Critical Assessment of Chelant-Enhanced Metal Phytoextraction

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Critical Review

Critical Assessment of Chelant-Enhanced Metal Phytoextraction BERND NOWACK,* RAINER SCHULIN, AND BRETT H. ROBINSON Institute of Terrestrial Ecosystems, ETH Zurich Universitaetstrasse 16, 8092 Zu ¨ rich, Switzerland

Chelant-enhanced phytoextraction has received a lot of attention in the past decade. In theory, this technique could cleanse metal polluted soils by solubilizing contaminating metals, allowing them to be taken up by plants that would subsequently be removed from the site. We review the processes of metal solubilization, uptake by plants, and leaching during chelant-enhanced phytoextraction. A large excess of chelant is required to solubilize the target metal due to the co-solubilization of Ca and Fe. Chelated metals are taken up via the apoplastic pathway. Disruption of the Casparian Band is required to achieve the high shoot concentrations needed for phytoextraction. Therefore, adding chelants to a soil increases not only the total dissolved metal concentration but also changes the primary route of plant metal-uptake from the symplastic to the apoplastic pathway. Depending on metal, plant species, and chelant concentration, significant increases in metal uptake are likely. Soil solution chelate concentrations of at least several mM are required to induce appreciable shoot concentrations. A simple calculation reveals that at such soil solution concentrations plants will remove only a small fraction of the solubilized metals. Leaching, exacerbated by preferential flow processes, is unavoidable. Chelant-enhanced phytoextraction is therefore limited to areas where the connection with groundwater has been broken, or where leaching is unimportant. Chelant-enhanced phytoextraction may nonetheless have a role in enhancing the uptake of essential trace metals. Such a role warrants further investigations into the use of biodegradable chelants such as ethylenediaminedisuccinic acid (EDDS).

the natural speciation of metals and influence metal bioavailability (5). Many chelating agents (e.g., EDTA) are not readily degraded under natural conditions and thus persist in the environment (6). The addition of large amounts of chelating agents to soils therefore warrants a thorough evaluation. Research into the interaction of plants with chelating agents started in the 1950s with a view to alleviating deficiencies in the essential nutrient metals Fe, Mn, Cu, and Zn (5). Initial results also showed that chelants such as EDTA enhanced plant uptake of Pb and Hg (7). Jorgensen in 1993 (8) and Huang and Cunningham in 1996 (9) showed that addition of chelating agents to soils increased Pb accumulation by crop plants to such an extent that they might be used for cleanup of Pb-contaminated soils. A subsequent flurry of research showed that the addition of chelating agents could increase Pb accumulation in shoots of various plants by factors as high as 265 (9-12). Enhanced uptake was not only observed in nutrient solution and pot experiments but also in the field (13-15). Publications about chelant-enhanced phytoextraction have increased steadily to about 15-20 per year in the last few years, indicating that this is a growing and active research field. Although some reviews and compilations of the available literature have been published (16, 17), there is only limited discussion of the key mechanisms of chelantinduced phytoextraction. Two groups of mechanisms dominate chelant-enhanced phytoextraction. Soil processes determine the mobilization and transport of metals, while plant processes control the uptake and translocation of the solubilized metals. We aim to provide a critical evaluation of the underpinning processes of chelant-enhanced phytoextraction with a view to elucidating the feasibility of this technology and reveal fertile areas for future research.

Introduction

Terminology

In the past decade, chelant-enhanced phytoextraction has received much attention from the scientific community. This technique aims to cleanse metal-polluted soils by inducing plants to accumulate the contaminating metal in the harvestable parts by adding chelating agents to the soil. The metal-rich biomass could then be removed from the site, and stored in an area where it does not pose a risk to the environment, such as a sealed landfill, or burned (1). However, adding chelating agents to soil may be harmful. The environmental fate of aminopolycarboxylate chelating agents has been discussed extensively (2-4) because they perturb

The term “chelate-enhanced phytoextraction” has been frequently used in the literature. However, this term is misleading because it suggests that chelates are applied to the soil. The term “chelate” denotes a complex between a metal and a chelating agent and not the chelating agent itself (18, 19). A shorter word for chelating agent is “chelant” or “chelator”. We therefore suggest using the term “chelantenhanced phytoextraction”. Other terms such as “chelantinduced” and “chelant-assisted” phytoextraction can be used as synonyms to chelant-enhanced phytoextraction. “Chelate” should be used whenever a metal-chelating agent complex is meant, e.g., when talking about a specific complex.

