Phytoremediation: Cleaning Environment Using Plants

Phytoremediation: Cleaning Environment Using Plants

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ISBN-978-93-86932-20-4

13 Phytoremediation: Cleaning Environment Using Plants Arvinder Singh1 and Yogesh Kumar2 1Department

of Botany, Akal University, Talwandi Sabo (Bathinda), Punjab–151302 of Botany, Kurukshetra University, Kurukshetra-136119 1Corresponding author: [email protected]

2Department

ABSTRACT With increasing use of pesticides and contaminated water in modern agriculture in parallel to industrial development has resulted in pollution of natural resources like water and soil with heavy metals and other inorganic substances. It is the present day environmental concern. Their remediation from soils and water is also the most difficult using the existing physical and chemical cleanup techniques which are highly costly. So, it led to the development of new cleanup technologies that have the potential to be low-cost, low-impact, visually benign, and environmentally friendly. Phytoremediation is a new concept that involves the use of green plants to remove environmental contaminants such as arsenic, mercury, lead, zinc, TNT etc., from the soil and water. It employs several ways like phytoaccumulation, phytodegradation, rhizofilteration, phytovolatizaion and phytoimmobilzation depending upon the nature of metals and soil properties and types. Number of plants namely Indian mustard, poplar, water hyacinth, duckweed etc., have been explored and being used in remediation process. Further, attempts to increase the heavy metal extraction efficiency, and also to introduce hyperaccumulator phenotypes in non-hypoaccumulator plants, genetic engineering techniques have been successful in introducing genes from bacteria and other organisms to produce transgenic plants.

INTRODUCTION The people generally think of plants for their role in providing food, shelter and

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fuel. However, in recent years, the potential of plants to combat the environmental degradation has been highlighted. One of the major environmental concerns in present days is the contamination of soil and water due to continuous addition of organic and inorganic wastes generated by humans through industrial and urban activities. The organic wastes can be degraded by soil microorganisms but inorganic wastes require physical techniques to remove these from the soil. The inorganic wastes may include heavy metals, combustible substances, petroleum products etc., At higher concentration, these may prove to be toxic for the plants by replacing essential enzymes or pigments; so disrupting their functions. A number of methods have been used in past to make the soil free of contaminants. These involved exsitu as well as in-situ approaches. The former requires the removal of contaminated soil from the site, its detoxification and then, destruction of contaminant either physically or chemically and returning it back to resorted site. On the other hand, in-situ methods remediate the soil without excavation from the contaminated site. These involve: a) The diluting of contaminated soil with clean soil, b) Covering the soil with inert material, c) Immobilization of heavy metals, or d) By raising the soil pH level with the addition of lime (Kuhlman and Greenfield, 1999; Mann,1999). These physico-chemical techniques are generally responsible for making land useless to plant growth as these affect the soil microflora as well as fauna viz., mycorhizza, fungi and bacteria during the process of clearing contamination. So, the best way is to introduce metal accumulating plants at the site of soil contamination. The plants behave in different ways to survive in the soil or water contaminated with metals. They either prevents metals from entering into their aerial parts/restrict metals in their roots or tolerate the high concentration of heavy metals by intracellular chelator compounds. Another group of plants can concentrate metals in their aerial parts viz., shoots and leaves. So, these plants based technologies used for cleaning the contaminated soil, air and ground water are collectively termed as phytoremediation. Now a days, the term is also known as green remediation, botanoremediation and agroremediation. In the recent years, this green technology is growing rapidly as a method to solve environmental contamination (Alberto and Sigua, 2013). More than 400 species representing 0.2% of total angiospermic plants have been known to represent metal hyperaccumulators (Baker et al., 2000). Some examples of plants used in phyore-mediation practices are the following: water hyacinths (Eichornia crassipes); poplar trees (Populus spp.); forage kochia (Kochia spp); alfalfa (Medicago sativa); Ken-tucky bluegrass (Poa pratensis); Scirpus spp, coontail (Ceratophyllum demersum L.); American pondweed (Potamogeton nodosus); and the emergent common arrowhead (Sagittaria latifolia) (Freshwater Management Series, 2000). A number of studies have also been conducted to check the

