Bioresource Technology 79 (2001) 273276

Review paper

Phytoremediation of organic contaminants in soils

Itziar Alkorta a, Carlos Garbisu b,*
a

Department of Biochemistry and Molecular Biology, University of the Basque Country, Apdo. 640, 48080 Bilbao, Spain b NEIKER, Basque Institute of Agricultural Research and Development, C/Berreaga, 1, 48160 Derio, Spain Received 29 November 2000; received in revised form 23 December 2000; accepted 3 January 2001

Abstract Soil pollution, a very important environmental problem, has been attracting considerable public attention over the last decades. Unfortunately, the enormous costs associated with the removal of pollutants from soils by means of traditional physicochemical methods have been encouraging companies to ignore the problem. Phytoremediation is an emerging technology that uses plants to clean up pollutants in the environment. As overwhelmingly positive results have become available regarding the ability of plants to degrade certain organic compounds, more and more people are getting involved in the phytoremediation of organic contaminants. Phytoremediation of organics appears a very promising technology for the removal of these contaminants from polluted sites. 2001 Elsevier Science Ltd. All rights reserved.
Keywords: Phytoremediation; Organic contaminants; Soil pollution

1. Phytoremediation Phytoremediation is an emerging green technology that uses plants to remediate soil, sediment, surface water, and groundwater environments contaminated with toxic metals, organics, and radionuclides (Pradhan et al., 1998). Phytoremediation is an eective, non-intrusive, and inexpensive means of remediating soils (Wiltse et al., 1998). It is more cost-eective than alternative mechanical or chemical methods of removing hazardous compounds from the soil (Bollag et al., 1994). Besides, phytoremediation is a natural, aesthetically pleasing low-cost technology (Pradhan et al., 1998). It is socially accepted by surrounding communities and regulatory agencies as a potentially elegant and beautiful technology (Ensley, 1997). Although phytoremediation has been employed to remediate environments contaminated with metals, radionuclides, organics, etc. there appear to be many more works on the search for hyperaccumulators of metals than any other topic. In fact, most publications appear to deal with phytoextraction of metal contaminants. Besides, most phytoremediation review papers

Corresponding author. Tel.: +34-4-452-22-95; fax: +34-4-452-23-35. E-mail address: cgarbisu@neiker.net (C. Garbisu).

focus on the phytoextraction of metals and dedicate only a few paragraphs to the phytoremediation of organics. Nevertheless, in this context, it is worth mentioning the remarkable reviews on phytoremediation of organic pollutants written by Cunningham and Berti (1993), Cunningham et al. (1995, 1996). As overwhelmingly positive results have become available regarding the ability of plants to degrade certain organic compounds, more and more people are getting involved in the phytoremediation of organic contaminants. Actually, the concept of using plants to remediate soils contaminated with organic pollutants is based on observations that disappearance of organic chemicals is accelerated in vegetated soils compared with surrounding nonvegetated bulk soils (Burken and Schnoor, 1996; Cunningham and Berti, 1993). Phytoremediation of organic contaminants has generally focused on three classes of compounds: chlorinated solvents, explosives and petroleum hydrocarbons. Nonetheless, in recent years, researchers have begun to address the potential of phytoremediation to treat other organic contaminants including polynuclear aromatic hydrocarbons (PAHs) and polychlorinated biphenyls (PCBs) (Ferro et al., 1994). Although correlations between agronomic performance and phytoremediation potential are yet to be determined, better agronomic performance of the plant may improve phytoremediation. Plants that are less

