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CRITICAL REVIEW

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A review with recent advancements on bioremediation-based abolition of heavy metals Nisha Gaur,* Gagan Flora, Mahavir Yadav and Archana Tiwari There has been a significant rise in the levels of heavy metals (Pb, As, Hg and Cd) due to their increased industrial usage causing a severe concern to public health. The accumulation of heavy metals generates oxidative stress in the body causing fatal effects to important biological processes leading to cell death. Therefore, there is an imperative need to explore efficient and effective methods for the eradication of these heavy metals as against the conventionally used uneconomical and time consuming strategies that have numerous environmental hazards. One such eco-friendly, low cost and efficient alternative to target heavy metals is bioremediation technology that utilizes various microorganisms, green plants or enzymes for the abolition of heavy metals from polluted sites. This review comprehensively discusses

Received 26th September 2013 Accepted 12th November 2013

toxicological manifestations of heavy metals along with the detailed description of bioremediation technologies employed such as phytoremediation and biosorption for the potential removal of these

DOI: 10.1039/c3em00491k

metals. It also updates readers about recent advances in bioremediation technologies like the use of

rsc.li/process-impacts

nanoparticles, non-living biomass and transgenic crops.

Environmental impact Levels of heavy metals are rising in the environment due to increased industrial usage causing severe damage to all spheres of life. Commonly followed methods like ion exchange, chemical precipitation, reverse osmosis, bio-piles, bio-slurries and land-lling are not only expensive but their byproducts are hazardous to the environment. Bioremediation is an upcoming technique which utilizes eco-friendly agents like enzymes, microorganisms and plants and can prove to be a suitable alternative for the elimination of these heavy metals. It is imperative to carry out conclusive research which can rene and improve this process to a level where it can be accepted universally. On this note this review throws light on the technology of bioremediation and discusses recent additions to this area.

Introduction Pollution refers to the state of existence of undesirable substances (pollutants) in the environment beyond a permissible limit which can harmfully affect every sphere of life. Sources of pollution can be both natural and anthropogenic. Natural sources include geothermal activities, comets, space dust and volcanic activities. Whereas, anthropogenic sources have arisen mainly on account of rapid industrialization and extensive use of chemical substances such as hydrocarbons, pesticides, chlorinated hydrocarbons and heavy metals.1 The latter mentioned source is the major contributor to pollution in contrast to the former.2 Out of a large number of aforementioned anthropogenic sources, toxicological manifestations caused by heavy metals are well known and are considered as highly detrimental. Lead (Pb), cadmium (Cd), arsenic (As) and mercury (Hg) are the major pollutants that bring about heavy metal toxicity. The non-biodegradable nature of these metals is the principle School of Biotechnology, Rajiv Gandhi Proudyogiki Vishwavidyalaya, Bhopal, M.P., India. E-mail: [email protected]; Tel: +91 8234884887

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reason that leads to their prolonged presence in the environment. Moreover, these metals can enter into the food chain and over a period of time become accumulated in the human body. This accumulation can cause many health effects which might be irreversible in nature.3 Chelation therapy is the mainstay of the treatment regime followed so far for curing heavy metal poisoning. However, this therapy is coupled with severe side effects as apart from the removal of toxic metals it also eliminates important minerals and metals from the body like iron (Fe), calcium (Ca), zinc (Zn) etc. which directly affects normal biological processes of the body.4 Thus, rather than a curative approach using chelation to treat heavy metal poisoning, a preventive approach can be an effective alternative focusing on the eradication of these heavy metals from the environment itself. Conventional methods like ion exchange, chemical precipitation, reverse osmosis, bio-piles, bio-slurries, and land-lling are used conventionally for the remediation of heavy metals present in water and soil.5 However, they suffer from a major drawback of being expensive owing to the requirement of sophisticated infrastructure. Moreover, they also generate toxic

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sludge which affects environment and might not completely remove the metals.6 Bioremediation is one such eco-friendly and sustainable process that can prove to be much more effective and efficient for eliminating heavy metals present in different spheres of the environment. This strategy aims to clean up the environment while maintaining the normal biological processes associated with it.7 According to Glazer and Nikaido, bioremediation is dened as a process that uses microorganisms, green plants or enzymes to treat the polluted sites for regaining their healthy condition.8 This technique is highly favored as it provides much better results through the application of low cost and economic inputs in comparison to conventional means. Bioremediation can thus be regarded as a highly cost-effective, eco-friendly and more pronounced solution to the problems arising due to the use of transition metals.

Heavy metal pollution in soil and water Heavy metals such as Pb, As, Cd and Hg are ubiquitous in nature and cause an unfavorable result on the surroundings particularly at high concentrations. Even though the heavy metals biochemical equivalence and geochemical cycles are normal components of the earth's crust, their concentration has become remarkably exacerbated following the advent of the industrial revolution which resulted in a manifold rise in the level of usage of these metals.9

These heavy metals are known to facilitate phytotoxicity through contamination of soil, a problem that has called for considerable attention over the past few decades. The presence of heavy metals in soil can considerably decrease the size of the microbial community along with reduction of environmental and biological activities such as organic matter mineralization and leaf litter decomposition.10 The level of contamination however depends on factors such as chemical composition, toxicity, mobility and varying bioavailability of the metal.11 As soon as these heavy metals come in contact with the soil surface they initially become readily adsorbed, which is followed by slow adsorption and distribution in the soil.12,13 When the plants grow on metal-polluted soil they tend to accumulate these heavy metals, which greatly affect their growth and development. This not only threatens their survival but also affects the life which consumes them. Owing to this contamination, a large amount of terrain has turned out to be dangerous and non-arable for humans and animals. In a manner similar to soil, both surface water and ground water can easily become contaminated by heavy metals through natural sources (leaching of ore, erosion of minerals with sediments and volcanic extruded products) or human activities (chemical fertilizers, pesticides, solid waste disposal, industrial and domestic wastes). Due to its polarity and hydrogen bonds, it may adsorb, dissolve and absorb many different compounds.

Nisha Gaur received her M.Tech in Biotechnology from Rajiv Gandhi Technological University, Bhopal, India. She is currently a research trainee at R&D department of Kilpest India Private Limited. Her research interests include bioremediation of organic and inorganic wastes.

Mahavir Yadav received his Ph.D in Molecular Biology at the Institute of Microbial Technology, Chandigarh, India. He is currently working as an Assistant Professor in the School of Biotechnology at Rajiv Gandhi Technological University, Bhopal, India. His research interests include biodiesel production and bioremediation of heavy metals.

