(PDF) Potential of Aquatic Macrophytes for Removing Contaminants from the Environment

The role of both terrestrial and aquatic plants in phytoremediation of various contaminants is well established. Phytoremediation has been successfully implemented at different locations, including military sites, agricultural fields, industrial units, mine tailings, and sewage and municipal wastewater treatment plants, with efficient capacity for removing various organic and inorganic pollutants through processes such as extraction, degradation, or stabilization. Aquatic macrophytes represent a diverse group of plants with an immense potential for removal/degradation of variety of contaminants, including heavy metals, inorganic/organic pollutants, radioactive wastes, and explosives. The present review emphasizes the role of aquatic macrophytes in phytoremediation technologies with due importance to each group irrespective of being free-floating, submerged, or emergent. Realizing the exorbitant abilities of aquatic macrophytes, their suitability for wider use in phytoremediation technologies including constructed wetlands is emphasized.

This article was downloaded by: [INFLIBNET India Order] On: 2 January 2010 Access details: Access Details: [subscription number 909277354] Publisher Taylor & Francis Informa Ltd Registered in England and Wales Registered Number: 1072954 Registered office: Mortimer House, 3741 Mortimer Street, London W1T 3JH, UK Critical Reviews in Environmental Science and Technology Publication details, including instructions for authors and subscription information: http://www.informaworld.com/smpp/title~content=t713606375 Potential of Aquatic Macrophytes for Removing Contaminants from the Environment Bhupinder Dhir a; P. Sharmila a; P. Pardha Saradhi a Department of Environmental Biology, University of Delhi, Delhi, India a To cite this Article Dhir, Bhupinder, Sharmila, P. and Saradhi, P. Pardha(2009) 'Potential of Aquatic Macrophytes for Removing Contaminants from the Environment', Critical Reviews in Environmental Science and Technology, 39: 9, 754 — 781 To link to this Article: DOI: 10.1080/10643380801977776 URL: http://dx.doi.org/10.1080/10643380801977776 PLEASE SCROLL DOWN FOR ARTICLE Full terms and conditions of use: http://www.informaworld.com/terms-and-conditions-of-access.pdf This article may be used for research, teaching and private study purposes. Any substantial or systematic reproduction, re-distribution, re-selling, loan or sub-licensing, systematic supply or distribution in any form to anyone is expressly forbidden. The publisher does not give any warranty express or implied or make any representation that the contents will be complete or accurate or up to date. The accuracy of any instructions, formulae and drug doses should be independently verified with primary sources. The publisher shall not be liable for any loss, actions, claims, proceedings, demand or costs or damages whatsoever or howsoever caused arising directly or indirectly in connection with or arising out of the use of this material. Critical Reviews in Environmental Science and Technology, 39:754–781, 2009 Copyright © Taylor & Francis Group, LLC ISSN: 1064-3389 print / 1547-6537 online DOI: 10.1080/10643380801977776 Potential of Aquatic Macrophytes for Removing Contaminants from the Environment BHUPINDER DHIR, P. SHARMILA, and P. PARDHA SARADHI Downloaded By: [INFLIBNET India Order] At: 09:07 2 January 2010 Department of Environmental Biology, University of Delhi, Delhi, India The role of both terrestrial and aquatic plants in phytoremediation of various contaminants is well established. Phytoremediation has been successfully implemented at different locations, including military sites, agricultural fields, industrial units, mine tailings, and sewage and municipal wastewater treatment plants, with efficient capacity for removing various organic and inorganic pollutants through processes such as extraction, degradation, or stabilization. Aquatic macrophytes represent a diverse group of plants with an immense potential for removal/degradation of variety of contaminants, including heavy metals, inorganic/organic pollutants, radioactive wastes, and explosives. The present review emphasizes the role of aquatic macrophytes in phytoremediation technologies with due importance to each group irrespective of being free-floating, submerged, or emergent. Realizing the exorbitant abilities of aquatic macrophytes, their suitability for wider use in phytoremediation technologies including constructed wetlands is emphasized. KEY WORDS: aquatic macrophytes, phytoremediation, heavy metals, organic contaminants INTRODUCTION Phytoremediation is an emerging cost-effective and eco-friendly technology that utilizes plants to remove, transform, or stabilize a variety of contaminants located in water, sediments, or soils.133 Both terrestrial and aquatic plant species have been exploited tremendously for application in Address correspondence to Bhupinder Dhir, Department of Environmental Biology, University of Delhi, Delhi 110007, India; E-mail: bhupdhir@yahoo.co.in 754 