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phytoremediation potential of mangroves and other wetland plant species like Rhizophora stylosa, Avicennia marina and Sonneratia apetala by different workers (Zhang et al. 2011, Sari et al. 2011, MacFarlane and Burchett, 2011). Their results revealed the accumulation of the different metals Cu, Pb, Zn Cd and Hg at varying concentrations in the roots and leaf tissue. Majority of the phytoremediation-related research in the past few years has been focussed on hyperaccumulator plants which are capable of accumulating 100 times more than the non-accumulators. But, recently rDNA technology has made it possible to develop transgenic plants which are more efficient than wild species in tolerating as well as accumulating heavy metals in their shoots or roots (Dhankar et al., 2002; Bennet et al., 2003). The primary objective of writing this Chapter is to concisely evaluate the various methods of phytoremediation, the mechanism of heavy metal uptake and the progress made in this technology using recent methods of molecular biology and biotechnology. PHYTOREMEDIATION METHODS The term phytoremediation (Greek words, phyto = plant and Latin, remediation = correct evil) was coined in 1991 which requires more effort than simply planting vegetation and, with minimal maintenance, assuming that the contaminant will disappear (Cunningham et al., 1997). Before selecting the most useful plants for the purpose, screening studies are required. The most important requirement to carry out efficient accumulation of metals is the selection of plants having vigorous growth, large biomass and deep root-system. Phytoremediation is done in variety of ways which include extraction of contaminants from soil or groundwater; concentration of contaminants in plant tissue; degradation of contaminants by various biotic or abiotic processes; volatilization or transpiration of volatile contaminants from plants to the air, or immobilization of contaminants in the root zone. However, These processes are briefly described here: a. Phytoextraction or Phytoaccumulation: It involves the planting of a crop species that has ability to accumulate contaminants in its shoots and leaves and, then harvesting the crop and removing the contaminants from the site (figure 1). Phytoextraction applies to metals (Ag, Cd, Co, Cr, Cu, Hg, Ni, Pb, Zn) metalloids (As, Se), radionuclides (Sr, Cs, U,), and non-metals (B) (Salt et al., 1995; Kumar et al.,1995) as these remain unchanged in their form within the plants. The plants employed for the phytoextraction should be able to produce high biomass rapidly, fast growth, should have dense and deep root system, high metal tolerance, resistance to pests and diseases as well as should be unattractive to animals so that risk of transferring the harmful metals to next trophic level be minimized. Hyper-accumulator (which can accumulate large amount of heavy metal in their biomass) plant species have been the main focus of phytoextarction process because these are able to accumulate metals 100 times more than the non-accumulators.

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Sunflower, Indian mustard, barley and Solanum nigrum are the few examples of hyperaccumulators. Generally, heavy metals are toxic for a plant but the hyperaccumulators tolerance could be attributed to certain possible physiological reason or the accumulation may provide a competitive advantage, a means to resist drought, inadvertent metal uptake, or a defence against herbivores or pathogens such as bacteria and fungi (Brooks, 1998a; Boyd, 1998). b. Rhizofiltration: This is also known as phytofilteration. This technique is used for removal of contaminants from the waste waters such as industrial discharge, agricultural run-off etc., It also works on the concentration technology but differs from phytoextraction in that the mechanism is root accumulation. The method involves the removal of those metals which have the primarily ability to retained within the roots like lead, cadmium etc., However, depending upon the contaminant, its concentration and the plant species, the metals after absorption could be translocated to other portions of the plants. A number of aquatic plants like water hyacinth (Eichhornia crassipes), duckweed (Lemna minor L.) and pennywort (Hydrocotyle umbellata L.) have the potential to remove heavy metals from the water. However, because of their small and slow growing roots, they seem to be less effective in doing so. The terrestrial plant species like sunflower and Indian mustard with much larger fibrous root system and surface area could be better choice for rhizofilteration of Cd, Cu, Cr, Ni and Pb from the water (Wang et al., 1996). Sunflower have successfully been implementedfor rhizofilteration at Chernobyl to remediate uranium contamination. c. Phytoimmobilization or in-situ inactivation: The contaminated sites where the large scale removal action or other in-situ remediation methods are not effectively applied, this strategy works efficiently. In this method, metals do not undergo ultimate degradation but remain captured in situ. Contaminant are absorbed and accumulated by roots, adsorbed onto the roots, or precipitated in the rhizosphere. Plants with high transpiration rate as well as dense root system like sedges, grasses are used in this method as these reduce or even prevent the mobility of the contaminants, preventing migration into the groundwater (Chottu et al., 2009). Disadvantages of phytostabilization include the necessity for long-term maintenance of the vegetation that the vegetation will be self-sustaining. d. Phytovolatization: Selenium, mercury and tritium are some of the metals removed from the contaminated soil using the approach called phytovolatization which involves taking up of these contaminants from the soil, transforming them into less toxic volatile form and then, transpiring into atmosphere. Transgenic Brassica and Nicotiana have already been produced for cleaning Hg-contaminated soils. Similarly, green alga, Chlorella, is being widely used for metabolizing the toxic selenium to volatize form, dimethylselenide.