Gagan Flora received his M.Tech in Biotechnology from Rajiv Gandhi Technological University, Bhopal, India. He will very soon be starting his doctorate studies. His research interests include toxicity of heavy metals.

Archana Tiwari received her Ph.D in Environmental Sciences from Barkatullah University, Bhopal, India. She is currently working as an Associate Professor and Head of the School of Biotechnology, Rajiv Gandhi Technological University, Bhopal, India. Her research interests include production of bioplastics from biological sources.

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Toxicity of heavy metals Metals having high atomic weight and a density of more than 5 g cm 3 are regarded as heavy metals or transition metals. More than 20 different kinds of heavy metals are found in nature but only a few of them are of concern to human health. According to the Agency for Toxic Substances and Disease Registry (ATSDR), lead, cadmium, arsenic and mercury are well known for showing a toxicity prole upon exposure. Although numerous cellular, intracellular and molecular mechanisms have been reported to underpin heavy metal toxicity, generation of oxidative stress is the well accepted mechanism which explains most of the arising symptoms14 (Fig. 1). Chiey, human exposure to these metals occurs from industries and toxic waste sites. The non-biodegradable nature of these heavy metals further results in their prolonged persistence in the environment. It is now known that existence of transition metals even at a very low concentration (picomolar) in humans can result in fatal health effects.15 1. Lead. Lead is a widely known ubiquitously present xenobiotic heavy metal. Its unique properties like high ductility, highly malleability, low melting point and soness makes it an important metal in industries such as automobiles, paint, ceramics, plastics etc.16 Due to this widespread usage, humans have become vulnerable targets for its exposure. No level of lead has been considered to be safe or benecial to living beings. Upon exposure it affects many organs like the nervous system, renal system, hematopoietic system, reproductive system and cardiovascular system, and shows some effects on bone. The nervous system is the most sensitive target compared to the others for lead-induced toxicity.17,18 High exposure of lead may cause fatal consequences like convulsions, lack of coordination, delirium and paralysis. It also affects the hematopoietic system which inhibits the

Fig. 1 Generation of oxidative stress in cell owing to exposure of heavy metals such as Pb+2, As+2, Cd+2, and Hg+2, leads to formation of reactive oxygen species and impairs anti-oxidant defense causing cell death.

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synthesis of hemoglobin and thus causes anemia. Renal dysfunction has also been reported on account of lead-induced toxicity.19,20 The major mechanism of lead-induced toxicity is induction of oxidative stress which occurs as a result of imbalance between pro-oxidant and anti-oxidant ratio. This imbalance brings about protein oxidation, lipid peroxidation and nucleic acid peroxidation making a cell prone to cell death.21 The ionic mechanism is the other mode of action of lead toxicity. In this process, lead mimics and substitutes other monovalent and bivalent ions like Na+, Ca2+, and Mg2+, and hinders many biological process like intracellular signaling, cell adhesion, protein folding, ionic transportation etc.17 Chelation therapy has been regarded as the mainstay treatment which involves introduction of chelating agents like calcium disodium ethylenediaminetetraacetic acid (CaNa2EDTA), D-penicillamine (DPA), Dimercaprol (BAL) and Succimer into the organism. These chelating agents then bind to the lead ions forming a complex known as a chelate which is excreted out of the body mainly through urine. Many natural anti-oxidants like vitamins (B, C and E), avonoids, and herbal avonoids have also been used for curing lead-induced toxicity.4 2. Cadmium. Cadmium is an extremely toxic metal having distinctive properties such as good lustre, high ductility, malleability and soness that have led to its extensive usage in diverse industries like Ni–Cd batteries, coatings and plating, and as stabilizers for plastics.22 It causes many adverse health effects by damaging kidney, liver, bone and cardiac tissues. The kidneys and liver are the chief targets for cadmium-induced toxicity. Nephropathy is the most common renal abnormality that occurs owing to cadmium exposure. Renal vitamin D metabolism is also affected when cadmium accumulates in the kidney.23 This signicantly brings about a calcium imbalance which leads to osteoporosis and osteomalacia as well as increased excretion of calcium (medical condition referred to as Itai-Itai).24 Cadmium is also regarded as a potent human carcinogen that is associated with high risk of renal and prostate cancer. It is also known to act as a robust mutagen and can cause multi-locus deletions. Cadmium weakens the antioxidant defense by severely reducing the intracellular glutathione levels. It also inhibits the activity of various antioxidant enzymes like superoxide dismutase and catalase along with generation of ROS.25 The combinatorial effect of these processes renders cells into a state of oxidative stress. The increased level of ROS causes damage to DNA and inhibits DNA repair resulting in mutation.23 3. Arsenic. According to the ATSDR, arsenic is regarded as the most common cause of acute heavy metal poisoning in adults and children.26 Arsenic is a ductile metalloid which exists in three allotropic forms: metallic grey, yellow and black arsenic. It is broadly used to make insecticides, fungicides, weed killer, antifouling agents and in preserving woods. Clinical manifestation of arsenic is referred to as Arsenicosis and is caused by the prolonged exposure of arsenic in humans. Pigmentation (development of spotty rain drop patches over the front of chest) and keratosis are the toxic aermaths on the skin.27 Arsenic toxicity leads to many respiratory diseases like

