mechanisms of Tl in plants. VOL. 38, NO. 19, 2004 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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Experimental Section Plant Growth. I. intermedia seeds were collected near St. Laurent le Minier, Southern France. Seeds were initially germinated in a covered Petri dish on moist filter paper, and then transferred to pots and buried with approximately 1 cm of moistened soil. Plants (4-8) were grown in 1.5 L plastic pots of commercial potting soil at circumneutral pH spiked with Tl(I)Cl at rates of 0 (control), 10, or 20 mg kg-1. Treatments were replicated 2-fold. The plants were grown in controlled environment growth chambers. Sixteen each of metal halide and sodium vapor lights were illuminated for sixteen hours per day to simulate approximately one-third sunlight (photosynthetically active radiation (PAR) of approximately 1100 µmol m-2 s-1) with an average temperature of 25 °C. No fertilizer, except nutrients present in the potting mixture, or pest control was applied to the plants. Water application was twice per week, 250 mL pot-1 for the first 3 weeks, increasing to 500 mL pot-1 as the plants matured. The I. intermedia plants were grown for 10 weeks (reaching an average height of 23 cm) prior to examination by µ-XANES and µ-XRF. There was no effect of added Tl on plant growth (data not shown). For each treatment 3 plants were removed, oven dried (40 °C), and weighed. Shoot sub-samples of 500 mg dry weight (DW) were digested in a mixture of 5 mL of HNO3 (70%) and 5 mL of H2O2 (30%) in PTFE vessels by microwave (Milestone, Bergamo, Italy) for 30 min at 40 W. The clear digests were diluted in 1% HNO3 and analyzed by ICP-MS (Agilent, Forest Hill, Victoria, Australia) by standard addition with Ho (40 µg L-1) as an internal standard. Also, three plants grown in the 20 mg kg-1 Tl treatment were separately harvested to determine Tl concentrations in roots, stems, and leaves. Roots were thoroughly washed in distilled water to remove adhering soil particles. Leaves were divided into five groups accordingly to their position on the stems. Simply, stems were divided in five parts of equal length and leaves on the different part of the stems were analyzed separately. The total Tl concentration in the leaves used for micro-X-ray absorption near edge spectroscopy (µ-XANES) and micro-X-ray fluorescence (µ-XRF) investigation was also determined as described above. X-ray Fluorescence and X-ray Absorption Near Edge Spectroscopies. The distribution and speciation of Tl were analyzed within the hyperaccumulator leaves by µ-XRF mapping and µ-XANES. Thallium (12 658 eV) LIII-µ-XANES spectra and µ-XRF maps were collected at beamline Sector 20-BM (Pacific Northwest Consortium-Collaborative Access Team (PNC-CAT)) at the Advanced Photon Source at Argonne National Laboratory, Argonne, IL. Energy calibration was accomplished by assigning the first inflection point of Au (LIII) foil to 11 919 eV, and transmission data for a Tl(I)CO3 standard were collected simultaneously with each scan to validate monochromator stability. The electron storage ring operated at 7 GeV with a top-up fill status. Scans were collected at ambient temperature in either fluorescence or transmission modes depending on the type of sample. Mapping data (µ-XRF) and µ-XANES spectra were collected in fluorescence mode with a solid-state 13-element detector. The µ-XRF mapping employed a 6 µm diameter spot size with a one second integration time per x-y step optimized with respect to Tl concentration and distribution within I. intermedia. Bulk XANES data were collected in transmission mode for reference standards and some plant analyses. The reference materials (ACS reagent grade; SigmaAldrich, Milwaukee, WI) included Tl(I)Cl, Tl(I)CO3, Tl(I)NO3, Tl(I)2SO4, Tl(III)Cl3, Tl(III)(NO3)3, and Tl(III)2O3. The Tl salts of chloride, nitrate, and sulfate were also examined in aqueous form at a 20 000 mg kg-1 concentration. Solid reference samples were examined in transmission mode by smearing a small amount of material on Kapton tape folded onto itself. 5096