755 Macrophytes Remove Contaminants from the Environment TABLE 1. Phytoremediation processes and mechanisms of contaminant removal Number 1 2 3 4 5 Process Mechanism Rhizofiltration Phytostabilization Phytoextraction Phytovolatilization Phytotransformation Rhizosphere accumulation Complexation Hyper-accumulation Volatilization by leaves Degradation in plant Contaminant Organics/inorganics Inorganics Inorganics Organics/inorganics Organics Downloaded By: [INFLIBNET India Order] At: 09:07 2 January 2010 Source: Ghosh and Singh60 phytoremediation technology as they possess immense potential to detoxify, degrade, and/or remove contaminants from the environment.62 The aquatic and wetland plant species—in particular, free-floating, submerged (rooted), and semi-aquatic/emergent (rooted)—gained importance worldwide as they depict exorbitant efficiency to remove variety of contaminants, including heavy metals, radionuclides, explosives, and organic/inorganic pollutants from wastewaters,27,46,133,137,148,194 though the degree of potential for removal varies from species to species. The present review focuses on the efficacy of aquatic macrophytes for removal of various contaminants from the environment with emphasis to mechanisms involved in their removal and due importance to each group of aquatic macrophytes (i.e., free-floating, submerged, and emergent forms). The major categories of phytoremediation include phytoextraction, phytotransformation/phytodegradation, phytostabilization, phytovolatilization, and rhizofiltration (see Table 1).141 Phytostabilization involves sorption, precipitation, and/or complexation of organic contaminants and depends upon root ability to limit contaminant mobility and bioavailability in the soil. It is mainly used for the remediation of soil and sediments. Phytoextraction includes absorption, concentration, and precipitation of toxic metals and radionuclides from contaminated soils into plant biomass.29,147 Phytovolatilization involves the use of plants to take up contaminants (mainly metals) from the soil, transforming them into volatile form and transpiring them into the atmosphere. Phytodegradation is the breakdown of organic contaminants taken up by the plant into simpler molecules that are incorporated into the plant tissues.31 Rhizofiltration is a technique that involves the use of plants roots to remove contaminants such as heavy metals from aqueous environment. The nutrients absorbed by roots are concentrated in roots and shoots.31,46,208 Phytoextraction and rhizofiltration are modes of remediation reported mainly in free-floating species, while phytostabilization is also an important phenomenon associated with submerged and emergent plant species. In aquatic plants, the pollutants are removed via submerged roots in sediments and/or absorption from water column through leaves.18,149 756 B. Dhir et al. Downloaded By: [INFLIBNET India Order] At: 09:07 2 January 2010 HEAVY METALS Heavy metals form one of largest category of contaminants that are efficiently removed by aquatic plants. Biomass of aquatic macrophytes, whether living or non-living, has been used in abatement (removal) and monitoring of heavy metals.77,86,98,153 Aquatic macrophytes, whether free-floating, submerged, or emergent, have been known to possess the ability to sequester heavy metals.103,118,121,155,185,186 Nutrient uptake in aquatic plants takes place by root uptake and foliar absorption (rooted macrophytes) or by foliar absorption only (floating macrophytes).38,157 The metal bioremoval in aquatic plants include bioaccumulation (a slow, irreversible ion sequestration step) and biosorption (an initial, fast, reversible metal binding process). The kinetics for metal adsorption by aquatic plants well fit in Langmuir and Freundlich isotherms and follow first-order kinetics.91,114 The potential of free-floating plant species for heavy metal removal/accumulation has been studied extensively.32,97,104,113,126,159,183,194,203 Eichhornia crassipes (water hyacinth), Salvinia herzogii, Salvinia minima (water ferns), Pistia stratoites (water lettuce), Nasturtium officinale (watercress), Spirodela intermedia, Lemna minor (duckweeds), Azolla pinnata (water velvet) are some of the aquatic plant species well known for their potential to scavenge heavy metals (see Table 2). In free-floating aquatic plant species, the active (rapid) uptake of metal occurs mainly by roots,65,104,156 from where it is translocated to other plant parts, whereas passive process of metal uptake primarily involves adsorption when plant species are in direct contact with the medium and results in the accumulation of metals mainly in aerial parts of the plants.104 Submerged rooted plants also bear the potential for extraction of metals from water as well as sediments.86,89,90,139,152,177 A few submerged species well known for the efficacy to accumulate heavy metal include Potamogeton crispus (pondweed), Potamogeton pectinatus (American pondweed), Ceratophyllum demersum (coontail or hornwort), Vallisneria spiralis, Mentha aquatica, and Myriophyllum spicatum (parrotfeather) (water