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e. Phytodegradation: It is also known as phytotransformation. The plants contain certain degrading enzymes which can breakdown and transform the contaminants within themselves after uptaking and metabolizing these (Pivetz, 2001). These smaller pollutant molecules may then be used as metabolites by the plants as it grows, thus becoming incorporated into the plant tissues. Populas tree has the ability to taken up and then breaking down the major water contaminant Trichloroethylene as its metabolic components. Yeast, fungi, bacteria and other microorganisms consume and digest organic substances like fuels and solvents.

Fig. 1. Pictorial Representation for Phytoremediation Overview.

f. Rhizodegradation: It is the breakdown of organic contaminants in the soil through microbial activities that are enhanced by the root zone (rhizosphere). Roots exudates like sugars, amino acids, fatty acids, sterols, and fatty acids result in increased microbial activities in the soil which further expedite the biodegradation of organic contaminants in the soil. Further, soil physical conditions like soil aeration and soil moisture content can be affected by plant roots, thereby, enhancing favorable conditions for indigenous microorganisms to biodegrade the contaminants. Thus, by using different approaches as explained above, different plant species are employed to remediate the different contaminants as summarizes in Table1. Moreover, metal extraction depends upon the fraction of the metal available in the soil for uptake which in turns dictated by the physico-chemical properties of the soil. Further in case of water, contaminated by metals, it is quite easy to remediate as the metals are present in soluble forms. On the other hand, most of the metals in soil occur in bound form to organic as well as inorganic matters. So, these have to be first solubilize in the soil solution for uptake and then, accumulation by the plants. Chelating compounds increase metals availability in soil solution by helping them to leach out. These chelating agents keep the metals in plant available forms by increasing the concentration of these larger chelated ions in solution, and by

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decreasing the ability of the free ions to react with the soil. Natural chelating agents include organic acids such as citric and acetic acid and synthetic include EDTA, NTA, DTPA, MGDA and EDDHA MECHANISM OF UPTAKE Following mobilization in rhizosphere, metals are first taken into the root apoplast (free diffusional space outside the plasma membrane). Some of the total amount of metal up taken is transported into the cells, while some are transported further into the apoplast and some are bound to the cell wall substances. The metals in root cells have to cross the endodermis and casparian strip to reach the xylem. Several metal transporters carrying metal-ions help in transporting metals from root symplast into xylem apoplast and is probably driven by transpiration pump. Uptake of metal ions from xylem apoplast into shoot symplast is also mediated by metal transporters. Several classes of proteins are known to act as metal transporters namely CPx-type ATPases, Nramn–Natural resistance against macrophage protein family, CDF-Cation diffusor facilitated family and ZIP–Zinc Iron permease family of proteins (Williams et al., 2000). After their translocation to shoot cells, metals are detoxified and stored/sequestered in cellular locations where these will not damage the vital cellular functions. So, a general mechanism of detoxification involves the chelation of metal ions by a ligand and then sequesteration of metalligand complex into vacuoles (Figure 2).