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reduced pulmonary function, lung cancer, chronic cough or chronic bronchitis. Peripheral neuritis, black foot disease, liver brosis and gastroenteritis is also caused due to the uptake of arsenic-contaminated water.28 Unlike lead and cadmium, the molecular mechanism underlying arsenic toxicity is multi factorial. It involves generation of oxidative stress, suppression of DNA repair, inhibition of cell cycle check points and induction of apoptosis.29 Chelation therapy is considered as the most preferred approach to control the toxic effects of arsenic. Numerous avonoids, vitamins and herbal extracts have also been reported for curing and preventing arsenic-mediated cellular and molecular damage.26,30 4. Mercury. Mercury is a naturally occurring metal that can exist in inorganic, organic (ethyl-, methyl-, alkyl-, or phenylmercury) and vapor states, with the organic state considered more hazardous in comparison to other forms. It has both industrial (batteries, fossil fuel emission, paints, cosmetic products etc.) as well as clinical applications (thermometers, sphygmomanometer, barometers etc.).31 In the environment, its exposure occurs through the erosion of mercury-containing ores and in the form of gases dissipating from volcanic eruptions which are rich in mercury. The route of absorption of all forms of mercury is different. 95–100% of organic mercury (methylmercury) is absorbed in the intestinal tract and almost 100% gets inhaled through vapor. The absorption rate of elemental mercury is less as compared to organic mercury and is found to be around 75–85% occurring mainly through inhalation. Inorganic mercury is absorbed at much lower rates (7–15%) of ingested dose and 2–3% of dermal dose.31,32 Two forms of mercury, i.e. organic and elemental, are lipophilic in nature and become distributed throughout the body. Both forms can cross the blood brain barrier (BBB) and even the placental barrier and nally accumulate in the brain and kidneys. Whereas, inorganic mercury is not capable of crossing the BBB or placental barrier. It is found in the brain neonates and accumulates in the kidneys.31,33 Mercury is a powerful neurotoxin which primarily affects the central nervous system.34 It may lead to lack of coordination of movements, impairment of speech and hearing, and muscle weakness. The lungs absorbs metallic mercury through the breathing process which can lead to respiratory impairment. It has diverse mechanisms through which it can cause biochemical damage to tissues and genes. Mercury induces toxicity by forming free radicals and generating oxidative stress.35 It also bind to thiol-containing enzymes and inhibits them.31 Methylmercury forms complexes with cysteine, a thiol-containing compound, which helps in intracellular absorption.36

Environmental Science: Processes & Impacts

hydrocarbons, organic solvents and crude oil from soil and water to improve its quality.37,38 Although every plant has the capability to remove contaminants, only a few selected or engineered plants are used extensively to remove contaminants efficiently such as Clerodendrum infortunatum, Croton bonplandianus, Pistia stratiotes, Thlaspi caerluescens, Brassica junceae, Alysum lesbiacum, etc.39 Phytoremedial strategies applied in context to heavy metal elimination take into consideration any of the following methods depending upon the nature of the contaminant:  Complete removal of the accumulated heavy metals.  Degradation or containment of heavy metals.  Combination of these. Compared to conventional strategies being followed (in situ vitrication, soil incineration, excavation and landll, soil washing, soil ushing and solidication) phytoremediation is an aesthetically pleasing, efficient and eco-friendly process in removing contaminants from low to moderate levels.40,41 It is also an economical method which reduces the cost to less than the half the price of the conventional methods. Moreover, it requires low installation and maintenance costs. It also provides an added advantage by not only cleaning polluted soil but by also preventing soil erosion and metal leaching.42

Mechanism of phytoremediation Specically, the process of phytoremediation is broadly divided into two phases for the sequestration of heavy metals from soil and water: ex situ and in situ. The ex situ bioremediation process for soil and water is a two-step method. Firstly, it involves the excavation of contaminated soil or pumping out the groundwater for treatment. The soil and water is then subjected to several chemical and physical methods like chemical reduction/ oxidation, dehalogenation, soil washing, uid vapour extraction, stabilization/solidication, and solvent extraction to eradicate the contaminants.43 Thereaer, the treated soil or water which is free from heavy metals is restored back to the original site. The removed pollutants are then transported to some other site for dumping.42 Although, this approach is less time consuming and can be performed under controlled conditions, due to dumping and off-site burial of the removed contaminants at the time of treatment, it can act as another threat to the environment at another location.44

Phytoremediation: a robust strategy for the eradication of toxic heavy metals Phytoremediation is as an emerging technology that involves application of selected plants to degrade, assimilate, metabolize or detoxify undesirable substances like heavy metals, pesticides,

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Fig. 2

Different mechanisms involved in phytoremediation.

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Fig. 3

Mechanisms of phytoremediation.

The in situ method on the other hand is a technology which removes the heavy metals from contaminated soil, water and air without performing excavation and transport of contaminants. The treatment regimes are carried out at the same site that precludes off-site burial of the removed pollutants and thus prevents contamination of the clean soil.42 This method causes less ecological disturbance and is also economically viable which makes it a better alternative than ex situ technology. This method is further divided into different categories to remove toxic metals from soil and water: phytoextraction, phytoltration, phytostabilization, phytovolatilization, phytodegradation, and rhizodegradation (Fig. 2 and 3).

Phytoextraction Also known as phytoaccumulation, this process includes the extraction of toxic metals from soil and water without disturbing its integrity. The absorption and uptake of heavy metals is performed by plant roots followed by their translocation and nally accumulation and concentration above ground in the biomass (shoots).43 Generally, this method is favored for the sites that are discreetly or supercially polluted. The underlying mechanism behind phytoextration is hyperaccumulation. It is the process in which the plants like Pteris vittata L, Thlaspi rotundifolium (L.) Gaudin, Fagopyrum esculentum Moench, and Betula papyrifera Marsh can accumulate toxic metals at relatively higher concentrations. Hyperaccumulation is widely favored on metalliferous soils (soils affected with high concentrations of transition metals) and the plants which grow on this type of soil are referred to as metallophytes.45 The plants used for phytoextraction should have high hyper-accumulating capacity and should be capable of growing on highly toxic soils (and water) in order to make the