mint) (see Table 2). In submerged plant species, leaves are the main site of mineral uptake.107 The foliar absorption of heavy metals occurs by passive movement through the cuticle, where the negative charges of the pectin and cutin polymers of the thin cuticle and polygalacturonic acids of the cell walls create a suck inward. Due to an increase in charge density inward, the transport of positive metal ions takes place.133 The mechanism of metal uptake in submerged plant species involves passive penetration of ions into apparent free space (AFS), the active uptake of ions into cytoplasm, and the active storage of ions into vacuoles from the cytoplasm. Among the semi-aquatic/emergent plant species, Typha latifolia (cattail), Phragmites (common reed), Scirpus spp. (bulrush) gained importance because of metal removing abilities (see Table 2). Qian et al.134 reported 757 Macrophytes Remove Contaminants from the Environment TABLE 2. Aquatic macrophytes known for their potential to accumulate heavy metals Plant species Heavy metals Downloaded By: [INFLIBNET India Order] At: 09:07 2 January 2010 Eichhornia crassipes Cr, Cu, Ni, Zn, Cd, Hg, Ag, Pb, Pt Pistia stratiotes Cr, Fe, Mn, Cu, Zn Lemna trisulca Cd Lemna gibba As, Cd, Ni Lemna minor As, Pb, Ni, Cu, Cr Lemna polyrhiza Pb, Zn, Ni Wolffia globosa Cd, Cr Spirodela polyrhiza Cr, As Salvinia minima Cr, Ni, Cd, As Azolla pinnata Zn, Cr Azolla filiculoides Cd, Cr, Zn, Pb, Ni Ceratophyllum demersum As, Cd, Cr, Pb Accumulation References Free-floating Muramoto and Oki,118 4000–6000 mg Cr kg−1 Delgado et al.,41 Fargo d.w., 2230 µg Cd and Parsons,49 Low g−1 d.w., 6000–7000 et al.,99 Zhu et al.,208 mg Cu kg−1 d.w., Vesk et al.,183 Olguin 1,000 ng Hg g−1 d.w., et al.,126 Molisani 1200 mg Ni kg−1 d.w., et al.,117 Hu et al.78 10,000 mg Zn kg−1 d.w. Sen et al.,156 Chua,33 800–1600 mg Cr Zayed et al.,203 Maine kg−1 d.w., 1030 mg Cu et al.,104 Miretzky kg−1 d.w., 7.9 mg Fe et al.,113 Odjegba and g−1 d.w. Fasidi125 1000 µg Cd g−1 d.w. Huebert and Shay,79 Zaraynika and Ndapwadza,202 Prasad et al.132 14,000 mg Cd kg−1 d.w., Zayed et al.,203 1790 µg Ni kg−1 d.w., Mkandawire et al.,116 1021 mg As kg−1 d.w. Mkandawire and Dudel115 Dirilgen and Inel,44 800 µg Cu g−1 d.w., Rahmani and 2140 µg Cr g−1 d.w. Sternberg,135 Axtell et al.,8 Kara,87 Ater et al.7 Charpentier et al.,30 10 µg Pb mg−1 d.wt., Sharma and Gaur157 27 µg Zn g−1 d.w. 80.65 mg Cd g−1 d.w., Boonyapookana et al.,19 73 mg Cr g−1 d.w. Upatham et al.180 −1 7.65 n mol As g d.w. Tripathi and Chandra,175 Appenroth et al.,5 Rahman et al.136 10,930 mg Cd kg−1 d.w. Srivastav et al.,166,167 Olguin et al.,126 Hoffman et al.75 −1 4316 mg Zn kg d.w., Jain et al.,84 Noraho and Gaur,122 Arora et al.6 9125 µg Cr g−1 d.w. −1 Sela et al.,155 2600–9000 mg Cd kg Zhao et al.,205,206 d.w., 371 mg Pb kg−1 −1 Sanyahumbi et al.,151 d w., 1010 mg Ni kg Benaroya et al.,11 d.w., 1260 mg Zn g−1 Bunluesin et al.,23 d.w. Arora et al.6 Submerged Garg and Chandra,57 3858 µg Pb g−1 d.w., −1 Ornes and Sajwan,127 420 µg Cd g d.w. Keskinkan et al.,90 Zheng et al.,207 Saygideger and Dogan,152 Bunluesin et al.23 (Continued on next page) 758 B. Dhir et al. TABLE 2. Aquatic macrophytes known for their potential to accumulate heavy metals (Continued) Plant species Accumulation References Rai et al.,139 Tripathi et al.,177 Singh et al.161 Vallisneria spiralis Cr, Cu, Cd 1378 µg Cr g−1 d.w. Sinha et al.162,163 Myriophyllum spicatum Pb, Cd 36,500 mg Pb g−1 dry Wang et al.,184 Sivaci et al.164 wt., 2800 mg Cd g−1 dry wt Gallon et al.52 Myriophyllum exalbescens Al 127 µ mol Al g−1 d.w. Myriophyllum aquaticum Cu, Zn 4300 µg Zn g−1 d.w. Cardwell et al.27 Emergent Molisani et al.117 Elodea densa Hg 82–177 ng Hg g−1 d.w Ye et al.,197,198 Typha latifolia Cu, Ni, Fe, Pb 177–287 µg Cu g−1 Qian et al.134 d.w., 448–640 µg Ni g−1 d.w., 500–3200 µg Fe g−1 d.w. Zurayk et al.,209 Nasturtium officinale Cr, Cu, Zn, Ni 1350 mg Cr kg−1 d.w., 10,000–19,000 Kara87,88 mg Cu kg−1 d.w. Mentha longifolia Cr 1600 mg Cr kg−1 d.w. Zurayk et al.209 Mentha aquatica Ni, Fe, Zn, Cu 2925 mg Ni kg−1 d w. Zurayk et al.,210 Kamal et al.86 −1 Carbonell et al.,26 Spartina alterniflora As, Hg, Cu, Pb Al, 0.3–7.2 mg As kg d.w. Ansede et al.,4 Fe, Zn, Cr, Se Windham et al.189,190 Aksorn and Visoottiviseth3 Spartina patens Cd, As 250 mg Cd g−1 d.w. Zayed et al.,203 Carbonell et al.26 Scirpus robustus Cd, Se, Hg 200 mg Cd g−1 d.w. Zayed et al.,203 DeSouza et al.39 Scirpus lacustris Cr 950 mg Cr kg−1 dry Gupta et al.,65 Zhu wt. et al.208 Phragmites australis Cu, Ni, Pb, Cd 147 µg Cu g−1 d.w. Crowder and St-Cyr,34 Ye 162 µg Ni g−1 d.w. et al.,199 Windham et al.,189,190 Fitzgerald et al.51 Potamogeton pectinatus Downloaded By: [INFLIBNET India Order] At: 09:07 2 January 2010 Heavy metals Cd, Fe, Cu, Mn, Zn 266 µg Cd g−1 d.w. Abbreviation: d.w. = dry weight. Polygonum hydropiperoides (smartweed) as the best wetland species for heavy metal phytoremediation, due to its faster growth and high plant density. Emergent plants bioconcentrate metals from water and sediments, though the site where the metals are localized varies from species