* Corresponding author present address: EMPA - Materials Science & Technology, Lerchenfeldstrasse 5, CH-9014 St. Gallen, Switzerland. Phone: +41 (0)71 274 7692; Fax: +44 (0)71 274 7862; E-mail: [email protected].

Soil Factors

10.1021/es0604919 CCC: $33.50 Published on Web 08/08/2006

 2006 American Chemical Society

The addition of chelants to soil usually increases the concentration of total dissolved metals. Under normal soil VOL. 40, NO. 17, 2006 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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FIGURE 1. Extraction of Cu, Zn, Cd, and Pb from soils polluted naturally in the field with chelating agents (bEDTA, 9NTA, 2EDDS, or [DTPA) as a function of the ratio chelant to total heavy metals. Data are from 28 publications, see Supporting Information for complete bibliography. conditions, one mole of an aminopolycarboxylate chelating agent complexes one mole of metal. The ratio of chelants to metals in the soil is of overriding importance. As the ratio increases, more chelant is present in soil solution, and metal solubilization is faster and more complete (20). However, this ratio is seldom used to guide the design of experiments. The application rates of chelants are normally 0.5-5 g chelant kg-1 soil (9, 11, 21-24), or 1-20 mmol kg-1 (10, 25-28), which corresponds to 0.3-6 g EDTA kg-1. Unfortunately, the knowledge of the applied amount is not sufficient to calculate the concentrations of solubilized metals. To evaluate the metal extraction potential of chelating agents, we compiled data from 28 publications. We selected articles that used soils contaminated under field conditions and where the extractions were carried out over about 24 h at an approximately neutral pH. Figure 1 shows the percentage of extracted metals as a function of the ratio of chelant to total metals in the soil for Cu, Zn, Cd, and Pb. A chelantto-metal ratio of at least 1 is needed to solubilize all the target metal. However, except for Pb, complete solubilization did not occur, even at a chelant-to-metal ratio of greater than 10. The data show a large variation between soils for a given chelant-to-metal ratio. In particular, the extraction of Zn varied between 1200 high transpiration days. However, this could not be achieved in a single cropping, as the plants rapidly die after VOL. 40, NO. 17, 2006 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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the application of the chelant. If we optimistically assume that plants continued to transpire for 10 days after chelant application, then between 8 and 100 crops would be needed to reduce the soil Pb concentration to 200 mg kg-1. More chelant would have to be added after each cropping, as the Pb-chelate is unstable with respect to Fe-chelate, there is downward leaching, and, depending on the used chelant, biodegradation. These calculations assume that the plant takes up all of the chelated Pb. However, mass balance calculations in greenhouse experiments show that, at the most, just 10% of the soil metal is taken up by the plant (41, 68). The remainder is either reprecipitated in the soil, or leaches into receiving waters. We now discuss the environmental implications of such massive additions of chelants to soils.

Environmental Concerns EDTA as a Persistent Contaminant. The use of EDTA in phytoextraction has received considerable attention due to its low cost and high efficacy of metal solubilization. EDTA offers the best cost/performance ratio of all chelants. However, EDTA has also received a lot of attention due to its persistence in the environment. While biodegradation of EDTA has been reported in pure cultures under controlled conditions, negligible degradation has been observed under natural conditions in soil and water (6). Due to this persistence, EDTA is found in almost all natural waters (19). EDTA has therefore been selected by the European authorities as part of the priority substances for extensive evaluation. According to the completed risk assessment report, EDTA has a low toxicity profile for humans and environmental risks are limited to some localized cases of high emissions to surface waters (69). The report concludes that risk reduction measures should be considered at concentrations above 2.2 mg L-1 (about 10 µM), a value hardly ever reached in natural waters. When applied to soil during phytoextraction, EDTA concentrations in soil solution are typically 1-100 mM, some 100-10 000 times higher than the 10 µM threshold above which risk reduction measures should be considered. Using eq 2, we can also calculate the fraction of the chelant that is taken up by the plants. We used again our model soil for this calculation and assumed uptake during 10 days. The chelant uptake during that time is between 0.14 and 0.011 mol m-2 using the highest and the lowest φ value. This is 12 and 1% of the total amount of chelant in the topsoil. At least 90% of the chelant stays in solution and can be leached down to groundwater. To reach the concentration of 10 µM which was found to be safe by the European risk assessment report on EDTA (69), the plants would need to take up 99.95% of the added EDTA. The deliberate “pollution” of groundwater by EDTA or another chelant in the course of a phytoextraction procedure is therefore unavoidable when using an environmentally persistent chelant such as EDTA except under climatic conditions that completely prevent any leaching of solutes out of the rooted zone. Metal Contamination of Receiving Waters. Even if a chelating agent is found that is effective, low-cost, and biodegradable, metal leaching into receiving waters is still an environmental concern. Free chelants only weakly interact with mineral surfaces at pH values in the plant-growth range, while strong adsorption occurs under acidic conditions (2). The adsorption of metal complexes generally differs from that of the free ligand (70). The relatively weak adsorption of chelates around neutral pH therefore results in excessive leaching. This has been observed in column experiments and in lysimeters (36, 38, 42, 71, 72). Leaching in the presence of the biodegradable chelant EDDS, however, was found to be significantly less than that for EDTA in small soil column (25). 5230

