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Halophytes Present New Opportunities in Phytoremediation of Heavy Metals and Saline Soils Eleni Manousaki and Nicolas Kalogerakis* Technical UniVersity of Crete, Department of EnVironmental Engineering, Polytechneioupolis, 73100 Chania, Greece
A more efficient performance of several basic biochemical tolerance mechanisms provides an advantage to halophytes with respect to several environmental factors including heavy metals. Therefore, halophytes have been suggested to be naturally better adapted to cope with environmental stresses, such as heavy metals compared to salt-sensitive crop plants commonly chosen for phytoremediation purposes, and, thus, offer a greater potential for phytoremediation research for the decontamination of heavy metal polluted soils. Research findings suggest that halophytes are ideal candidates for phytoextraction, phytostabilization, or phytoexcretion of heavy metal polluted saline and nonsaline soils, while recent findings encourage the use of salt-accumulating halophytes for soil desalination in arid and semiarid regions. 1. Introduction As a result of the increasing competition for fresh water due to a steady increase in the demand for drinking and irrigation water, there is a gradual and irreversible spread of salinization. Salinity is affecting fresh water and soil, particularly in arid and semiarid regions. Ironically, irrigation has resulted in the accumulation of salt to above normal concentrations in the rooting zone of arable land, as high rates of evaporation and transpiration draw soluble salts from deep layers of the soil profile.1 The United Nations Food and Agriculture Organization and the United Nations Environment Programme estimate that there are currently 4 million square kilometers of salinized land and approximately 20% of agricultural land and 50% of cropland in the world is salt stressed threatening agricultural productivity.1,2 Salt-impacted soils show structural problems created by certain physical processes and specific conditions which affect water and air movement, plant-available water holding capacity, and root penetration as well as devastating effects on plant growth and survival through both ionic and osmotic stresses which act on plants in various ways and on different complexicity levels.3-6 However, about 1% of the species of land plants can grow and reproduce in coastal or inland saline sites. These remarkable plants, halophytes, are able to survive and reproduce in environments where the salt concentration is around 200 mM NaCl or more and tolerate salt concentrations that kill 99% of other species.7 Among these salt-adapted halophytes are annuals and perennials, monocotyledonous and dicotyledonous species, shrubs, and some trees. There is a wide range of morphological, physiological, and biochemical adaptation mechanisms in such plants, which vary widely in their degree of salt tolerance.1,7 The main sets of these control mechanisms, with each one to include a variety of different control processes, are salt tolerance in which plants tolerate the presence of salt within the cells, and salt avoidance in which plants exclude salt from their cells, while the last control mechanism is presented in plants either as salt exclusion by the roots or as salt secretion and export by means of salt excreting organs.8,9 It is obvious that not only one of these control processes is active in different types of halophytes. One set can be active in one group, whereas another * To whom correspondence should be addressed. Tel.: +30-2821037794. Fax: +30-28210-37852. E-mail: nicolas.kalogerakis@ enveng.tuc.gr.
set is dominant in another group leading to the classification of halophytes into salt-excluders (e.g., Rhizophora mangle), saltincluders (often possessing means of salt-recretion, e.g. species of genus Tamarix), and salt-accumulators (some species of genus Atriplex).9 Some of these control mechanisms are also active in nonhalophytes, but some of them are very specific features, which have evolved in halophytes.4,9,10 Salt tolerance is a complex trait involving several interacting properties, and generally not much is known about the regulatory networks involved. However, it is known that the ability of halophytes to adapt to such harsh environments relies on controlled uptake and compartmentalization of Na+ and Cl-, the synthesis of organic “compatible” solutes even where salt glands are operative, and the inducement of antioxidant systems.7-9,11 Tolerance of halophytes to ionic and osmotic components of salt stress are linked to their ability to synthesize osmoprotectants in order to maintain a favorable water potential gradient and to protect cellular structures.12 Proline is one of these osmoprotectants which is also found to have significant beneficial functions under metal stress by three major actions, namely metal binding, antioxidant defense, and signaling. A large body of data suggests that proline accumulates in response to Cd, Cu, and other heavy metals.11-16 Additionally, in a recent study, it was found that the presence of cadmium may trigger glycinebetaine