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extraction and translocation process of toxic metals in the shoots effective.46 In this process, regular cropping of the hyperaccumulator plant is required until the metal concentration reduces down to the desired level at the concerned site. Aer that the contaminated plant biomass is either burned and converted into ash or is used in various industries (e.g. wood, cardboard, etc.). This process can also be put into commercial use such as phytomining which essentially involves extraction of biomass in the form of bio-ore (extracts of saleable heavy metals obtained by the plant biomass ash).47 The phenomenon of hyperaccumulation is of two types: natural hyperaccumulation and chemically-enhanced hyperaccumulation. Natural hyperaccumulation utilizes specic kinds of hyperaccumulators capable of absorbing the toxic metals in the roots followed by its translocation in shoots. Finally, storage of these translocated heavy metals occurs the in aerial portion of the plant in a nontoxic form. These plants have high tolerance capacity and are credited with the ability of high translocation mobility of metals by secreting metal chelating compounds (phytosiderophores) and organic acids.48 Chemically-enhanced hyperaccumulation is applied in case of some metals like lead and gold that are immobile in soil and cannot be absorbed readily. For this purpose some chemical inducers like chelating agents (EDTA, NTA, malate etc.) or acidifying agents are used which enhance their mobility in the soil by increasing the bioavailability of the metals in soil which ultimately boosts their uptake.49 Kaur et al. reported that the chemically-enhanced phytoextraction showed better accumulation capacity as compared to the natural phytoextraction process. They also found that Brassica juncea arawali can act as an excellent chemicallyenhanced hyperaccumulator.50 A recent study showed the uptake of heavy metals from municipal solid waste by chelateassisted Festuca arundinacea. It was also reported that the nitrilotriacetic acid signicantly enhanced the metal accumulation capacity of Festuca arundinacea in contrast to its absence.51 In a phytoextraction analysis the effect of inducers like EDTA on texturally different soil was assessed. It was revealed that the induction of EDTA considerably enhanced the lead accumulation capacity of wheat shoots in loamy sand than that of the sandy clay loamy soil.52 In a recent study, assessment of natural plants in Turkish serpentine soil was carried out for analysis of its Ni accumulation capacity. Scientists tried to establish the possible relationship between amount of phytoavailable Ni in the soil and the Ni content of potential accumulator plants. It was found that susceptibility and Ni requirement of a plant was species specic. They presented Isati spinnatiloba as potential Ni hyperaccumulator species.53 Phytoextraction can be performed by three means i.e. phytoextraction by trees, by crops and by grasses. Each has its own advantages and disadvantages. Phytoextraction by trees produces high biomass but due to shedding of leaves on to surface the metal again becomes transported into the soil. Phytoextraction by grasses has high metal accumulation capacity but has low biomass production as well as slow growth rate. Phytoextraction by crops has both the above mentioned

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Environmental Science: Processes & Impacts

advantages. However, they pose a threat due to the ingestion of crops by herbivores and thus entry of metals into the food chain.54 There are four major steps involved in metal hyperaccumulation in plants:55 1. Bio-activation of trace metals in the rhizosphere. 2. Root adsorption and compartmentation with the help of transporters and chelators. 3. Metal uptake by shoots. 4. Distribution, detoxication, and sequestration of metal ions. Hyperaccumulators need to have the facility of metal homeostasis while growing in an impure surrounding. The Thlaspi family are hyperaccumulating plants among which twenty three species hyperaccumulate nickel, ten species hyperaccumulate zinc, three species (T. caerulescens, T. praecox and T. goesingense) hyperaccumulate cadmium and one species hyperaccumulates lead.56 T. caerulescens is regarded as one of the nest and well-known hyperaccumulators.57 Interestingly, this plant is able to grow in serpentine soils, which contain elevated levels of heavy metals including Zn, Co, Pb, Cr, Cd and Ni, being capable of up taking up to 30 000 and 1000 mg kg 1 Zn and Cd, respectively in their shoots, while its development remains unaffected.58 Moreover, due to the advancement in genetic engineering, the genes which help in remediation of heavy metals have been isolated and then inserted into the large biomass producing non-accumulating plants.59

advantages over rhizoltration because of the fact that seeds can grow independent of environmental conditions and absorb higher amounts of heavy metal during initial phase of their life cycle.66 Removal of lead from wastewater using Carexpendula was achieved by Yadav et al. using the rhizoltration technique. They carried out pot and simulation experiments and found that Carexpendula accumulated a signicant amount of lead especially in root biomass as compared to shoot.67 In another study, rhizoltration of cadmium and lead was performed by using four different macrophytes (Pistiastratiotes L., Salvinia auriculata Aubl, Salvinia minima Baker and Azollaliculoides Lam). It was seen that Pistiastratiotes L. had extensive bioaccumulation efficiency of removing lead and cadmium. The accumulation of these two heavy metals in the roots was 10-fold higher than that of the leaves.68 Vesely et al. reported the efficiency of organic acids to enhance the mobility of heavy metals through rhizoltration. They studied the bioaccumulation potential of Pistiastratiotes L. against the removal of Cd, Pb and Zn. They found that the organic acid substantially increased the mobility of all heavy metals. However, translocation of heavy metals decreased in the plant in a time-dependent manner.69 Rhizoltration has an advantage of absorbing metals readily but this method works only in water and not in soil. Moreover, metals get accumulated in the plant biomass which must be disposed of regularly to reduce the risk of contamination.70

Phytofiltration

Phytostabilization is a process which involves absorption and precipitation of contaminants like heavy metals by plants through immobilization. The process aims at the stabilization of the heavy metal at the contaminated site instead of its removal. This prevents movement of these contaminants via ground water and wind.71 The underlying mechanisms that determine the phenomenon of phytostabilization are as follows:72,73 (a) Phytostabilization in the root zone: In this the root gets exudated (converting contaminants into less bioavailable form) in the rhizosphere so as to immobilize the heavy metal in the root zone itself. (b) Phytostabilization of the root membrane: This step leads to the binding of the heavy metals to the root surfaces which prevents their entry inside the plant. (c) Phytostabilization in the root cells: This step further prevents the translocation of heavy metals by sequestering them into the cell vacuole. For effective phytostabilization, the plants should have rich root (to absorb large quantity of water) and shoot systems but a poor translocation mechanism so as to prevent entry of heavy metals into the shoots. Dense coverings of shoots tend to increase transpiration which prevents precipitation of heavy metals into the groundwater. Moreover, upward ow can be maintained by fast transpiration by plants which prevents downward leaching.62 Cambrolle et al. investigated the capability of two Spartina species in terms of phytostabilization and bioaccumulation of

This process can be carried out in both terrestrial and aquatic environments, though mainly it is carried out to purify ground water or other water bodies.60 This process enables the plant roots to absorb or adsorb, concentrate and precipitate the heavy metals from a polluted effluent source (industrial discharge, agricultural runoff, acid-mine drainage etc.). If plants use roots for remediation purposes then it is known as rhizoltration. Such kind of plants shows rapid growth of roots and removal time of toxic metals is minimal.61 This process involves absorption of heavy metals by plants roots followed by accumulation and transportation in the stem or leaves. The contaminants are removed through harvesting at an appropriate time.62 Development of feeder layer fertilization (suspending several layers of soil above a polluted stream of water through which the plant obtains the nutrients and simultaneously removes heavy metals) system led to a boost in rhizofertilization technology. Extensive root network development can be carried out by regular application of concentrated fertilizers to this feeder layer.63 A second generation technology which uses plant seedlings for the removal of heavy metals from contaminated water is known as blastoltration.64 The seedlings have the potential to absorb or adsorb a high percentage of toxic heavy metals. Special kind of seedling cultures are prepared through economic means using seeds, water and along with appropriate exposure to light and darkness.65 This process shows

