Phytoremediation of Toxins

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Phytoremediation, a subcategory of bioremediation, is generally defined as removal of toxins from the environment by the use of hyperaccumulator plants. This word has been derived from the Greek "Phyto" meaning plant, and Latin "Remedium" meaning refurbishing balance, removal, or remediation. Thus, in the process of phytoremediation, pollutant/toxins from contaminated soils, water or air are mitigated/removed by using plants which are able to hold, breakdown or remove metals, salts, insecticides, pesticides, organic solvents, toxic explosives, crude oil and its derivatives, and a variety of other contaminants from different environmental components. Phytoremediation is generally considered as efficient, inexpensive and environment-friendly technique, as compared to other mechanical or chemical methods of remediation that involves excavation of soil from contaminated site and ex-situ treatment for the removal of contaminants (Cunningham and Ow 1996).

Phytoremediation of contaminated soils can be achieved through various processes. These include phytoextraction, phytoimmobilization or phytostabiliza-tion, phytotransformation, phytodegradation, phytostimulation, phytovolatilization and rhizofiltration (Schwitzguebel 2000; Cummings 2009). Of these strategies, phytoextraction or phytoaccumulation consists of natural or induced (enhancement through use of chelating agents) potential of plants, algae and lichens to uptake and remove pollutants from soil, water environment by accumulating them into harvestable biomass. This method is traditionally used for the removal of heavy metals and salts from the contaminated soils. Phytostabilization is stabilization of the toxic pollutants over a long-term. Some plants have natural ability to immobilize pollutants by providing a region around the roots where these pollutants can be precipitated and stabilized. Unlike phytoextraction, phytostabilization involves sequestering of toxins into the rhizosphere, thereby preventing metal uptake by plant tissues. Therefore, pollutants turn out to be less mobile and bioavailable to plants, wildlife, livestock, and humans. Phytotransformation is the conversion of different types of organic pollutants by certain plant species to non-toxic substances. In addition, microorganisms living in soil and water and those associated with plant roots may metabolize these substances to non-toxic ones. However, it is imperative to note that these tenacious and complex compounds cannot be degraded to simple molecules such as water, carbon dioxide etc. by plant metabolism. However, in this process, a change in their chemical structure is brought about that reduces their tox-icity to living organisms. Phytostimulation involves the enhancement of uptake of pollutants by increasing the activity of soil microorganisms to degrade the contaminants. This involves normally the activity of those organisms that live in association with the roots of higher plants. Phytovolatilization is the removal of substances from soil or water and hence, their release into the atmosphere. Rhizofiltration is the filtration of contaminated water through a mass of roots so as to remove toxic substances or surplus nutrients (Raskin and Ensley 2000).

The use of phytoremediation approach for the removal of environmental toxins has been greatly appreciated due to its environmental friendliness. In comparison to the conventional methods being used for cleaning up contaminated soil that damage soil structure and hamper soil fertility, phytoextraction can clean up the soil without causing any major change in soil quality and fertility. Another potential benefit of phytoextraction is that it is comparatively cost-effective as compared to any other traditional clean up method in vogue. In addition, the effectiveness of plants in the process of phytoremediation can be easily monitored by their growth potential under contaminated soils (Salt et al. 1995,1997; McIntyre and Lewis 1997; Sadowsky 1999; Raskin and Ensley 2000; Schwitzguebel 2000). Despite all these advantages, the process of phytoremediation is criticized due to its certain limitations. For example, it can reclaim only surface soils as well as up to the depth occupied by the plant roots. As this process depends on the ability of plants to uptake and degrade/metabolize, so more time is required as compared to traditional but highly efficient methods used for cleaning of contaminated soils. In addition, with plant-based remediation systems, preventing leaching of pollutants to ground-water aquifers is not easy without the complete removal of the pollutants from the soil. The survival of the plants growing in the contaminated land is determined by the extent of toxicity of pollutants. Finally, there is always a risk of bio-accumulated contaminants in plants to enter into the food chain, from primary producers to primary consumers and upwards, and finally to humans (McIntyre and Lewis 1997; Chaudhry et al. 2002; Prasad 2004a, b; Lupino et al. 2005).