Fig. 2 Vacuolar Sequestration of Heavy Metal in Plant Cell (Yang and Chu, 2011).

The sequesteration of thio-reactive metals is carried out by cysteine-rich and sulfur-rich peptides—the metallothioneins (MTs) and phytochelatins (PCs) respectively. Whereas MTs were first identified in mammalian tissues as Cd-binding peptides (Salt et al., 1998), PCs were in Yeast. Later on PCs have been reported in wide varieties of monocot and dicot plant species, gymnosperms and algae (Gekeler et al., 1989) The metals such as Ag (I), Cd (II). Co (II), Cu (II), Hg (II), and Ni (II) are sequestered by bonding with organic sulfur (R-SH) on the cysteine residues of these peptides.

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Table 1: Chemicals Plants can Remediate.

Plant Arabidopsis Bladder campion Brassica family (Indian Mustard & Broccoli) Buxaceae (boxwood) Compositae family Euphorbiaceae Tomato plant Trees in the Populus genus (Poplar, Cottonwood) Pennycress Sunflower genus Lemna (Duckweed) Parrot feather Pondweed, arrowroot, coontail Perennial rye grass

Chemical Mercury Zinc, Copper Selenium, Sulfur, Lead, Cadmium, Chromium, Nickel, Zinc, Copper, Cesium, Strontium Nickel Cesium, Strontium Nickel Lead, Zinc, Copper Pesticides, Atrazine, Trichloroethylene (TCE), Carbon tetrachloride, Nitrogen compounds, 2,4,6-trinitrotoluene (TNT), hexahydro-1,3,5trinitro-1,3,5 triazine (RDX) Zinc, Cadmium Cesium, Strontium, Uranium Explosives wastes Explosives wastes TNT, RDX Polychlorinatedphenyls (PCP's), polyaromatichydrocarbons (PAH's)

GENETICALLY ENGINEERED PLANTS FOR METAL UPTAKE/ TOLERANCE The first goal in phytoremediation is identifying the plant species that is capable of tolerating and accumulating a particular contaminant. Most of these plants are located near the areas where the soil rich in underground metal ores is present or around the boundary of polluted sites. Once these plants are identified, traditional breeding methods are used to optimize their tolerant behaviour towards particular contaminant. Now a day, genetic engineering techniques have made it possible to modify the existing metabolic pathways in these plants for more metal uptake, its accumulation and degradation. A number of genes for metal chelator, metal transport, metallothionein and phytochelatin (PC) peptides have been transferred/overexpressed in plants for improved metal uptake and sequestration (Table 2.). These genes help the plants in different ways. Metal chelator genes when expressed within plant tissue facilitate the movement of metals to above-ground parts out from the roots. Similarly, metallothioneins genes after its expression in transgenic plant increased the plant tolerance towards the high metal concentration rather than increase in its uptake. Another approach utilizes the transfer of genes for metal transport which enhances the ability of plants to uptake metal ions. Transgenic plants viz., Arabidopsis and tobacco, which detoxify or accumulate mercury, have been developed in recent years by transferring bacterial genes. Similarly, E. coli genes have also been transferred by different scientists in another plant species Brassica juncea for increased tolerance of this species towards cadmium and arsenic. Transgenic plants transferred with mouse Se-cys lyase gene have been shown an enhanced concentration of Se in their shoots when compared with to wild type.

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Alteration of oxidative stress related enzymes may also result in altered metal tolerance as in the case of enhanced Al tolerance by overexpression of glutathioneS-transferase and peroxidase. Table 2: Transgenic Plants Produced for Improved Metal Uptake. Transgenic plants Indian mustard

Gene/s transferred -ECS and Glutathione synthetase merA and merB

Origin of gene/s Bacteria

Indian mustard Arabidopsis

APS gene

Bacteria

Arsc and  -ecS

Bacteria

Indian mustard

APS and  -ECS or GS

Bacteria

Tobacco

Metallothionein (MT) gene

Mouse

Yellow Poplar

Bacteria

Results

Workers

More Cd accumulation than wild plants

Zhu et al. (1999)