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Phytostabilization

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heavy metals like Co, Cr and Ni in two marshes with different levels of contamination. They reported that in all the site samples, the concentration of these heavy metals in both species were higher in below-ground tissues as compared to the above-ground tissues. Both species of Spartina showed good phytostabilization capacity towards Co in the contaminated soil.74 Varun et al. reported the phytostabilization potential of Typhalatifolia L. in industrial sludge. Their ndings showed that Typhalatifolia L. had higher potential for immobilization of Zn, Mn, Cr and As but had less phytostabilisation potential towards Ni, Cd and Co.75 Recently, the phytostabilization capacity of six different plant species was assessed for the immobilization of the lead in mine tailing using eld and pot experiments. It was found that A. mangium had the best ability for phytostabilization towards lead mine tailing out of six plant species. A. mangium stored a higher concentration of lead in the roots which aerward could be used in the timber industry or paper industry etc.76 In another study, a Sorghum species was used by Soudek et al. for the immobilization of heavy metals (Zn, Cd) in soil deposited due to industrial activities. They found that initially the root had a higher concentration of heavy metal, but as the concentration of zinc and cadmium in the solution increased they were transferred into the shoots which ultimately caused toxicity to leaves. The toxicity affected the Chl a/b ratio in the leaves.77 This technology is highly cost-effective in nature and does not require the disposal of soil and contaminants aer treatment. However, this technology is not feasible for all sites (restricted only to water) and also requires containment of contaminants for an indenite period as they remain inside the soil for a long time.78

Phytovolatilization This process uses plants for the uptake of contaminants from soil and water followed by subsequent degradation into less toxic forms which are then transpired into the environment.79 Plants can volatilize both organic and inorganic contaminants provided that the inorganic contaminants should not form methyl and hydride derivatives.80 Contaminants which have high Henry's constant (KH is characteristic of particular solute, solvent and temperature)81 i.e. KH> 10 atm-m3 water per (m3 air) are applicable for the phytovolatilization mechanism.82 The mechanism includes open stomata of the leaves to diffuse volatile contaminants in the environment in less toxic forms. The plants used in this process shows high levels of ux of the pollutant towards the atmosphere through the transpiration process.80 This method not only removes the pollutants from contaminated site in a volatile form but the removal is done in safer forms of that particular pollutant. Sakakibara et al. reported the eradication of As through a remediation process by using Pterisvittata. They found that Pterisvettata had a good efficiency of volatilizing As (90%) from arsenic-polluted soil. However, secondary arsenic pollution was said to be caused if a large amount of arsenic is released into the environment.83 In another study, the effect of ethylene glycol on the phytovolatilization of 1,4-dioxane was estimated. DN34

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poplar trees were used for this study and it was seen that when 10 g l 1 of ethylene glycol was present in ground water it reduced the growth rate of plants to 28%. Similarly the effect of ethylene glycol on Arabidopsis was also observed and it was understood that ethylene glycol had an inhibitory effect on its growth and under hydroponic conditions it inhibited the phytovolatilization of 1,4-dioxane.84 Carvalho et al. carried out studies on four aquatic plants (Typha domingensis, Lemna obscura, Hydrilla verticillata Royle and Crinum americanum) for the removal of aqueous selenium. Initially, they found that the plants accumulated the selenium in their tissues. But, later it was concluded that the main mechanism behind selenium accumulation was phytovolatilization. In this process, plants converted the inorganic form of the selenium into the organic form which is less toxic and was then transpired.85 The advantage of this technology is that it does not require disposal of any contaminant thereby circumventing any site disturbance and erosion. This process is restricted only for abolition of volatile compounds and cannot be applied for the removal of nonvolatile heavy metals. However, the main disadvantage of phytovolatilization is that the heavy metals are still toxic to some level even when they are volatilized. The rate of their migration and translocation cannot be predicted in the polluted area.62

Phytodegradation This process exploits the capability of plants that possess certain specialized enzymes (dehalogenase, reductase and oxygenase) or cofactors for the degradation of contaminants from soil and groundwater.86 This method is limited only to organic pollutants because these are biodegradable in nature. Phytodegradation differs from rhizodegradation mainly because of the fact that the former encompasses the breakdown of contaminants with the help of microorganisms present in the rhizosphere and is a relatively slower mechanism. Flavonoids and carbohydrates secreted by plants facilitating phytodegradation further enhance the microbial activity. Properties like solubility, polarity, hydrophobicity and partitioning coefficient (Kd) of organic contaminants directly interferes with their entry into plant through the root membrane.87 For the removal of heavy metals some genetically modied plants have been developed such as transgenic poplars.88 Farias et al. worked on petroleum-contaminated soil and studied the tolerance and phytodegradation potential of Erythrina crista-galli L. in three different conditions: non-contaminated soil, vegetation-contaminated soil and non-vegetation contaminated soil. They found that the growth of Erythrina crista-galli L. in vegetation-contaminated soil was reduced as compared to non-contaminated soil. On the other hand the degradation of petroleum in vegetation-contaminated soil was higher as compared to non-contaminated soil.89 Recently, a study has been done on a transgenic tobacco plant which expresses bacterial organophosphorus hydrolase (an enzyme that degrades organophosphorus pesticides). Aer 14 days of growth it was found that the tobacco plant degraded more than 92% of methyl parathion and gives more root and shoot

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biomass as compared to the wild tobacco plant. This research holds importance for the removal of organophosphorus compounds from the environment.90

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Biosorption Biosorption is a process which uses biological materials for the removal of contaminants through different mechanisms like adsorption, absorption, surface complexation, precipitation and ion exchange. It depends on numerous factors like substance to be sorbed, environmental issues, biosorbent used, presence and absence of metabolic process (in living organisms).91 The two terms absorption (process in which one substance gets incorporated into another of different state) and adsorption (physical phenomenon in which adherence and binding of ions or molecule occur on the surface of another molecule) comes under sorption process. In the case of adsorption, the adsorbate is the substance which gets adsorbed on a solid surface and the adsorbent is the soil surface.92 If the adsorption phenomenon results in the formation of a stable molecular phase at the interface, it is described as a surface complex which can be of two types: inner and outer sphere surface complexes. In the former one, the adsorbent gets bound to at least one molecule of the hydration sphere of the adsorbate but in the latter one without any hydration sphere the molecule gets directly bound to the adsorbent.93,94 The contaminants that can be removed by biosorption could be organic and inorganic or soluble and insoluble. Metals (K+, Mg+) that are highly mobile and accordingly do not get accumulated with biomass during phytoremediation can be easily removed through biosorption.95 Heavy metals (lead, arsenic, cadmium, uranium, mercury) along with dyes, phenolic compounds and pesticides are receiving a lot of attention for their eradication through this process.96