oversynthesis which is the most efficient osmoprotectant synthesized by Chenopodiaceae.12 Hence, since heavy metals induce in plants both a secondary water stress16,17 and an oxidative stress,18-20 the capability of halophytic plants to synthesize those organic compatible solutes may be involved in their ability to cope with heavy metals.12 Furthermore, the tolerance of halophytes to salt stress is generally correlated with a more efficient antioxidant system,21 and thus, halophytes are expected to be more capable to cope with heavy metals stress than common plants. Available experimental data suggests that stress-related responses induced by salt and copper overlap to some extent probably due to common integrated mechanical and chemical signals, supporting the hypothesis that tolerance to salt and heavy metals may, at least in part, rely on common physiological mechanisms.15,22 Thus, it can be safely assumed that halophytes and heavy metal-tolerant plants possess specific but also general functioning mechanisms of tolerance toward a wide range of abiotic factors.11
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Consequently, the advantages of halophytes over nonhalophytic plants toward several abiotic factors may simply result from the more efficient performance of several basic biochemical tolerance mechanisms.10 Therefore, halophytes have been suggested to be naturally better adapted to cope with environmental stresses including heavy metals compared to salt-sensitive crop plants commonly chosen for phytoremediation purposes for the removal of heavy metals from soils.23-25 Furthermore, it has been speculated that salt-tolerant plants may also be able to accumulate metals22 and thus offer greater potential for phytoremediation research. In this manuscript, we summarize current knowledge and experimental data concerning the prospects on the use of halophytes as clean up tools for the remediation of heavy metal and salt-impacted soils. 2. Phytoremediation Using Halophytic Plants Phytoremediation is an emerging technology that uses various plants to degrade, extract, contain, or immobilize contaminants from soil and water. This plant-based technique is potentially applicable to a variety of contaminants, including some of the most significant ones, such as heavy metals, chlorinated solvents, and polycyclic aromatic hydrocarbons. It can also be classified based on the contaminant fate or the mechanisms involved: degradation, extraction, containment, or a combination of these.26,27 In the case of heavy metals and the serious environmental and human health problem caused by their increased accumulation in soils, there is still a need of an effective and affordable technological solution since the enormous costs associated with the removal of metals from soils by traditional methods have been encouraging the industry to ignore the problem.28 Within the field of phytoremediation, phytostabilization and phytoextraction have been highlighted as alternative techniques of soil remediation from heavy metals as they offer the benefits of environmentally friendly, low-cost, and in situ operation, easily accepted by the public.29,30 The former is defined as the use of plant to stabilize the metals in their rhizosphere preventing them from mobilization and migration in soil, groundwater, or air, and decreasing erosion, runoff, and leaching, while the most effective but also technologically the most difficult strategy is phytoextraction which is the utilization of plants to transport and concentrate metals from soil into the harvestable plant parts and their removal from the site by harvesting.29,30 Furthermore, a new approach of phytoremediation termed phytodesalination, has attracted much interest during the past few years for the reclamation of salt-affected soils. This method probably could be included in the phytoextraction technique as it involves the use of Na-accumulating halophytes and removal of sodium from the soil by plant harvesting and it is of great importance especially for arid and semiarid regions since shoot sodium accumulation has been reported to reduce soil sodium content and consequently its salinity.2,31,32 2.1. Phytostabilization. The ideal plant for phytostabilization applications is a metal-tolerant, nonaccumulator plant which should tolerate, but not translocate and accumulate, the metals into its aerial parts, with high biomass, rapid growth, an extensive root system growing into the zone of contamination, and tolerance to other environmental factors such as drought and high temperature, providing a sufficient vegetation cover that could stabilize low levels of metals in soils and, thus, prevent metals from mobilizing or leaching into groundwater and surface water.27,33 Halophytes, as already discussed, are tolerant not only to salt but also to several other environmental stresses such as chilling,
Figure 1. Lead concentration (mg/kg dry weight) in individual parts of 12 month old Nerium oleander L. plants grown for 10 weeks on soil polluted with increasing concentrations of Pb (pot experiment). Values shown are means (n ) 3) with minimum and maximum values.