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The action level for Pb in water in the United States is 0.015 mg L-1, equivalent to 0.07 µM. To reduce the 16 mM Pb in our example in the topsoil to this level, the plants would need to take up 99.99999% of the solubilized Pb. One liter of topsoil solution with 16 mM Pb would raise the Pb concentration of 220 000 L of water above the action level without plant uptake. Even if the plants would take up 99% of the mobilized Pb from the example used above, the remaining 1% leached from 1 m2 of soil surface would raise 50 million L of water above the action level for Pb. Solute transport through soils occurs via percolation through the soil matrix and preferential flow through macropores and other structures of rapid transport. Preferential flow, occurring in virtually all soils (73), permits the rapid passage of solutes through the soil with minimal interaction with soil particles and plant roots (74) and may result in solute transport up to 2 orders of magnitude faster than matrix flow (75). Even with noncomplexed metals, these transport pathways have been shown to exacerbate groundwater contamination by reducing the contact time of the soil solution with organic and clay material that could otherwise retard the movement of dissolved metals (76). Therefore, some leaching of chelant and chelated metals is unavoidable. Implications for Phytoremediation. In the best case scenario, where chelant-induced phytoextraction is used to remediate a modestly contaminated soil under optimal conditions, this technology requires large masses of chelant to be applied to soil over the course of several years. Leaching is unavoidable during this time. Preferential flow processes will result in a significant proportion of the chelant and solubilized metal descending below the root zone, possibly into receiving waters. Chelant-induced phytoextraction may therefore be limited to applications where the connection to receiving waters has been broken, or where leaching is unimportant. In the former case, phytoextraction could be conducted ex situ. Here, the contaminated material would be placed on a liner whereby any leachate could be collected and recycled. Such systems are already used for soil washing and the recovery of gold from low-grade ore bodies. Plants would aid in metal recovery by concentrating the metal in their biomass. The economic feasibility of induced gold phytoextraction has been demonstrated (77). Alternatively, if groundwater contamination is not an issue, chelants may be used as chemical ploughs, reducing soil metal contamination by leaching below the root zone and precipitating the metal where it is unavailable for plant uptake. Some research has also been carried out with biodegradable chelating agents. A promising chelant is EDDS, which has received attention in the last years as potential replacement for EDTA in soil washing and chelant-enhanced phytoextraction (20, 25, 31, 42, 61, 78, 79). Metal-EDDS complexes have been shown to be easily biodegradable in soils (42, 47, 80). An approach combining the application of a biodegradable chelant (EDDS), phytoextraction by plants, and a reactive permeable barrier for complete biodegradation of the leached chelant has been proposed (26). An additional factor that should also receive more attention ia possible adverse effects of high chelant doses on soil microbial and fungal activity (25, 81, 82).

Supporting Information Available A description of modeling the extraction of Pb and Ca in the presence of chelants; a description of the conditions used to calculate the extraction of Pb in the presence of Ca and Fe(III) by EDTA and EDDS; the list of references used to draw Figure 1; a table summarizing the conditions to calculate uptake of Pb into the shoots. This material is availabe free of charge via the Internet at http.//pubs.acs.org.

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Received for review March 2, 2006. Revised manuscript received June 16, 2006. Accepted June 28, 2006. ES0604919