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FIGURE 1. Experimental setup of in vivo µ-XRF and µ-XANES investigation of Tl (LIII edge) speciation and distribution in I. intermedia. XANES data were analyzed using WinXAS (24). The collected scans for a particular sample were checked for calibration, averaged, and normalized, and the background was removed by spline fitting. An obstacle in the µ-XRF and µ-XANES investigations was the awkwardness of situating a live plant in the beam path (Figure 1). An attempt to determine metal speciation and distribution in live plant tissue by synchrotron methods has not been observed in the literature. However, this approach was deemed necessary to avoid pretreatment of the plant material that could cause artifacts both in terms of elemental distribution between the different plant tissues and in relation to the oxidation state of Tl. The silver box in the left portion of Figure 1 houses the Kirkpatrick-Baez focusing mirrors (beam spot size of 6 µm) and the gold tube protruding from the right of the figure is a component of the 13-element detector. A nonmetallic sleeve at the end of the 13-element detector aided efforts in isolating a single leaf for analysis. The isolated leaf was securely taped to a sample holder mounted at a 45° angle relative to the electron beam on an x-y-theta step motor stage to raster the sample as the synchrotron beam passed through the leaf. Soil moisture within the pots was kept at field capacity during the µ-XRF and µ-XANES experiments. Other leaves that appeared to interfere with the beam path were removed with a scalpel.

Results and Discussion Initial fluorescence data for energies 200 eV above the Tl edge indicated the presence of Tl and Ca in I. intermedia grown in Tl-spiked soil, with Ca being the lightest detectable element for our experimental conditions. Obviously other elements including K were present in the leaves; however, K could not be definitely differentiated from the Ca peak. Calcium is an important component of cell walls and involved in cellular membrane permeability. Calcium and potassium play vital roles as enzyme activators and cofactors (25). Analysis of plant tissue, via total digestion, for Tl concentrations yielded two expected trends. First, Tl concentrations in I. intermedia shoots increased as Tl concentrations in soil increased, from 6.8 mg kg-1 DW in the control treatment to 3450 and 5670 mg kg-1 DW in the soil spiked with Tl at 10 and 20 mg kg-1, respectively. Second, Tl concentrations in I. intermedia were greater in mature (basal) leaves than young (apex) leaves (Table 1). A similar increase in Ni and As concentrations with leaf and frond age was also observed in the Ni hyperaccumulator Berkheya coddii and in the Ashyperaccumulating fern Pteris vittata (26, 27). The results reported in Table 1 show that although roots and stem

TABLE 1. Dry Weights, Tl Concentrations, and Relative Tl Distribution in Various Part of I. intermedia Plants Grown in a Soil Spiked with Tl (20 mg kg-1)a dry weight part of plant

mg

root 148 (36) stems 59 (10) leaves (average) 225 (49)

Tl concentration

% of total mg kg-1 DW % of total 34 (3) 14 (2) 52 (4)

304 (26) 525 (69) 5787 (575)

3 (0.6) 2 (0.4) 95 (0.9)

leaves position (fraction of total height) 0.0-0.2 (base) 13429 (885) 0.2-0.4 6878 (193) 0.4-0.6 4385 (369) 0.6-0.8 3583 (587) 0.8-1.0 (apex) 2543 (397) a

Standard errors are reported in parentheses.

represented almost 50% of the total weight of the plant, they contained only about 5% of the total Tl accumulated by the plant. The majority (95%) of Tl was stored in the leaves. Therefore, phytoextraction technologies must maximize the harvesting of this part of the plant, and removal of the root system may not be necessary. The I. intermedia plants employed in the µ-XRF and µ-XANES studies were grown on 20 mg kg-1 Tl spiked soils to ensure plant concentrations adequate for fluorescence detection. Figure 2 shows the µ-XRF maps for Tl and Ca for the area encompassing the main central vein of a mature I. intermedia leaf. It is evident from Figure 2 that Tl and Ca are closely associated and localized within the vascular system of the leaf. Identical results were obtained for other leaves and sections of leaves including minor veins between the main central vein and the edge of the leaf (Figure 3). Regardless of leaf maturity, Tl and Ca were localized to veins (primary and smaller secondary veins) within the leaves of I. intermedia. This distribution of Tl in leaves is comparable to that reported for K in a number of hyperaccumulator plants (28), and likely results from the chemical similarity of K(I) to Tl(I).