Detoxifying mercury contaminated soil Three times more Se accumulation than wild 2-3 folds arsenic (As) accumulation than wild Accumulation of 1.5 times more Cd and 1.5- to 2fold more zinc (Zn) Increased heavy metal tolerance

Rugh et al. (1998) Pilon-Smits et al. (1999) Dhankar et al. (2002) Bennett et al. (2003) Maiti et al. (1991)

ADVANTAGES/DISADVANTAGES OF PHYTOREMEDIATION Phytoremediation technique provides number of advantages as compared to other physical and chemical techniques used for remediating the soil. It is really inexpensive and causes minimal environmental disturbance (Raskin and Ensley, 2000). Also, growing vegetation at the contaminated sites results in reducing wind and water erosion. Soil can be left at the site after contaminants are removed, rather than having to be disposed or isolated. As a green technology, it is applicable for varied organic and inorganic pollutants and provides aesthetic benefits to the environment using trees and creating green areas which is socially and psychologically beneficial for all (Ghosh and Singh, 2005). If the site is contaminated by more than one kind of pollutant, it has been shown to has potential to treat the site (Hegedus et al., 2009). However, several drawbacks and limitations are also associated with the process. Many growing seasons may be required to clean up the site. Only the soil containing contaminants up to the depth of a meter can be remediate with the process because of the short roots of the plants. However, trees can do the same upto 10-12 feet but the problem still persists in the deep aquifers. There still remains possibility of passing absorbed toxic metals to the next trophic level in the food chain. The use of invasive or nonnative species can affect biodiversity. Another concern associated with phytotechnology is the safe disposal of harvested biomass containing heavy metals. The need to harvest contaminated biomass and possibly dispose off it as hazardous waste subject to RCRA standards creates an added cost and represents a potential drawback to the technology.

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CONCLUSION Phytoremediation is an attractive technology of recent time for environment cleanup because of it is effective, environmentally friendly and inexpensive technology. The uptake of metal contaminants from the soil by plants, their translocation to the site of metabolism and then converting these to harmless products is well understood. However, at the present time, phytoremediation still seems to be a nascent technology that seeks to exploit the metabolic capabilities and growth habits of higher plants. Proteomics and DNA microarray techniques may be applied for searching the genes/proteins for phytoremediation. Results of such technologies help us better understanding of the plant metal metabolism and more efficient utilization of plants for cleaning our environment. Further, a multidisciplinary approach involving research endeavour of botanists, microbiologists, soil chemist and biotechology could help in finding new plant species with new strain of associated bioremediating microrganisms and their genes to make the phytoremediating technique more efficient in restoring the balance in metal stressed environment. SUMMARY Present day environmental concern is the pollution of soil and water with heavy metals and other inorganic contaminants. These are the most prevalent forms of contamination found at waste sites, and their remediation in soils and sediments is also the most difficult using the physical and chemical techniques. Moreover, these existing cleanup technologies are highly costly. It led to the search for new cleanup technologies that have the potential to be low-cost, low-impact, visually benign, and environmentally sound. Phytoremediation is a new concept that involves the use of green plants namely grasses, forbs, and woody species to remove environmental contaminants such as heavy metals, trace elements, organic compounds, and radioactive compounds present in soil or water. The removal of highly dilute contaminants is based on the well-known ability of plants and their associated rhizospheres. However, different approaches are used by plants to perform the process of remediation. These include phytoextraction or phytoaccumulation, phytovolatization, rhizodegradation, phytoimmobilization and rhizoinfilteration depending upon the plant species. Results of research and development into phytoremediation processes and techniques report it to be applicable to a broad range of contaminants including numerous metals and radionuclides, various organic compounds such as chlorinated solvents, BTEX, PCBs, PAHs, pesticides/insecticides, explosives, nutrients, and surfactants. The plants having the ability to accumulate heavy metals in their shoots are characterized by large biomass, with rapid growth and deep root system. These are termed as hyperaccumulator. Sunflower and Indian mustard are the example of this category and have been reported to be good accumulators of arsenic present in soil. However, for cleaning contaminated water systems, rhizofilteration is the appropriate way. This method was found suitable for accumulating the lead