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aected by compounds in contaminated soils are healthier and more persistent and will produce healthier root systems and greater top growth (Wiltse et al., 1998). 2. Phytoremediation ex planta There are two dierent strategies for the phytoremediation of organics: direct phytoremediation and phytoremediation explanta (Anderson et al., 1993; Cunningham et al., 1995; Salt et al., 1998). The latter is based on the secretion by plants of their photosynthate in root exudates, which support the growth and metabolic activities of diverse fungal and bacterial communities in the rhizosphere (Anderson et al., 1994; Shimp et al., 1993). Some organic compounds in root exudates (i.e., phenolics, organic acids, alcohols, proteins) may serve as carbon and nitrogen sources for growth and long-term survival of microorganisms that are capable of degrading organic pollutants. Densities of rhizospheric bacteria can be as much as two to four orders of magnitude greater than populations in the surrounding bulk soils as well as displaying a greater range of metabolic capabilities (Anderson et al., 1994; Walton et al., 1994; Salt et al., 1998). The chemical composition of root exudates and rates of exudation dier considerably among plant species (Rao, 1990; Salt et al., 1998). This has led some research groups to screen for plant species that exude phenols capable of supporting PCB-degrading bacteria (Fletcher and Hedge, 1995; Salt et al., 1998). Since not all plants produce and release the same types of phenolics (Rao, 1990), it would be expected that some plants may preferentially harbor PCB-degrading (polychlorinated phenols) bacteria in their rhizosphere (Wenzel et al., 1999). Fletcher and Hedge (1995) screened 17 dierent perennial plants for release of phenols that could support PCB-degrading microbes and found that mulberry (Morus rubra L.) had many attributes that would favor its use in phytoremediation eorts. Rhizospheric microorganisms may also accelerate remediation processes by volatilizing organics such as PAHs (polynuclear aromatic hydrocarbons) or by increasing the production of humic substances from organic pollutants (Cunningham et al., 1996; Dec and Bollag, 1994). Similar experiments have been performed to remediate soils contaminated with TCE (trichloroethylene) and TNT (trinitrotoluene) (Anderson and Walton, 1995; Foth, 1990; Wolfe et al., 1993). 3. Plant-derived degradative enzymes In addition to secreting organic compounds that support the growth and activities of rhizospheric microorganisms, plants also release a number of enzymes

into soils and waters and these enzymes degrade organic contaminants (Salt et al., 1998; Wenzel et al., 1999). Soil enzymes derived from plant sources include laccases, dehalogenases, nitroreductases, nitrilases and peroxidases (Boyajian and Carreira, 1997; Carreira and Wolfe, 1995; Schnoor et al., 1995). Field tests of plant-derived nitroreductases and laccases showed signicant degradation of ammunition wastes (TNT, dinitromonoaminotoluene, and mononitrodiaminotoluene) and triaminotoluene, respectively (Wolfe et al., 1993). Boyajian and Carreira (1997) reported on the ability of nitroreductase to degrade various additional nitroaromatic compounds. Similarly, other studies have examined the ability of a nitrilase to degrade 4-chlorobenzonitrile and of halogenases to metabolize hexachloroethane and TCE (Wenzel et al., 1999). The degree of enzyme release into soils and sediments remains poorly understood but the measured half-life of these enzymes suggests they may actively degrade soil contaminants for days following their release from plant tissues (Schnoor et al., 1995). The presence of plant-derived enzymes capable of degrading environmentally problematic xenobiotics will no doubt be exploited for the development of future phytoremediation strategies (Salt et al., 1998). 4. Direct uptake of organic contaminants By analogy with the phytoextraction of metals, direct uptake of organic contaminants is primarily limited by the availability of the target compound and uptake mechanisms (Salt et al., 1998). With a few notable exceptions, movement of organics into plants occurs via the liquid phase of the soil, which has been extensively investigated in plants for uptake of pesticides and herbicides (Briggs et al., 1982; Paterson et al., 1990; Topp et al., 1986). The primary factors that govern the uptake of xenobiotics are the physicochemical characteristics of the compound, i.e., the octanol-water partition coecient, log Kow , acidity constant, pKa , concentration and others (Wenzel et al., 1999). Organics that are most likely to be taken up by plants are moderately hydrophobic compounds with octanolwater partition coecients ranging from 0.5 to 3 (Briggs et al., 1982; Ryan et al., 1988; Wenzel et al., 1999). In addition to factors that govern the bioavailability of organics for uptake, there appears to be a signicant disparity in the uptake and translocation of organics among plant species, as observed for nitrobenzene (MacFarlane et al., 1990) and atrazine (Anderson and Walton, 1995; Burken and Schnoor, 1996). Dierences in evapotranspiration rates that are known to have a marked eect on the contaminant uptake could explain these dierences (Burken and Schnoor, 1996).