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cannot be done efficiently from living biomass as metals bind intracellularly.98,100 Peptidoglycan carboxyl groups and phosphate groups provide the metal binding sites in gram-positive and gramnegative bacteria respectively.101 In addition, the proteinaceous S-layer and sheath also contribute to metal binding which are made up of proteins and polysaccharides. The metal binding component of many cyanobacterial cell walls contains peptidoglycan and some of them contain a sheath as well as extracellular polymeric substances.102 Pseudomurein is another cell wall component which resembles peptidoglycans present in archaea bacteria along with sulfonated polysaccharides and glycoproteins which provides the anionic sites (carboxyl and sulphate groups).103 Amongst all the components present in the algal cell wall, cellulose is common in all algal diversity which along with other components (depending on the presence) like polysaccharides (mannan, alginic acid, xylans) and proteins provides the binding sites (phosphate, sulphate, hydroxyl, amine groups) for metal attachment.104 Chitins, glucans, mannans and proteins are the components of fungal cell walls. Apart from these it also contains other polysaccharides, lipids and pigments (melanin) which facilitate binding of many metal ions.105 An important structural component of the fungal cell wall is chitin which is cheaper as compared to activated carbon and acts as an efficient biosorbent for metals as well as radionuclides.106 Like chitin, chitosan (derived from deacetylation of chitin) and other derivatives of chitin also have effective biosorption capacity.107 Carboxyl, phenolic, hydroxyl, carbonyl and methoxyl groups are

Types of biosorbent Primarily biosorbents fall into the following categories: living biomass and non-living biomass. Living biomass includes bacteria (gram-positive bacteria, gram-negative bacteria and cyanobacteria), fungi (mould, mushroom and yeast), algae (micro-algae, macro-algae, brown seaweeds and red seaweeds). While non-living biomass includes industrial waste (fermentation wastes, food/beverages waste, activated sludges, anaerobic sludges), agricultural waste (fruit/vegetable waste, rice straws, wheat bran, soybean hull etc.), natural residues (plant residues, sawdust, tree bark, weeds etc.) and other biomaterials (chitosanbased materials, cellulose-based materials etc.).91,97 Many studies show that non-living biomass has gained more preference over living biomass for the biosorption process because it does not require any maintenance and nutrient supply.98 Moreover, the biomass can be easily obtained from industrial waste which adds the ease of availability and makes the process economic.99 Whereas, living biomass demands proper maintenance of healthy microbial culture coupled with sustained environmental conditions. Even by providing these conditions, recovery of heavy metals

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Mechanisms of biosorption can be categorised on the basis of cellular metabolism and location of biosorption. Further, cellular metabolism based biosorption is divided into metabolism-dependent and non-metabolism-dependent. Metabolism-dependent includes transport through cell membrane and precipitation. Non-metabolismdependent includes ion exchange, precipitation, complexation and surface adsorption. On the basis of location, biosorption is classified as extra cellular accumulation/precipitation, cell surface sorption/ precipitation, intracellular accumulation and further they are divided in the same fashion as metabolism-dependent and non-metabolismdependent processes.

Fig. 4

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important as they bind to the oxygen binding sites which are present in the phenolic polymers and melanins of the fungal cell wall.93 Due to the availability of fungal biomass and rapid growth rate these are receiving considerable attention as biosorbents among living cells. As discussed above, due to the abundance and lesser processing requirement, agricultural and industrial waste and their by-products are very economic and have received good acceptance. Adsorbents include leafs, bers, fruit peels, saw dust bark etc. from agricultural and forest industries has been used in removing metals from contaminated water. Due to their physico-chemical characteristics and their availability they can be used as adsorbents.108 Vargas et al. worked on waste fruit cortex for the removal of heavy metals from contaminated water. They checked the biosorption capacity of banana (Musa paradisiaca), lemon (Citrus limonum) and orange (Citrus sinensis) peel. They found that lemon and orange cortex showed good biosorption potential for lead and copper as compared to banana. In the case of cadmium, banana showed greater biosorption efficiency than lemon and orange. They also studied the relationship between particle size and surface area and found them to be inversely related to each other.109 In another investigation, Amaranthus hybridus stalk and Carica papaya were used for removal of Mn and Pb ions from wastewater. The study showed that among both substrates Mn had greater percentage removal than lead. The adsorptive capacity of Carica papaya in all cases was higher as compared to Amaranthus hybridus stalk.110 In a recent study, researchers worked on chitin and a-(1,3)-b-D-glucan (from industrial bio-waste exhausted from brewer's yeast) for the removal of heavy metals from acid mine drainage (Merladet and Faith open-cast mines). They found that the Faith mine drainage was contaminated with U, Al, Cu, Mn, etc. and the Merladet mine drainage with Al, Mn, Zn, and Cu. They reported that Saccharomyces cerevisiae L. acted as an efficient biosorbent which eliminated heavy metals from polluted water.111 Suryan et al. used paper mill waste for the removal of heavy metals (Pb, Cd, Ni and Cu) from aqueous solution. They found that adsorption process was affected by pH and adsorption rate in case of all metal ions was above 70% (pH 2 to5). They concluded that the paper mill waste did not require any pre-treatment and recommended this as an option for better utilization of waste.112

Biosorption mechanism(s) The mechanism of biosorption is a highly complex process owing to the complexity of the biological structures involved. Functional groups like carboxyl, phosphate, hydroxyl, amino, thiol etc. are present on the structure of biomass which interacts with different heavy metals with variable degree which may be affected by physico-chemical factors. There are number of factors on which the binding of sorbate and sorbent depends like number of binding site in the biosorbent, binding strength of pollutant and functional groups present on the biosorbent, availability and accessibility of sites. There are various criteria on the basis of which mechanisms of biosorption can be divided. This includes cell metabolism