to species. Most of the plants retain more of the metal burden in belowground parts (roots), in contrast to a few other species that redistribute a greater proportion Downloaded By: [INFLIBNET India Order] At: 09:07 2 January 2010 Macrophytes Remove Contaminants from the Environment 759 in above-ground tissues, especially leaves. For example, Phragmites australis sequester metal belowground, while Spartina alterniflora release more via leaf excretion.185,191 The metal uptake by plants results in the transport of metals across the plasma membrane of root cells, xylem loading and translocation, and detoxification and sequestration of metals at cellular level. In general, the rate of absorption, accumulation, and translocation of metal in plants depends on plant species and is further regulated by environmental factors like the chemical speciation of the metal, temperature, pH, redox potential, and salinity. pH is important for the speciation of metals and thus regulates the availability of metals to macrophytes. The redox potential also regulate heavy metal uptake in plants. Low redox potentials support the metal binding to sulfides in sediments, thus immobilizing them.133 Other factors such as salinity decrease the uptake of metals in plants due to the formation of chloride complexes. Metal chelators released by plants and bacteria enhance bioavailability of metals. Chelators such as siderophores, organic acids, and phenolics release metal cations, making them bio-available for plants and hence promoting uptake.169 Several transport proteins including ATPases, Nramps, cation diffusion facilitator (CDF) proteins,188 and zinc ion permeases (ZIP)64 facilitate metal uptake in plants and also play an important role in homeostasis. Some plants possess an ability to absorb extraordinary high levels of contaminants from the environment followed by their concentration in roots, shoots, and/or leaves.140 The plant species that accumulate extraordinarily high levels (more than 1% of metal in their dry matter) of heavy metals are termed as metal hyperaccumulators.9 Some common metal hyperaccumulator aquatic plant species include Spirodela polyrhiza (i.e., Cr, Pb), Eichhornia crassipes (i.e., Cd, Zn), and Elodea nuttali (i.e., Cu).5,59,119,208 The hyperaccumulation of metals is associated with mechanism of hypertolerance that provide an insight into the various strategies adapted by plants to resist toxicity. The mechanisms known to contribute to heavy metal tolerance in plants include the following: r chelation-binding of metal ions by high-affinity ligands, which reduce the r r r r concentration of free metal ions in the solution and binding of metal ions via thiol-rich peptides such as phytochelatin (PC) and metallothionein (MT) synthesis,63 amino acids,143 and organic acids22,142,173 ; compartmentalization, the metal deposition in vacuoles driven by ATPdependent Cd/H+ antiport or ABC proteins or excretion by specific glands; alterations in membrane structures40 ; synthesis of stress metabolites and/or proteins121 ; efficient antioxidant machinery82,150 ; 760 B. Dhir et al. r biotransformation, the toxicity of the metal can be reduced by plants by the chemical reduction of the element and/or incorporation into organic compounds or enzymatic degradation; r reduced uptake or efflux pumping of metals at plasma membrane; and r binding to cell wall.69 The production of metallothioneins and phytochelatins induced by metals such as Cd, Ag, Pb, Cu, Hg, and Zn has been reported in several plant species, including Hydrilla verticillata, Vallisneria spiralis, and Pistia stratoites.66,67,138,176 Downloaded By: [INFLIBNET India Order] At: 09:07 2 January 2010 EXPLOSIVES The phytoremediation studies related to removal/degradation of explosives by aquatic macrophytes have been focused on removal of explosives such as 2,4,6-trinitrotoluene (TNT), hexahydro-1,3,5-trinitro-1,3,5-triazine (RDX), and octahydro-1,3,5,7-tetranitro 1,3,5,7 tetrazocine (HMX). Several aquatic plant species including Elodea michx (elodea), Phalaris sp. (canary grass), Ceratophyllum demersum, Potamogeton nodosus, Sagittaria latifolia (arrowhead) showed a capacity to remove explosives such as TNT and RDX from contaminated groundwater (see Table 3).12,15 In general, submerged aquatic plant species showed higher uptake and transformation potential when compared to free-floating species. The recent studies in phytoremediation of TNT using Myriophyllum aquaticum demonstrated the potential of aquatic macrophytes for oxidative and reductive metabolism of TNT. The rapid sorption/sequestration of explosives such as TNT is followed by reduction, resulting in the formation of primary reduction products, namely, 2-amino-4, 6-dinitrotoluene (2ADNT) and 4-amino-2, 6-dinitroluene (4ADNT) and their TABLE 3. Aquatic plant species with the potential for removing/accumulating explosives Plant species Contaminants Myriophyllum aquaticum TNT, RDX, HMX Myriophyllum spicatum Potamogeton nodosus Ceratophyllum demersum Elodea canadensis Phalaris arundinaceae Typha angustifolia Saggittaria latifolia Elodea