Upon collection of initial µ-XRF maps during the experimental run, Tl µ-XANES spectra were collected to speciate, in vivo, the form of Tl in the plant. However, it became evident that plant cell stability was an issue for replicate scans of a particular x-y coordinate. In fact, we observed slight beaminduced damage of the I. intermedia leaf tissue after µ-XRF mapping. It is worthwhile noting that this in vivo synchrotron research method could only be accomplished on a bending magnet (BM) beamline rather than an insertion device (ID) beamline, which has approximately 1000 times greater intensity and would certainly disintegrate the leaf tissue. By examining “hotspots” (color concentration gradient of µ-XRF map, light colors represent highest concentrations) via µ-XANES relative to locations detected on µ-XRF maps, a reduction in fluorescence was noticed for triplicate scans of the same x-y coordinate with integration times ranging from 2 to 0.5 s (Figure 4). To overcome this problem, we chose a one-second integration time for XANES analysis and collected 50 spectra at 50 separate x-y coordinates along the central vein of a particular leaf by moving the sample motor stage linearly by a simple algebraic autosampler sequence program. The one-second integration time provided the best combination of consistent fluorescence yield (i.e., limited plant tissue damage) and data quality. Based on fluorescence counts, the collection of 50 XANES spectra at one-second integrations was calculated to provide statistically sound data. Two series of 50 XANES spectra from two different leaves were analyzed as outlined in the Experimental Section and each series merged into an averaged spectra. To aid in the speciation of Tl for data collected during the µ-XANES experiments, bulk XANES spectra (Figure 5) and derivative of the XANES spectra (Figure 6) of Tl reference materials were collected in transmission mode. The edge energies for Tl(I) and Tl(III) measured in our study were 12 660 eV and 12 683 eV, respectively. Shapes of the curves in Figures 5 and 6 are characteristic of first neighbor coordination to the particular species of Tl. Tl(I) salts readily dissolve in water to form ionic, aqueous Tl species. The aqueous Tl(I) salts of chloride, nitrate, and sulfate show near identical XANES spectra (Figure 5) and derivatives (Figure 6) indicate similar

FIGURE 2. Optical image and XRF maps showing the direct correlation of Tl and Ca within the main central vein of I. Intermedia basal leaf. Image and maps cover an area of 660 × 500 µm. Dark to light color scale represents increasing Tl signal intensity. Total Tl in the leaf was 13 595 mg kg-1 DW (as determined by ICP-MS).

FIGURE 3. XRF maps showing the distribution of Tl within the secondary veins in I. intermedia basal leaf. Relative Tl signal intensity is represented on the z-axis. Total Tl in the leaf was 11 962 mg kg-1 DW (as determined by ICP-MS). VOL. 38, NO. 19, 2004 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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FIGURE 4. Integration time optimization for I. intermedia µ-XANES (Tl LIII edge) studies. Triplicate scans of a particular x-y coordinate could not be accomplished; rather, single scans of multiple x-y coordinates were collected.

FIGURE 5. Normalized XANES spectra of Tl (LIII edge) reference samples. nearest neighbors (water molecules) and first shell coordination environment of Tl. Thus, the XANES spectra of Tl2SO4(aq) was significantly different from that of Tl2SO4(solid) (Figures 5 and 6). Reduction of Tl(III) to Tl(I) occurs rapidly except in the presence of extreme oxidizing agents or acidity (29) and, as such, the aqueous Tl(III) standards were acidified during preparation. The XANES spectra and derivatives of the XANES spectra are shown in Figures 7 and 8, respectively, for results of Tl speciation in two µ-XANES investigations and one bulk XANES sample of I. intermedia. The bulk XANES sample 5098

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FIGURE 6. Normalized first derivatives of XANES spectra of Tl (LIII edge) reference samples. was prepared and examined by placing approximately 10 leaves from one plant in a stack, so as to align the main central vein of each leaf. The bundle of leaves was taped together with Kapton film and placed in line with the electron beam for bulk XANES analysis in transmission mode. The spectra shown in Figures 7 and 8 for the µ-XANES samples are the collection, reduction, and average of 50 individual µ-XANES scans in close proximity on the same central vein of two separate leaves from different plants grown in 20