Remediation of saline soils by using highly salt tolerant plants (halophytes) has been suggested as an economical approach. Some halophytic species (e.g., those of Atriplex, Suaeda, Salsola, Chenopodium and Portulaca) could uptake salt ions through roots and metabolize or store them in the leaves through the process of phytoextraction (McKell 1994; Grieve and Suarez 1997). The salt uptake and accumulation by these halophytes can reduce the salt level at least at rhizospheric level, and make the soil suitable for growth of the agricultural crops with better yield (Zuccarini 2008). This approach seems to be effective because many halophytic and highly salt tolerant plant species naturally grow on highly saline soils and hence can be employed to reclaim saline soils. This approach appears to be less expensive when conventional soil reclamation and advanced biochemical and genetical modification approaches are costly. However, it should be clear that the salt tolerance ability varies greatly within species as well as within populations of the same species. In addition, it also depends on interaction of salinity stress with other environmental adversaries that limit plant growth under that set of environments (Ashraf 2004). Therefore, the successes of a particular halophyte may differ greatly under different environments that need to be explored by proper experimentation. In addition, if the phytoremediation potential of halophytes is aided by other conventional techniques, the amelioration processes would be more fast, effective, reliable and sustainable (Ashraf et al. 2008).

Heavy metals from contaminated soils can best be removed by phytoextrac-tion or phytoaccumulation techniques without destroying the soil structure and fertility. In this approach, toxic metals are absorbed and accumulated into the biomass that can be easily harvested and removed from the contaminated areas (Huang and Cunningham 1996; Chaney et al. 2000; Lasat 2000). Phytoextraction can be achieved using natural or chelate assisted extraction of heavy metals from the contaminated soils. Continuous or natural phytoextraction involves the removal of metals depending on the natural ability of a particular plant species to accumulate metal contaminants without showing any significant symptoms of toxicity (Salt et al. 1995, 1997). In contrast, in chelate assisted or induced phytoextraction, the phytoremediation potential of different species is enhanced by synthetic chelates such as ethylenediaminetetraacetic acid (EDTA), S,S-ethylenediaminedisuccinic acid (EDDS), trisodium nitrilotriacetate (Na3NTA), N-hydroxyethyl-ethylenediamine-triacetic acid (HEDTA), ethylenediamine di-(o-hyroxyphenylacetic acid) (EDDHA), trans-1,2-diaminocyclohexane-N,N,N',N'-tetraacetic acid (CDTA), ethylene glycol-bis(^-aminoethyl ether),

N,N,N ',N-tetraacetic acid (EGTA), and diethylenetriaminepentaacetic acid (DTPA) (Blaylock et al. 1997; Kulli et al. 1999; Kayser et al. 2000; Grcman et al. 2003; Kos and Lestan 2003). These chelates generally increase the mobility and uptake of metal contaminants by plants many-folds as compared to natural conditions. However, it must be understood that the success of phytoextraction technique mainly depends on the ability of a plant species to (i) extract large quantities of heavy metals into their roots, (ii) translocate the heavy metals to above-ground parts, and (ii) produce a large quantity of plant biomass (Grcman et al. 2003; Kos and Lestan 2003; Luo et al. 2004). Other factors such as growth rate, element selectivity, resistance to disease, methods of harvesting, are also important in determining the success of this technique (Baker et al. 1994; Cunningham and Ow 1996). Therefore, slow growth, shallow root system and small biomass production limit the potential of hyperaccumulator species (Brooks 1994). This technique has successfully been used for the removal of almost all known metal contaminants by various plant species.

Phytovolatilization involves the uptake of contaminants from polluted soil and their transformation into volatile compounds and their extraction into the atmosphere by transpiration. This technique is relatively less useful for removal of heavy metals as the pollutant must (i) be taken up by plants through roots, (ii) pass through the xylem to the leaves (iii) be converted into some volatilable compounds, and (iv) volatilize to the atmosphere (Mueller et al. 1999). Despite these limitations, this technique has been reported to be useful for the removal of mercury from the polluted soils by transgenic tobacco plants carrying bacterial mercury detoxification genes merA and merB (Rugh et al. 1996, 1998; Bizily et al. 1999, 2000). The genes (merA) encodes the enzyme mercuric ion reductase that reduces ionic mercury (Hg+) to the less toxic volatile Hg(0) using NADPH reducing equivalents. In this process, the mercuric ion is transformed into methylmercury (CH3Hg+) and phenylmercuric acetate (PMA), that are fat-soluble and finally to metallic elemental mercury Hg(0) that is volatile at room temperature (Langford and Ferner 1999). In another study, plants growing on high selenium media have been shown to produce volatile selenium in the form of dimethylselenide and dimethyldiselenide (Chaney et al. 2000). However, this technique has the biggest disadvantage that most of the pollutants evaporated into the atmosphere are likely to return back to the ecosystems by precipitation (Hussein et al. 2007). Additionally, the success of this technique has a been test only for a limited scale under controlled conditions and a lot of work has to be done for determining its effectiveness for other metals as well as under field conditions.