canadensis Scirpus cyperinus TNT TNT, RDX TNT, RDX RDX, HMX TNT, RDX TNT, RDX TNT, RDX RDX, HMX TNT, RDX References Best et al.,12–14 Hughes et al.,80 Rivera et al.,145 Pavlostathis et al.,129 Bhadra et al.,16,17 Hughes et al.80 Best et al.,12,13 Bhadra et al.17 Best et al.,12,13 Bhadra et al.17 Rivera et al.,145 Best et al.13 Best et al.13,14 Best et al.13,14 Best et al.,12 Bhadra et al.17 Rivera et al.,145 Best et al.13,14 Best et al.12–14 Downloaded By: [INFLIBNET India Order] At: 09:07 2 January 2010 Macrophytes Remove Contaminants from the Environment 761 conjugates,12–14,16,129 whereas oxidative metabolism of TNT establishes the role of plausible enzymes as oxygenases, which are the cytochrome P-450 group of enzymes localized in microsomes (endoplasmic reticulum) of plant cells.16,71,80 The major oxidation products reported so far include 2, 4-dinitro6-hydoxy-benzyl alcohol, 2-amino-4, 6-dinitrobenzoic acid, and 2, 4-dinitro6-hydroxytoluene.16 The site of localization of TNT and metabolites varies from submerged to emergent plant species. In submerged species, leaves are reported as the major site of compartmentalization, whereas in emergent species, roots are sited as the major site followed by stem and leaves.13,129 The rate of removal of TNT by plant is rapid and varies with treatment conditions, such as plant density, contaminant concentration, and temperature. Studies revealed that the decline in TNT concentration from the aqueous medium is exponential and follows first-order kinetics as assessed by the Michealis–Menton model, while the uptake of TNT by aquatic plants including Myriophyllum aquaticum is a mixed, second-order rate that is a function of the mass of the plant.111,129 RADIONUCLIDES Aquatic plant species also exhibit an equally high potential to accumulate radionuclides (see Table 4).1,130,158 The accumulation of high levels of radionuclides such as 137 Cs, 60 Co, and 54 Mn have been reported in several aquatic plant species, including Potamogeton lucens, Potamogeton perfoliatus, Nuphar lutea (cow lily), Nitellopsis obtuse (starry stonewort), Phragmites australis, Typha latifolia, Elodea canadensis, Ceratophyllum demersum, and Myriophyllum spicatum.105,106,120 Duckweeds have been TABLE 4. Aquatic plant species with the potential for accumulating radiouclides Plant species Contaminant Hattink et al.,73 Wolterbeek et al.,193 Weltje et al.,187 Popa et al.131 60 Lemna gibba Co, 32 P, 134 Cs El-Shinawy and Abdel-Malik47 137 Azolla carolianiana Cs, 60 Co Popa et al.130 137 60 32 60 134 89 Ceratophyllum demersum Cs, Co, P, Co, Cs, Sr El-Shinawy and Abdel-Malik,47 Abdelmalik et al.,1,2 Shokod’ Ko et al.,158 Bolsunovskiı̆ et al.20 238 137 90 Potamogeton pectinatus U, Cs, Sr Kondo et al.92 90 Potamogeton lucens Sr Bolsunovskiı̆ et al.20 137 90 241 Elodea canadensis Cs, Sr, Am Shokod’ Ko et al.,158 Bolsunovskiı̆ et al.,20 Bolsunovsky et al.21 Lemna minor 140 La, 99 Tc, 60 References Co Downloaded By: [INFLIBNET India Order] At: 09:07 2 January 2010 762 B. Dhir et al. identified as the major group among aquatic plant species with potential for removal/degradation of radioactive wastes. Lemna minor (duckweed) showed great accumulation and retention of technetium (99 Tc), one of the radionuclide formed by considerable fission of nuclear fuels such as uranium (U) and plutonium (Pu). In aquatic plants, the major mode of entrance for − Tc is foliar absorption of TcO− 4 . Technetium (TcO4 ) taken up by plants is actively transported across the plasma membrane or transported to leaves, where it is photoreduced (chloroplast), followed by complexation with ligands present in the cell including proteins, cysteine, and glutathione.72,74,95 The total amount of Tc present in plants is the sum of both the pertechnetate and reduced Tc form.73 The uptake and reduction of radionuclides by aquatic plants is rapid. Kinetics revealed that radionuclide absorption by plants is time- and concentration-dependent and depicts first-order uptake rate.158,193 In general, the uptake of radionuclides in plants involves two steps: 1) passive: a rapid binding of metal ions to negatively charged groups on the cell surface and transport through the cell wall within a short duration; and 2) active: metabolically dependent penetration of metal ions through cell membrane, movement inside cytoplasm, and the bioaccumulation of the metal ions onto the protoplasts. The fractions of polysaccharides and lipids present on the cell surface are actively involved in the accumulation of radionuclides. The uptake of radionuclides is also facilitated by the presence of carbonate groups present on the surface of the plant.131 ORGANIC POLLUTANTS Aquatic plant species possess the potential to remove, sequester, and transform organic contaminants.37,96,178 The capacity of aquatic plants for uptake and accumulation of organophosphorus, organochlorine compounds, and chlorobenzenes has been studied extensively (see Table 5).54,55,61,144,192 The amount of organic compound sequestered by aquatic plants depends on the plant species, the biochemical composition of the plant tissues, and