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(Pb) and cadmium (Cd) contaminants in roots of the plants. Aquatic plants like water hyacinth and duckweed have been reported to have this potential. Selenium (Se), mercury (Hg) and tritium are some of the metals which could be removed from the contaminated soil using the another approach called phytovolatization. Transgenic brassica and some green alga like chlorella are widely being used for metabolizing the toxic selenium to volatize form. Besides aforementioned methods of phytoremediation, phytodegradation is also used by some woody species like Poplar tree which contain certain degrading enzymes within themselves. These enzymes breakdown the complex toxic compounds into simpler one which further may be used as metabolites as the plants grow. In addition to these, the plant rhizosphere contain a critical component called root-exudates. These complex root secretions like sugars, amino acids, fatty acids, sterols, and fatty acids enhance the microbial activities in the soil which further expedite the biodegradation of organic contaminants in the soil. Root exudates may also include enzymes such as nitroreductase, dehalogenases, and laccases which have important natural function of degrading organic contaminants that contain nitro groups (e.g., TNT, other explosives) or halogenated compounds (e.g., chlorinated hydrocarbons, many pesticides). Primarily, the effective soil remediation strategy depends upon the soil type and its properties or characteristics. Metals exist as a variety of chemical species in a dynamic equilibrium as governed by soil physical, chemical and biological properties. As the heavy metals are present in soluble forms in case of contaminated water, it is quite easy to remediate this. On the other hand, most of the metals in soil occur in bound form to organic as well as inorganic matters. So, this needs to be first solubilize in the soil solution for uptake and then, accumulation by the plants. For the purpose, certain kinds of chelators must be present in plants naturally or supplied externally. Chelating compounds increase metals availability in soil solution by helping them to leach out. These chelating agents keep the metals in plant available forms by increasing the concentration of these larger chelated ions in solution, and by decreasing the ability of the free ions to react with the soil. Natural chelating agents include organic acids such as citric and acetic acid and synthetic include EDTA, NTA, DTPA, MGDA and EDDHA. Once the root absorbs the metal ion from the soil, it passes through root apoplast to xylem apoplast, and then to shoot symplast with the help of metal transporters. Thereafter, metals are stored/sequestered in cellular locations where these will not damage the vital cellular functions. This step requires the use of cysteine-binding peptide namely, phytochelators (PC) and metallothionine (MT). Advanced fields like biotechnology and molecular biology have made it possible to transfer hyperaccumulator characteritics of a plant into fast-growing, high biomass yielding with deep root system non-accumulator plants that could be effectively used in phytoremediation. Now a day, recombinant DNA technology has resulted in the modification of

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the existing metabolic pathways in these plants for more metal uptake, its accumulation and degradation. A number of genes for metal chelator, metal transport, metallothionein and phytochelatin (PC) peptides have been transferred/overexpressed in plants for improved metal uptake and sequestration. Indian mustard have been modified by transferring APS gene from a bacteria which has made it three times more efficient in accumulating selenium than wild plant. Similarly, Metallothionein (MT) gene from mouse resulted in increasing heavy metal tolerance in tobacco plant. The primary advantages of using plants in bioremediation include-its costeffectiveness, more eco-friendly nature and its aestheticness than traditional methods. Another thing that plants also offer is a permanent, in situ, self sustained method of removal of soil contaminants. Moreover, these accumulated metals can be extracted more easily through the plant harvest than from the soil. Phytoextraction also enables scientists to reclaim and recycle a wide variety of precious useable metals from the soil. However, at the present time, phytoremediation still seems to be a nascent technology that seeks to exploit the metabolic capabilities and growth habits of higher plants. Further, a multidisciplinary approach involving research endeavour of botanists, microbiologists, soil chemist and biotechology could help in finding new plant species with new strain of associated bioremediating microrganisms and their genes to make the phytoremediating technique more efficient in restoring the balance in metal stressed environment. References • • • •

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