Rhizofiltration i.e., removal of metals by passing through a mass of roots, can be used for the removal of lead, cadmium, copper, nickel, zinc and chromium, which are primarily retained with in the roots (Chaudhuri et al. 2002; United States Environmental Protection Agency Reports 2000). This technique has been tested using different crop plants such as sunflower, Indian mustard, tobacco, rye, spinach and corn, as well as tree plants such as poplar (Chaney et al. 1997; Eapen et al. 2003; Pulford and Watson 2003; Biro and Takacs 2007; Lee and Yang 2009). Among these, sunflower and poplar have the greatest ability to remove metals from the contaminated environment (Prasad 2007; Zacchini et al. 2009). The greatest benefit of the rhizofiltration method is that it may be conducted in-situ, with plants being grown directly in the contaminated soil and water bodies. It does not involve removal and ex-situ treatment of contaminants. Therefore, it is considered as a relatively cheep procedure with low capital costs. Operational costs are also low but it depends on the type of contaminant as well as selection of plant species. Additionally, crop may be converted to biofuel, used as a substitute for fossil fuel or used in other domestic and agricultural purposes (Chaudhry et al. 2002; Rugh 2004). Despite this, the applicability of this method is very limited. First of all, the plants species selected may grow well in moderately contaminated areas but might show poor performance in highly contaminated sites. Secondly, contaminants that lie in deep soil below the rooting depth will not extracted by this method. Therefore, plants with shallow root system will not be much effective as the deep-rooted plants. Thirdly, it normally takes many years to reduce the concentration of the contaminant to regulatory levels. Fourthly, most sites are contaminated with a variety of contaminants including metals, inorganics and organics. In this case, the use of plants for removing the pollutant through rhizofiltration will not be sufficient and would require support of some other methods. Plants grown on polluted water and soils may become a threat to animal and human health. Therefore, a careful attention should be taken while harvesting and only non-fodder crops should be chosen for the remediation of soil and water through the rhizofiltration method (Cunningham and Ow 1996; Chaudhry et al. 2002).

In bioremediation of herbicides and pesticides, plant metabolism contributes to their removal by transformation, break down, stabilization or volatilization after uptake from soil and groundwater. Biodegradation of these chemicals is mainly carried out by both bacteria and plants. However, bacterial degradation of these chemicals is more efficient as compared to plants (Roberts et al. 1993; Allison et al. 1995; Hall et al. 2000; Hendersona et al. 2006; Liao and Xie 2008). Bioremediation by microbes is mostly active in the upper layer of the soil surface, where the organic matter is the source of nutrients for their activity (Navarro et al. 2004). The degradation process consists of formation of metabolites and their decomposition to inorganic and simple products that are generally harmless to living organisms (Sassman et al. 2004, Sparks 2003, Kale et al. 2001). Some fungal species such as Phanerochaete chrysosporium and Phanerochaete sordida have also been shown to actively degrade pesticides such as DDT from the contaminated soils. This extremely toxic chemical was transformed into comparatively less toxic products such as DDD and DDE (Bumpus and Aust 1987; Safferman et al. 1995). Although both these chemicals are less toxic to micro-organisms, which have the ability to metabolize and detoxify them into more simple products and their high concentration can prove extremely toxic to these organisms (Bumpus and Aust 1987; Safferman et al. 1995; Osano et al. 1999).

In addition to the role of bacteria in biodegradation of herbicides and pesticides, many plants contain certain enzymes that can break down and convert ammunition wastes, chlorinated solvents such as trichloroethylene and other herbicides to simpler and harmless molecules. The enzymes include oxygenases, dehaloge-nases and reductases (Black 1995). In some studies, it has bee reported that some grass species such as big bluestem, switchgrass, and yellow Indian-grass have a potential to remove pesticide residues from the contaminated soils. These species can develop a region around rhizosphere with microflora that can readily detoxify pesticide residues (Hoagland RE, Zablotowicz 1995; Marchand et al. 2002; Hendersona et al. 2006). Specific strains of atrazine-degrading bacteria have been shown to have atrazine chlorohydrolase that can enhance the rate of biotransformation of atrazine in soil. In addition, these prairie grasses were also found to reduce the rates of leaching of pesticides from soil to ground water (Hendersona et al. 2006). In another study by Coats and Anderson (1997) some members of Kochia sp. were found to be effective in degradation and detoxification of various chemicals such as atrazine and trifluralin. In this case, most of the degradation occurred in the rooting zone (rhizosphere), suggesting that micro-organisms residing in the rhizosphere of these plant were involved in enhanced degradation of these pesticides. Additional experimentation on members of Kochia sp. by the same authors have shown to be promising for the removal of pesticide from soils and groundwa-ter (Arthur and Coats 1998). In laboratory experiments, poplar tree with fast growth potential and deep root system were found to be very successful in the removal of atrazine and arochlor from soil and groundwater. In this case, poplar plantations absorbed and metabolized these harmful compounds to less toxic chemicals (Burken and Schnoor 1996; Burken and Schnoor 1997; Nair et al. 1993).