physico-chemical properties (Kow, aqueous solubility, volatility) of the contaminant. The passive uptake of contaminant is driven by availability of the contaminant in its protonated form. The protonated form of the contaminant is considered as the species available for biotic partitioning in plants, which further gets coupled to enzymatic transformation and compartmentalization Macrophytes Remove Contaminants from the Environment 763 TABLE 5. Aquatic plant species with the potential for removing/accumulating various organic contaminants Plant species Free-floating Eichhornia crassipes Lemna gibba Lemna minor Downloaded By: [INFLIBNET India Order] At: 09:07 2 January 2010 Spirodela oligorrhiza Contaminants Ethion, dicofol, cyhalothrin, pentachlorophenol Phenol, 2,4,5-trichlorophenol (TCP) 2,4,5-trichlorophenol (TCP), halogenated phenols Organophosphorus and organochlorine compounds (o,p-DDT, p,p-DDT), chlorobenzenes Submerged Myriophyllum aquaticum Simazine, o,p-2 DDT, p,p-2 DDT, HCA, CT, perchlorate Potamogeton crispus Phenol Ceratophyllum demersum Organophosphorus and organochlorine compounds, chlorobenzenes Elodea canadensis Phenanthracene, organophosphorus and organochlorine compounds, chlorobenzenes Elodea Hexachloroethane (HCA), DDT, Carbon tetrachloride (CT) Emergent Pontaderia cordata Oryzalin (herbicide) Scirpus lacustris Phenanthracene Reference Roy and Hanninen,146 Xia et al.195,196 Hafez et al.,68 Ensley et al.,48 Sharma et al.,158 Tront and Saunders178 Day and Saunders,37 Tront and Saunders,178 Tront et al.179 Gobas et al.,61 Wolf et al.,192 Rice et al.,144 Gao et al.54,55 Knuteson et al.,94 Nzengung et al.,123 Gao et al.54 Barber et al.10 Gobas et al.,61 Wolf et al.,192 Rice et al.,144 Gao et al.54,55 Gobas et al.,61 Wolf et al.,192 Rice et al.,144 Machate et al.,101 Gao et al.54,55 Nzengung et al.,123 Gao et al.,54 Garrison et al.58 Fernandez et al.50 Machate et al.101 in vacuoles.178 Kinetics revealed the concentration-dependent pseudo-firstorder rate coefficients for uptake of organic contaminants such as halogenated phenols by aquatic plants.179 The sequestration of organic compounds such as halogenated organic compounds by plants includes rapid physical (adsorption, absorption, partitioning) and chemical processes such as complexation and reaction with cuticular and membrane components.124 Kinetics revealed the first-order rate equations for the uptake and elimination of organic contaminants by aquatic plants.123,178 The potential of aquatic plants to sequester organic contaminants depends upon the plants lipid rich cuticle, which helps in the sequestration of lipophilic organic compounds.54,55,58,178 The metabolic pathways for the transformation of organic contaminants by aquatic plant species have been identified.37,48,54,55 The exposure of aquatic plants to organic chemicals results in rapid uptake or sequestration Downloaded By: [INFLIBNET India Order] At: 09:07 2 January 2010 764 B. Dhir et al. followed by transformation or degradation, which can be reductive or oxidative, resulting in the formation of metabolites, which finally get assimilated by covalent binding to plants.124 The phytoreduction reactions mainly include dehalogenation reactions, which have been reported specifically for halogenated compounds such as hexachloroethane (HCA), dichloro-diphenyl trichloroethane (DDT), and others.58,123 The phytoreduction products either get oxidized into polar compounds or are covalently bound to plant tissues (assimilated), though the concentration of reduction products is always higher for any plant species than the oxidation products.124 Garrison et al.58 reported enzyme-mediated reductive transformation processes in plants. A dehalogenase activity from Elodea that reductively transformed HCA to form perchloroethylene (PCE) is also reported.43,123 Studies with Elodea also established the reduction of DDT to corresponding DDD analogs, plant-bound fractions, and other unknown products.54,58 The mechanisms involved in the removal of halogenated organic compounds from water by aquatic plant species include rapid sequestration by partitioning to the lipophilic plant cuticles, phytoreduction to less halogenated metabolites, phytooxidation, and assimilation into plant tissues as non-toxic products, presumably formed by covalent binding with the plant tissues. The phytoreduction reactions in plants and are catalyzed by enzymes like dehalogenases, such as glutathione-S-transferase and Fe-S clusters in chloroplast ferredoxin, while phytooxidation and covalent binding (phytoassimilation process) are reactions mediated by oxidative-enzymes (possibly cytochrome P-450 with monooxygenase activity, glutathione, or laccase).124 Glutathione-S-transferases are the main group of enzymes involved in the detoxification of herbicides by conjugating them with tripeptide glutathione. Knuteson et al.94 suggested biodegradation involving dealkylation as the probable mechanism for metabolism of simazine (herbicide) into 2-chloro-4amino-6-isopropylamino-s-triazine or hydroxysimazine followed by storage of end products in vacuoles. INORGANIC