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and the location of biosorption (Fig. 4). Cell metabolism mediated biosorption can further be divided into metabolismdependent and non-metabolism-dependent processes:113  Metabolism dependent: occurs only in viable cells and plays a vital role in the defence mechanism of microbes showing reaction with toxic metals. Metabolism-dependent biosorption may further be classied as: » Transport across cell membrane: microorganisms shares the same mechanism for transport of heavy metals across the membrane as well as transport of metabolic ions like sodium, magnesium etc.88 It has no association with metabolic activity and comprises two steps: 1. Metabolism-independent binding where the metals bind to the cell walls. 2. Metabolism-dependent intracellular uptake which includes transport of metal ions across the cell membrane. » Precipitation: metabolism-dependent precipitation is oen related to the microbe's defense mechanism where their reaction in the presence of toxic metals produces compounds favouring precipitation.114  Non-metabolism-dependent: involves the interaction between metal and functional groups present on the microbial surface. As already discussed, many functional groups (carboxyl, phosphate, sulphate etc.) are present on the microbial surface because the microbial cell wall is made up of polysaccharides, proteins and lipids. It can further be categorised as follows: » Physical adsorption: a physical phenomenon involving van der Waal's and electrostatic forces. Even dead biomasses of algae fungi and yeasts have shown adsorption of heavy metals like copper, uranium, cobalt, zinc and cadmium through electrostatic interactions.93 » Ion exchange: here, the polysaccharides of microbial cell walls act as counter ions and facilitate the exchange of bivalent metal ions. The marine algae alginates which occur as salts of Mg2+, K+, Na+, Ca2+ can adsorb heavy metals by exchange of counter ions like Co2+, Cu2+, Cd2+ and Zn2+.115 » Complexation: interaction of metals with active groups mediates their removal from solution via the formation of cell surface complexes. Organic acids produced by microbes also play an important role in chelating toxic metals by their solubilisation and leaching resulting in generation of metalloorganic molecules. Complexation and adsorption of metals is brought about by carboxyl groups in microbial polysaccharides and polymers.116 » Precipitation: metabolism-independent precipitation results from the metal and cell surface interaction which is a chemical phenomenon. The location-dependent biosorption can be categorised on the basis of location where removed metals from solution accumulate. It is of the following types:  Extracellular accumulation/precipitation.  Cell surface sorption/precipitation.  Intracellular accumulation. These can further be categorised in exactly the same fashion as that in the case of metabolism-dependent and independent biosorption.114

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Merits and demerits of biosorption Conventional methods like ion exchange, electrodialysis, reverse osmosis etc. are expensive and their efficiency of removing heavy metals is very low. For this reason, biosorption is receiving much attention because it shows many advantages over traditional methods stated as follows:88 3 It is cost effective, selective and shows efficient removal of metals even at low concentrations. 3 Unlike conventional methods it does not produce any toxic sludge during the removal process which presents the opportunity of metal recovery and recycling of biosorbent. 3 Low cost adsorbents like industrial solid waste, agricultural waste etc. have shown excellent heavy metal removal efficiency. 3 It has a great advantage of being used in situ without the need of any industrial process in integration with other ecofriendly systems. 3 With dead biomass, concerns related to toxicity, microbial constrains and media formulation is alleviated. The only disadvantage of using biosorbents is there is no control over the biological characteristic of the biosorbent and early saturation while performing experiments.

Recent developments in bioremediation Recently new strategies for the process of bioremediation have been uncovered. Scientists have shown the application of nanoparticles, non-living biomass and genetically modied plants for the removal of heavy metal toxicants from different sources. These approaches are credited with having quick and high bioremediation capacity. Use of nanoparticles Application of nanotechnology is widely being used for the development of resourceful, efficient and environment friendly nanomaterial systems in different spheres of biotechnology including bioremediation. The physiochemical properties of the nanoscale particles vary signicantly from their larger counterparts. This is due to the very high surface to volume ratio of the nanomaterials which provides them with high adsorption capacity. Moreover, they have low cost and augmented bioavailability which makes them excellent candidates for bioremediation.117 Lately, superparamagnetic iron oxide nanoparticles (SPION) have been used for the separation of contaminants from wastewater because of their ultrane structure and high competence. In this technique, the carriers contain a polymeric shell having functional groups and a magnetic core (FeO, Fe3O4 and Fe2O3) which provides a strong magnetic response.118 Shen et al., prepared and implemented Fe3O4 nanoparticles for the purication of wastewater contaminated with heavy metals (Cd2+, Cr6+, Cu2+ and Ni2+). The nanoparticles prepared were of different size and were prepared by co-precipitation and polyol method. They found that particles of 8 nm size were very effective for the recovery and removal of metals from

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wastewater. It was found that the adsorption capacity of Fe3O4 particles increased with decreasing the particle size or increasing the surface area. Furthermore, maximum adsorption was seen to occur at pH 4.0 under room temperature (20  C) and the adsorption capacity of nanoparticles was found to be as high as 35.46 mg g 1 (7 times higher than that of the coarse particles).119 In another nding, the bioaccumulation capacity of magnetic gel beads (prepared from Fe2O3 nanoparticle and gellan gum) as potent bioadsorbents was assessed. They concluded that the magnetic gel beads were effective for the removal of lead, manganese and chromium in the order of Pb2+ > Cr3+ > Mn2+. Additionally, it showed the high desorption capacity with sodium citrate which would prove be very economical.120 Bezbaruah et al., used calcium alginate beads for the entrapment of zero-valent iron nanoparticle (Feo) to remove the test contaminant present in ground water (nitrate). Zerovalent iron nanoparticles (nZVI) have been known to eradicate various groundwater contaminants like chlorinated compounds, pesticides and heavy metals. However, it suffers from higher mobility, agglomeration and settlement problems by non-target compounds. They found that the overall removal efficiency of entrapped nZVI towards contaminants was comparable to that of bare nZVI.121 Another investigation reported the formulation of magnetic chitosan nanoparticles by a one-step in situ co-precipitation method with an aim to examine the sorption property for removing Cu(II) from aqueous solution. The process was found to be highly competent and the maximum sorption capacity was calculated to be 35.5 mg g 1.122