FIGURE 7. Normalized XANES (LIII edge) spectra of I. intermedia bulk- and micro-XANES samples with aqueous Tl(I)NO3.

a similar mechanism could be involved in the Tl detoxification. Oxidation of Tl(I) to Tl(III) was observed in planktonic communities. In contrast to monovalent Tl, Tl(III) could form stable complexes and should not interfere with K metabolism. However, our results showed that Tl(I) was the dominant species of Tl in this plant and alternative detoxification mechanisms are probably involved. Determining the speciation and localization of Tl in the hyperaccumulator I. intermedia to be similar to aqueous Tl(I) within the vascular system of the leaves will aid in the next step of harvesting Tl for beneficial reuse. Thallium(I) has a very low stability constant with both organic and inorganic ligands (1, 29) and therefore should be easily extractable from the leaves. Likewise, a candidate may be Tl metal recovery by redox since the standard electrode potential to convert Tl(I) to Tl(0) is a mere -0.336 V (29). The application of I. intermedia to phytomining Tl may raise concerns for nearby populations of humans and animals that may be in contact with the plant. Due to large internal concentrations of Tl in I. intermedia confinement of phytomining activities would need to be considered. However, Tl(I) is much less toxic than Tl(III). For instance, in a study to assess the toxicity of different Tl species to Chorella sp., it was found that Tl(III) was 50 000 times more toxic than Tl(I) on a free ion basis (18). Therefore, the finding that Tl(I) is the dominant species present in I. intermedia means that risks from ingestion of this plant by animals or humans are much less than those calculated assuming all Tl was present as Tl(III). Similar speciation analysis needs to be conducted in fodder and food crops before the risk associated with ingestion of Tl-containing plants can be correctly assessed. As economic demand for Tl increases, I. intermedia phytomining in Tl-contaminated environments could be environmentally sound and financially feasible. But, of course, limiting release of Tl into the environment from the onset would be the best solution of all.

Acknowledgments

FIGURE 8. Normalized first derivatives of XANES (LIII edge) spectra of I. intermedia bulk- and micro-XANES samples with aqueous Tl(I)NO3. mg kg-1 spiked soil. The reference spectrum for aqueous Tl(I)NO3 is shown in Figures 7 and 8 as the best representation of the data collected for the speciation of Tl in the plant tissues. Consistent with results of Nolan et al. (23), the XANES results indicate the Tl speciation in I. intermedia is aqueous Tl(I). The compartmentation of Tl within the vascular system of the plants may be implicated with the high tolerance of I. intermedia to this metal. It should be remembered that the leaf veins are complex structures containing a number of different tissues and at this stage it is not clear which are those involved in Tl sequestration. However, it is difficult to explain how this strict compartmentation is achieved since Tl(I) appears to be uncomplexed in solution. In addition to compartmentation, detoxification of toxic metals and metalloids in hyperaccumulator plants is also accomplished through transformation and complexation of the toxicant in the plants. An interesting example is represented by the As hyperaccumulator fern Pteris vittata. In this plant As(V) is reduced to As(III), which is generally considered more toxic, but it does not interfere with P metabolism and can be complexed by phytochelatins (27, 30). We hypothesize that

The U.S. EPA has not subjected this manuscript to internal policy review. Therefore, the research results presented herein do not, necessarily, reflect Agency policy. Mention of trade names of commercial products and companies does not constitute endorsement or recommendation for use. PNC-CAT facilities and research at these facilities is supported by the U.S. DOE Office of Science grant DE-FG03-97ER45628. Use of the Advanced Photon Source was supported by the U.S. DOE under Contract W-31-109-ENG-38. We extend our deepest appreciation to the staff of the Pacific Northwest Consortium-Collaborative Access Team, especially Drs. M. Balasubramanian, R. Gordon, and S. Heald for their assistance and expertise during data collection. The authors appreciate the efforts of three anonymous reviewers. An interest in the copyright of this paper belongs to the Crown Her Majesty the Queen in right of Australia as represented by the Minister of Natural Resources.

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Received for review March 19, 2004. Revised manuscript received June 25, 2004. Accepted July 29, 2004. ES049569G