Various plant species have the potential to remove cyanides from the polluted environments. These include hybrid willows (Salix matssudana Koidz x Salix alba L.), weeping willows (Salix babylonica L.), basket willows (Salix viminalis), poplar (Populus deltoides), upright hedge-parsley (Torilis japonica), Chinese elder (Sambucus chinensis), snow-pine tree (Cedrus deodara (Roxb.) Loud), water hyacinth (Eichhornia crassipes) and many other plant species (Ebbs et al. 2003; Yu et al. 2004 2005; Larsen et al. 2004; Taebi et al. 2008). However, their remediation ability varies greatly and differs with plant species, age and level of toxin in the environment. Hence, the decision whether to use a particular species for phytoremediation of cyanides should be carefully evaluated before any sound recommendation. In addition, it has also been shown that the removal of cyanide may also be carried out by certain species of micro-organisms through the process of biodegradation (Dubey and Holmes 1995).

As mentioned earlier, some plant species have the ability to uptake, transport and detoxify the cyanogenic compounds. The basic detoxification mechanism in tolerant species is phytodegradation in which the conversion of cyanides to cyanogenic glycosides is carried out by specific enzymes. This helps these plants to reduce the level of cyanide to non-toxic levels and maintain growth under cyanide polluted environment. In view of a report a small amount of cyanides can also be evaporated through phytovolatilization (Trapp and Christiansen 2003). This postulation was confirmed by the work of Yu et al. (2004) in which it was found that 1.5% of total cyanide fraction could be evaporated through leaves. However, they suggested that this small fraction is not sufficient enough to confirm whether the process of phytovolatilization is involved in the removal of cyanides from contaminated soils. Later, Larsen et al. (2004) did not find a significant relationship between evaporation and removal of cyanides by basket willows. However, they confirmed the involvement of two potential enzymes beta-cyanoalanine synthase and beta-cyanoalanine hydrolase in the ability of willow to detoxify cyanides. This evidence, although insufficient, shows that bioremediation of cyanides from the environments polluted can be carried out mainly by biodegradation and on a limited scale through phytovolatilization.

The primary solution for the remediation of soils affected with explosive chemicals is soil evacuation and ex-situ treatment by incineration or secured land-filling. However, this method is extremely cost-intensive, destructive to the environment, and not practicable by any means. In this situation, bioremediation is an affordable and environment-friendly method and has been evaluated using a number of bacterial strains and a few plant species. A number of fungi, yeast, bacteria and other microorganisms present in the root zone (rhizosphere) of higher plants have been shown to break down organics such as explosives, fuels and solvents (French et al. 1998; Bhadra et al. 1999; Burken et al. 2000; Hawari et al. 2000). Among plants, willow and poplar have been extensively used in the cleaning-up of soils contaminated with toxic explosives. It has been reported that hybrid poplar (Populus deltoids x P. nigra) is very effective in removal of TNT when it was grown in hydroponic solution, but it translocated only 10% of total TNT to the foliar parts (Thompson et al. 1998). In another study, clones of hybrid willow (Salix clone EW-20) and Norway Spruce (Picea abies), were found to be very effective in readily metabolizing TNT to non-toxic intermediates (Schoenmuth and Pestemer 2004).

A limiting factor for using phytoremediation approach of explosives is that it is a very slow and in most of the cases an incomplete process. This leads to accumulation of a variety of intermediate metabolites that can be further incorporated into the food chain and may ultimately reach humans (Dietz and Schnoor 2001; Aken 2009). Recently, a number of bacterial genes have been introduced into plants to enhance inherent limitations of plant detoxification capacities. For example, various bacterial genes encoding enzymes involved in the detoxification of explosives have been successfully introduced in plants. In this regard, the genes encoding nitroreductase and cytochrome P450, have been successfully engineered in a number of plants. This has resulted in a considerable improvement in uptake, detoxification and tolerance to toxic explosives by these plant species (Cherian and Oliveira 2005; Park 2007; Aken 2009).

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