Use of non-living biomass Another favorable strategy that is used extensively for bioremediation includes use of living microorganisms such as bacteria, fungi, algae etc. They provide a large surface area to volume ratio because of the smaller size of microorganisms. However, they suffer from several disadvantages such as causing redox reactions between cell and medium which leads to an increase in pH of the system. Also, this method increases the biological oxygen demand and chemical oxygen demand as it requires nutrient uptake.123 In contrast to this, the application of dead biomass can be regarded as a suitable and favorable alternative. Dead biomass does not require growth media or nutrients and does not cause toxicity during the metal removal process. Besides, this method is very economical in comparison to living biomass.124 A recent investigation showed the biosorption capability of nonliving biomass of marine macrophytes for arsenic removal. Different phyla of alga were used to check their capability under different pH conditions. Considerable adsorption was exhibited by all the species. The highest observed value was by red alga Ceramium (1.3  0.1 mg g 1) and seagrass Zostera, comparable to other low-cost adsorbents like activated carbon. It was also observed that there were many factors on which biosorption rested like composition and structure of outer layer of macrophytes, availability of functional groups present on arsenic, different pH levels and counter ionic interaction with arseniate.125 Ekmekyapar et al., studied the biosorption capacity of

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Cladonia rangiformis (a non-living lichen) for the removal of lead from aqueous solution. They found that the non-living lichen is a natural biomass, harmless and easily available and exhibited a high accumulation capacity towards lead which can be exploited for the treatment of industrial effluents.126 Mohamad et al., reported the capability of dead cells of Mesorhizobium amorphae to act as a robust biosorbent for the removal of Cu2+ from aqueous solutions.123 Biosorption capacity of non-living biomass of Spirulina sp. for the removal of lead and zinc was also reported in a work carried out by Goyal et al.127 Use of genetically modied plants (GMP) The main aim of genetic engineering in the eld of phytoremediation is to enhance the capacity of plants to tolerate, accumulate and absorb contaminants. Many genes from different organisms have been identied and characterized that are involved in acquisition, allocation and decontamination of metals. The recombinant proteins produced by these transgenic plants play an important role in chelation (e.g. citrate, phytochelatins, metallothioneins, phytosiderophores and ferritin), assimilation and membrane transport of metals.128 Recently transgenic Arabidopsis thaliana was developed to increase the tolerance and accumulation of arsenic and cadmium by simultaneous over-expression of AsPCS1 and YCF1 genes. These genes are derived from garlic and baker's yeast. This work was based on chelation of metals and vacuolar compartmentalization which are the main strategies for heavy metals/metalloids detoxication. It was found that the two genes simultaneously increased the accumulation capacity as compared to use of a single gene.129 Zhang et al., carried out a study on a transgenic alfalfa plant with a motive to enhance its resistance capability towards the heavy metals and organic pollutants. This transgenic plant expressed both human CYP2E1 and glutathione S-transferase which were produced from hypocotyl segments by the use of Agrobacterium-mediated transformation. They found that the transgenic alfalfa plant which expressed both genes simultaneously had a remarkable potential to remove mixed contaminants as compared to the wild type and transgenic plant expressing the single gene.130 Another GMP, Nicotiana tabacum carrying a yeast metallothionein gene was shown to accumulate cadmium in the root of the transgenic plant.131

Conclusion Levels of heavy metals are increasing day by day due to increased industrial usage causing their accumulation in living beings. Their exposure can cause fatal consequences to organ systems through several mechanisms (primarily due to generation of oxidative stress). Oxidative stress leads to the production of free radicals followed by the decrease in the level of antioxidants and nally leading to cell death. Presently, conventional remediation methods like ion exchange, chemical precipitation, reverse osmosis, landlling and bio-piles are used for the removal of heavy metal contaminants. Although they have several advantages like ease of metal

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recovery, pure effluent production and high productivity, they have severe disadvantages which includes their high cost, production of toxic sludge and incomplete removal of metals. So, as a potential alternative to these methods, bioremediation is a promising upcoming technology which uses plants, microbes and their enzymes for the removal of heavy metals in an eco-friendly manner. Bioremediation involves two approaches i.e. phytoremediation and biosorption. Phytoremediation makes use of plants which have the capability to accumulate, degrade and/or volatilize the heavy metals, hydrocarbons and organic solvents leading to improvement in the quality of soil and water. Depending upon the conditions for e.g. on the basis of the site (soil or water) and property of contaminants (organic or inorganic), phytoremediating plants implement different mechanisms which include phytoextraction, phytoltration, phytostabilization, phytovolatilization and phytodegradation. Another mode of bioremediation exists called biosorption which uses low cost adsorbents like industrial waste, agricultural waste, microbial biomass and their derivatives for the treatment of aqueous waste. Different mechanisms are used by the adsorbent on the basis of location of biosorption and cellular metabolism. Further, they are divided into ion exchange, precipitation, complexation and physical adsorption. The heavy metal adsorption depends upon the type of adsorbent used, surface area, particle size, shape of the adsorbent and experimental conditions. Biosorption is a promising approach and is not only cost effective but also shows selectivity and high efficiency towards the removal of heavy metals. Moreover, it does not produce any toxic sludge. The latest addition to this technology is the application of nanoparticles, non-living biomass and transgenic crops. These novel approaches carrying out bioremediation have given highly encouraging results and in addition of being efficient they are also economical and give rapid results. Thus, bioremediation has bright prospects for the abolition of heavy metals from polluted sites. Also, its applicability could be further enhanced by identifying and implementing more novel plants and biosorbents that can offer better scope for heavy metal removal without the need for any substrate modication. Consequently, the processing cost for modication of adsorbents could be saved. Conclusively, it can be said that the bioremediation technology has given us a platform that could direct us towards the elimination of heavy metal pollution in an eco-friendly manner.

Competing interest The authors declare that they have no conict of interest.

Abbreviations ROS BBB EDTA

Reactive Oxygen Species Blood Brain Barrier Ethylenediaminetetraacetic acid

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CaNa2EDTA Calcium disodium ethylenediaminetetraacetic acid DPA D-Penicillamine BAL Dimercaprol NTA Nitrilotriacetic acid Chl Chlorophyll KH Henry constant Kd Partitioning coefficient.

Acknowledgements I heartily acknowledge Ms. Batul Diwan (School of Biotechnology, Rajiv Gandhi Proudyogiki Vishwavidyalaya, Bhopal, India) who played a major role in correcting and editing of the manuscript.

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Environ. Sci.: Processes Impacts, 2014, 16, 180–193 | 193

A review with recent advancements on bioremediation-based abolition of heavy metals.

There has been a significant rise in the levels of heavy metals (Pb, As, Hg and Cd) due to their increased industrial usage causing a severe concern t...
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