freezing, heat, drought, and heavy metals. Thus, the identification of high biomass halophytic plants that tolerate the metal of interest but do not translocate it into their aerial parts provides opportunities for phytostabilization applications. For instance, Nerium oleander L., which is a fast growing with high biomass, salt tolerant endemic plant of the Mediterranean region, North Africa, and South Asia, although it has not been studied as of yet for phytoremediation purposes, was recently investigated in our laboratory. In Greece, this plant can be found along the side of heavily trafficked highways where Pb concentrations have been very high in the past, along the seashores or in Mediterranean riverbeds that remain dry most of the year, suggesting that this plant is able to adapt to a wide range of stressors and tolerates considerable drought, high temperature, strong winds, poor drainage, high salt content in the soil, and probably heavy metals.34 The results of pot experiments performed with oleander grown on polluted soil with increasing concentrations of lead revealed that the main lead accumulation site is the plant roots, and even in as high concentrations as 2400 mg Pb/kg soil, the concentration in aerial parts remained notably at low levels indicating an important restriction of the transport of the metal from the roots toward stems and leaves (Figure 1). Moreover, the plant developed no visible toxicity symptoms as well as no growth or chlorophyll content reduction, indicating that it is a Pb-resistant plant which does not translocate the metal into its aerial tissues.35 Therefore, Nerium oleander L. is obviously suitable for phytostabilization applications of soils polluted with lead. 2.2. Phytoextraction. Research studies in our laboratory focusing on the Cd and Pb phytoextraction potential of the xerohalophyte Atriplex halimus L. which is a Mediterranean big biomass saltbush species highly resistant to drought,36 salinity,37 and heavy-metal stress,38 confirmed that it is a Pb- and Cdtolerant plant. Furthermore, it was revealed that although metal concentrations achieved in plant tissues were kept generally at low levels, its high above ground biomass production suggests that it deserves further investigation for phytoextraction purposes (Figure 2).39 Similarly, experiments on the salt-tolerant Mediterranean tree Tamarix smyrnensis Bunge revealed that it is also a Pb- and Cd-tolerant plant; however, it is not a metalhyperaccumulator (Figure 2).40-42 It has been suggested that trees are potentially the lowest-cost type of plants to be used for phytoextraction despite their relatively low accumulation of heavy metals, because of their extensive root system, high biomass, and low-input cultivation. They also provide an economic return on contaminated land through the production
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Figure 2. The total amount of Cd in individual parts of 12 month old Nerium oleander L., 8 month old Tamarix smyrnensis Bunge, and 11 month old Atriplex halimus L. grown for 10 weeks on soil polluted with 800 ppm Pb and 40, 20, and 16 ppm Cd, respectively (pot experiments). Values shown are means (n ) 3) with minimum and maximum values.
of biomass, and furthermore, they can grow on land of marginal quality which allows their use for phytoremediation of soils with low fertility and poor soil structure, resulting in low operating costs.28,43,44 Moreover, halophytes have additional advantages for phytoextraction because they are probably the only candidates for the reclamation of heavy metal polluted saline soils16,24 and because they can be cultivated with salt-water irrigation since the availability of fresh water is becoming a serious problem. In particular, as only about 1% of the water on Earth is fresh whereas there is an equivalent supply of brackish water (1%) and a vast quantity of seawater (98%), probably the time has come to explore the agronomic use of these resources.1 More importantly, salinity has been suggested to be a key factor in the translocation of metals from roots to the aerial parts of the plant45,46 providing an additional advantage for phytoextraction applications. This is also suggested by our findings from pot experiments with halophytes grown on soil polluted with Cd and irrigated with saline water (Figure 3). Especially in the case of Tamarix smyrnensis Bunge, salinity was found to affect significantly the translocation of Cd from the roots to the aerial parts of the plant resulting in leaf/root Cd concentration ratios above 1 which is an important characteristic for a plant to be used for phytoextraction purposes.41 Furthermore, salinity is known to affect heavy metal bioavailability and speciation in soil, especially for metals with high mobility like Cd, due to displacement of metals from binding sites in the soil matrix by
salt cations and formation of soluble chloro-complexes of Cd which tend to shift Cd from solid to solution phase.39,47-49 In a comparison study of induced phytoextraction between the halophyte Atriplex nummularia and the glycophyte Zea mays for their chelatorsfacilitated metal uptake ability, it was shown that the halophyte translocated more metals from roots to shoots than the glycophyte when treated with EDTA suggesting that halophytes, despite their slower growth rates, may have greater potential to selectively phytoextract metals from contaminated soils than glycophytes.23 2.3. Phytoexcretion. As a secondary tolerance mechanism against excess salt, some halophytes have salt excretion organs (salt glands, salt bladders, or trichomes) in their leaves which regulate plant tissue ion concentration,4,8,12 and although not all halophytes have these regulating organs, salt accumulating glands are mostly