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As mentioned above, bioavailability of organics in soils appears to be a primary restriction for eective phytoremediation of organic pollutants (Cunningham et al., 1996; Schnoor et al., 1995; Salt et al., 1998). The application of soil amendments has been considered a major breakthrough in the development of ``induced'' (as opposed to ``continuous'') metal phytoextraction strategies. Unfortunately, similar attempts have not been made in relation to organic uptake of plants. The use of synthetic (triton X-100, SDS) and naturally-produced biosurfactants (rhamnolipids) to enhance the apparent water solubility and bacterial degradation of organic contaminants is well documented (Bragg et al., 1994; Desai and Banat, 1997; Providenti et al., 1995; Van Dyke et al., 1993; Zajic and Panchel, 1976). It has also been reported (Brusseau et al., 1997) that cyclodextrins increase the solubilities of both organics and metals. Potential advantages of using biosurfactants or cyclodextrins which have the ability to solubilize both organics and metals (Miller, 1995; Nivas et al., 1996) could be instrumental in remediation of soils with mixed contaminants. If plants are to be used for phytoextraction of organic contaminants it is essential to determine the fate of the parent compounds and their metabolites (Wenzel et al., 1999). The partitioning of organics between roots and aboveground tissues varies considerably depending on the chemical in question. Following uptake, organic compounds may have multiple fates: they may be translocated to other plant tissues (Cataldo et al., 1987; Fellows et al., 1996; Schroll et al., 1994) and subsequently volatilized, they may undergo partial or complete degradation (Goel et al., 1997; Newman et al., 1997; Schnoor et al., 1995; Wolfe et al., 1993) or they may be transformed to less toxic compounds and bound in plant tissues to nonavailable forms (Field and Thurman, 1996). Schroll et al. (1994) found that hexachlorobenzene (HBC) and octachlorodibenzo-p-dioxin (OCDD) could be taken up by roots or leaves but that no translocation from roots to shoots or vice versa was observed. On the other hand, root and foliar uptake of the herbicides chlorobenzene and trichloroacetic (TCA) was followed by translocation in both directions (Wenzel et al., 1999). Preferential concentration in the roots has also been documented for TNT and aniline and in shoots for hexahydro-1,3,5-trinitro-1,3,5-trizazine (RDX), phenol, and quinoline following uptake by roots (Cataldo et al., 1987; Fellows et al., 1996; Wenzel et al., 1999). Most organics appear to undergo some degree of transformation in plant cells before being sequestered in vacuoles or bound to insoluble cellular structures, such as lignin (Salt et al., 1998). However, few chemicals appear to be fully mineralized by plants to water and CO2 , and where this does occur, it represents only a small percentage of the total parent compound (New-

man et al., 1997). This property puts plants at a relative disadvantage compared with bacteria in degrading organic pollutants. In addition, the possibility that plant metabolites of pollutants may be more toxic than the original pollutants creates a dicult regulatory environment for remediation of organics.

5. Conclusions Phytoremediation of organic compounds is still a growing technology. There is a need for researchers and regulators to pool resources and share knowledge that is being gained both in the laboratory and in the eld (Newman et al., 1998). The recomendation is made that the practitioners of phytoremediation test the eectiveness of a given plant toward a particular compound since the eciencies of plants to take up and degrade that compound may vary enormously. References
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