CONTAMINANTS Aquatic plant species present in natural and constructed wetlands also depict the potential to remove excessive concentration of inorganic nutrients such as nitrogen and phosphorus from wastewaters.102,172 A few studies conducted with plant species such as Ceratophyllum demersum, Potamogeton crispus, Eichhornia crassipes, Elodea nuttallii, and Elodea canadensis proved the effective use of the plants in removing excess of inorganic nutrients such as nitrogen and phosphorus from hydroponic systems and microcosms.81,102,112,128,165,174 The nitrogen removed by plants showed assimilation predominantly in the form of ammonium and nitrate.165 The roots Macrophytes Remove Contaminants from the Environment 765 and leaves contributed relatively higher nutrient (inorganic nitrogen and phosphorus) uptake, especially in case of submerged plant species.102 Artificial wetlands having laterite-gravel rooted Phragmites mauritianus reactors showed improvement in wastewater quality by removing phosphorus and nitrogen. The reactors achieved a reduction efficiency of greater than 90% for phosphorus and greater than 60% for nitrogen after a five-day water retention time, though the mass balances indicated a higher uptake rate of phosphorus by the plant over nitrogen.154 Downloaded By: [INFLIBNET India Order] At: 09:07 2 January 2010 WETLANDS AND THEIR ROLE IN REMOVAL OF CONTAMINANTS Aquatic species form a major part of both natural and constructed wetlands. Constructed wetlands constitute a complex ecosystem, formed by the interaction of biological and physical components with an efficient mechanism capable of removing different types of contaminants from water.24,110 An artificial wetland is designed to improve water quality,85 and the efficiency is dependent on plant processes.70,170 The high purification activity of the plants is due to rapid growth in polluted wastewater and capacity to remove contaminants. In constructed wetlands, various emergent, submerged, and/or free-floating aquatic species are used. The common species include Myriophyllum sp, Elodea sp., Azolla sp., Lemna sp., Eichhornia crassipes, Scirpus maritimus, Scirpus robustus (salt marsh bulrush), Polypogon monospeliensis (rabbitfoot grass), Typha latifolia, Typha angustifolia, Typha latifolia (cattail), Juncus xiphioides (Irish-leaved rush), and Spartina sp. (see Table 2). For contaminants like heavy metals, the soils present in the wetland immobilize heavy metals in a highly reduced sulfite or metallic form,53 and plants play an important role in filtration, adsorption, and cation exchange through plant-induced chemical changes in rhizosphere.45 The roots act as filters, removing suspended particles from the water through mechanical and biological activity. Phytostabilization is the major approach for immobilization of metals in plants and storage in belowground parts such as root and soil, while phytoextraction involves the use of hyperaccumulators to remove metals. The degree of uptake is dependent upon plant species and environmental conditions. Ion uptake results from the contact of the plant with the medium and occurs directly through leaf cells.28 The site of metal accumulation and form in which they are absorbed varies from species to species. The submerged aquatic plant species such as Elatine triandra accumulate heavy metals such as As mainly in organic forms (e.g., methylarsonic acid and methylarsinic acid207 ) while semi-aquatic plant species such as Spartina alterniflora and Spartina patens accumulate inorganic arsenical in roots, and organic form dimethylarsinic acid is translocated to shoots.25 The tolerance mechanism in plants includes the sequestration of metals in tissues or cellular Downloaded By: [INFLIBNET India Order] At: 09:07 2 January 2010 766 B. Dhir et al. compartments (vacuoles), restricting the movement to shoots (avoidance).182 The plant species also tend to alter speciation of metals in the process of uptake/removal. For example, the uptake of Cr6+ by Eichhornia crassipes subsequently results in the reduction of toxic Cr6+ to less toxic Cr3+ .100 The root surface of wetland plants possess some specialized structures called metal-rich rhizoconcretions or plaques,181 which are mainly composed of iron hydroxides and/or Mn, which are immobilized and precipitated on the root surface. The plaques restrict metal uptake at low pH conditions but enhance that at higher pH.185 The rhizosphere associated with the plants also play an important role in the degradation and breakdown of contaminants. De Souza et al.39 reported low accumulation of Se and Hg in Scirpus robustus and Polypogon monospeliensis when antibiotics inhibited growth of bacteria present in the rhizosphere. In addition, mycorrhizae provides an interface between roots and soil, increasing the absorptive surface area of root hairs and thereby promoting the effective assimilation of metals present in toxic concentrations in soil.185 Constructed wetlands have been used for removing a wide range of inorganic contaminants, including heavy metals, perchlorate, cyanide, nitrate, and