common in the families of Poaceae, Tamaricaceae, Chenopodiaceae, and Frankenaciaceae. Studies on halophytes such as Tamarix aphylla L.,50 Atriplex halimus L.,12 mangroves, and a number of other estuarine and saltmarsh halophytes51-55 have revealed that these glandular tissues are not always specific to sodium and chloride ions and other toxic ions such as cadmium, zinc, copper, or lead are excreted though the salt glands from leaf tissues onto the leaf surface. Furthermore, studies in our laboratory on Tamarix smyrnensis Bunge showed that its salt glands accumulate and excrete Cd and Pb on the surface of its leaves suggesting that it uses its salt excretion mechanism to excrete excess metals on its leaf surface as a detoxification mechanism against the metal burden.41,42 Moreover, cadmium excretion was found to rise with increasing soil salinity where there is also a higher salt excretion (Figure 4).41 On the basis of these findings and the idea of using plants as biological pumps for heavy metals, the term “phytoexcretion” has been introduced to indicate a novel phytoremediation process for sites contaminated with metals, bringing new potential for technological developments as the excreted metals can be collected before they return into the soil again and, at the same time, the important problem of managing the disposal of contaminated plant parts is reduced.41,42 This strategy could be based for instance on the use of metal binding/absorbing “blankets” where the metals in the excreted droplets from the plants are retained for later collection. Furthermore, it is found that 50% or more of the salt entering the leaf of a salt-excreting halophyte can be excreted,8 and hence, it is suggested that this novel approach of phytoremediation could be used for the remediation of salt-affected soils based on the same idea of the
Figure 3. Cadmium concentration (mg/kg dry weight) in individual parts of 12 month old Nerium oleander L., 2.5 month old Tamarix smyrnensis Bunge, and 11 month old Atriplex halimus L. grown for 10 weeks on soil polluted with 40, 20, and 16 ppm Cd, respectively, at three different soil salinities (0, 0.5, and 3% NaCl) (pot experiments). Values shown are means (n ) 3 for oleander and atriplex and n ) 4 for tamarix) with minimum and maximum values.
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which receive and accumulate high concentrations of salt in their above ground tissues and consequently saline soils can be improved by harvesting the plants. Acknowledgment This project was funded by the European Economic Area Financial Mechanism, Grant EL-0075. Literature Cited
Figure 4. Cadmium excretion from leaf tissue of 2.5 month old Tamarix smyrnensis Bunge plants treated for 10 weeks with 16 ppm Cd of dry weight of soil at different soil salinities (0 and 0.5% NaCl) (pot experiment). Values shown are means (n ) 6) with minimum and maximum values.
collection of the excreted salt before it returns to the soils again resulting in a reduction of soil salinity. 2.4. Phytodesalination. Several authors encourage the use of Na+ and Cl- hyperaccumulating halophytes for soil desalination since species such as Suaeda maitima, Suaeda portulacastrum, Suaeda fruticosa, Suaeda salsa, Suaeda calceoliformis, Kalidium folium, SesuVium portulacastrum, Arthrocnemum indicum, Atriplex nummularia, and Atriplex prostrata have been reported to accumulate high concentrations of salt in their above ground tissues, and consequently, saline soils can be upgraded by harvesting the plants on a regular basis.2,8,31,32,56-59 For example, studies with Suaeda fruticosa reported that more than 2400 lbs (1088.6 kg) of salt can be removed from 1 acre by a single harvest of the aerial parts in the fall each year.56 Studies with Suaeda salsa indicated that a density of 15 plants/m2 could potentially remove 3090-3860 kg Na+/ha if the plants were harvested at the end of the growing season.57 According to the above, since it was found that it exhibits no growth inhibition on a long-term basis under relatively high salinity stress conditions,37-39 Atriplex halimus L., which is also a saltaccumulating halophyte with operative salt bladders, deserves further investigation for the determination of the rates of salt uptake and accumulation in order to explore its potential use for phytodesalination applications. 3. Conclusions Halophytes are of significant interest since these plants are naturally present in environments with an excess of toxic ions and research findings suggest that these plants also tolerate other environmental stresses, especially heavy metals as their tolerance to salt and to heavy metals may, at least partly, rely on common physiological mechanisms. Therefore, halophytic plants have been suggested to be naturally better adapted to cope with heavy metals compared to glycophytic plants commonly chosen for phytoremediation research. Under these considerations, halophytes are potentially ideal plants for phytoextraction or phytostabilization applications of heavy metal polluted soils and moreover of heavy metal polluted soils affected by salinity. Furthermore, a novel process for the phytoremediation of heavy metal contaminated soils termed phytoexcretion has been recently introduced based on findings that some salt-excreting halophytes use their excretion mechanism in order to remove the excess of toxic metal ions from their sensitive tissues and on the idea of using plants as biological pumps for heavy metals. Finally, phytodesalination has attracted much interest for the desalination of soils with the use of salt-accumulating halophytes
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ReceiVed for reView February 3, 2010 ReVised manuscript receiVed May 23, 2010 Accepted June 1, 2010 IE100270X