phosphate,76,108 as well as certain organic contaminants, including explosives and herbicides (see Table 6).83,101,109 A successful implementation of constructed wetlands for removing significant levels of trace elements such as selenium (Se) from the effluents was seen at oil refineries at San TABLE 6. Examples of constructed wetlands implemented successfully at different contaminated sites Site Lake Drainage District (TLDD) of San Joaquin Valley,Corcoran, California, USA Savannah River Site, Aiken, South Carolina, USA Lead-zinc mining facility (Tara Mines), Ireland Widows Creek Electric Utility, Alabama, USA; electrical power station at Springdale, Pennsylvania, USA Iowa Army Ammunition Plant, Iowa, USA Contaminants References Se Agricultural subsurfacedrainage Gao et al.56 Fe, Mn Industrial effluent Knox et al.93 Pb, Zn, Fe Mine wastewater O’Sullivanet al.168 Co, Ni, Fe, Mn, Coal combustion Cd byproduct ash leachate Ye et al.200 TNT Best et al.12 Milan Army Ammunition Plant, TNT, RDX Tennessee, USA San Joaquin Valley, California, USA Source Se Explosivescontaminated groundwater Explosivescontaminated groundwater Effluents from oil refineries Best et al.,13 Sikora et al.160 Hansen et al.70 Downloaded By: [INFLIBNET India Order] At: 09:07 2 January 2010 Macrophytes Remove Contaminants from the Environment 767 Francisco Bay-Delta and Tulare Lake Drainage district of San Joaquin Valley, California.70,204 It was observed that some proportion of the soluble Se entering the wetland became chemically reduced and bound to sediments, but a major portion of it was absorbed by plants, accumulated in roots, and volatilized. The plants and microbes (present in the roots) took up Se mainly in the form of selenate or selenite and metabolized it to volatile forms like dimethyl selenide (DMSe), which escaped to the atmosphere, minimizing the effects to other components of food chain. The process was referred as biological volatilization. Volatilization of Se involves the assimilation of inorganic Se into the organic selenoaminoacids selenocysteine (SeCys) and selenomethionine (SeMet). The latter can be methylated to form dimethylselenide (DMSe), which is volatile.56,171 Constructed wetlands using emergent plant species such as Scirpus cyperinus, Myriophyllum spicatum, and Typha latifolia have been used successfully used to treat groundwater contaminated with explosives13,14,160 and heavy metals from coal combustion byproduct leachate.200,201 Though the utility of wetlands for mass scale removal of contaminants is well established, a few questions regarding their functioning still need to be addressed. It is observed that metals taken up by roots are transported upward to aboveground tissues, but the route for their excretion is not clearly defined. The decomposing litter of plant species will get enriched with metals over time, which may leach or may become available to detritus feeders. As the levels of pollutants increase, the ability of a wetland system to incorporate wastes can be impaired, and the wetland itself can become the source of toxicity.185 BIOTECHNOLOGICAL APPROACH A transgenic approach can be used to target the genes responsible for overexpression or knockdown of membrane transporter proteins to enhance uptake, accumulation, and/or degradation of various contaminants. The genetic engineering programs for the development of transgenic wetland species such as Spartina sp., Typha sp., and Scirpus sp. by insertion of the Mer genes have been initiated.35,36 The wetland species Scirpus maritimus and Typha latifolia have shown the accumulation of toxic heavy metals such as Se that is facilitated by plant-bacteria interactions at the root interface, as well as further transformation by bacteria to organic form, which can be further excluded by methionine biosynthetic pathway or converted to volatile form that can escape into atmosphere.70 These prospective transgenic wetland plants can be planted in contaminated aquatic ecosystems or in constructed wetlands to clean up Hg or Se pollution. Realizing the capabilities of aquatic plants for removing various contaminants, it is desirable 768 B. Dhir et al. Downloaded By: [INFLIBNET India Order] At: 09:07 2 January 2010 to engineer high-biomass producing, fast-growing plants with an enhanced capacity to accumulate metals and degrade xenobiotics. Aquatic macrophytes possess an inbuilt potential to remove and degrade heavy metals and other contaminants, reducing them to non-toxic forms or incorporating them into organic compounds. The important features such as hardiness, high productivity, ease of handling, rapid growth, and tolerance to survive adverse environmental conditions together with higher bioaccumulation potential establish them as potential agents for phytotechnology. However, when aiming for a wider application of phytoremediation technology using aquatic plants, the exact mechanisms responsible for uptake, accumulation, and degradation need to be explored and understood at depth to utilize maximum potential of aquatic macrophytes. 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