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Journal of Environmental Management 134 (2014) 175e185

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Journal of Environmental Management

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Review

Review of remediation techniques for arsenic (As) contamination:A novel approach utilizing bio-organisms

Shahedur Rahman a, Ki-Hyun Kimb,*, Subbroto Kumar Saha c, A.M. Swaraz a,Dipak Kumar Paul d

aDepartment of Genetic Engineering and Biotechnology, Jessore University of Science and Technology, Jessore 7408, BangladeshbDepartment of Civil & Environmental Engineering, Hanyang University, 222 Wangsimni-Ro, Seoul 133-791, Republic of KoreacDepartment of Animal Biotechnology, Konkuk University, Seoul, Republic of KoreadDepartment of Applied Nutrition and Food Technology, Islamic University, Kushtia 7003, Bangladesh

a r t i c l e i n f o

Article history:Received 16 October 2013Received in revised form24 December 2013Accepted 27 December 2013Available online 7 February 2014

Keywords:Arsenic (As)AccumulationBioremediationBio-organism

* Corresponding author. Previously at: Dept. of EnUniversity, Seoul, Republic of Korea. Tel.: þ82 70 756

E-mail address: kkim61@nate.com (K.-H. Kim).

0301-4797/$ e see front matter � 2014 Elsevier Ltd.http://dx.doi.org/10.1016/j.jenvman.2013.12.027

a b s t r a c t

Arsenic (As) contamination has recently become a worldwide problem, as it is found to be widespreadnot only in drinking water but also in various foodstuffs. Because of the high toxicity, As contaminationposes a serious risk to human health and ecological system. To cope with this problem, a great deal ofeffort have been made to account for the mechanisms of As mineral formation and accumulation bysome plants and aquatic organisms exposed to the high level of As. Hence, bio-remediation is nowconsidered an effective and potent approach to breakdown As contamination. In this review, we provideup-to-date knowledge on how biological tools (such as plants for phytoremediation and to some extentmicroorganisms) can be used to help resolve the effects of As problems on the Earth’s environment.

� 2014 Elsevier Ltd. All rights reserved.

1. Introduction

Arsenic (As) is known to exert mutagenic, cytotoxic and geno-toxic effects with an increased risk of cancers on skin, kidney, lung,and bladder (Liu et al., 2011). As a class one carcinogen, As isdistributed ubiquitously in the environment (Zhao et al., 2010;Duan et al., 2012). At present, As is estimated to affect more than150 million people worldwide with its increasingly elevated con-centrations in drinkingwater (Stroud et al., 2011). For instance, overthe past 2-3 decades, Bangladesh and the neighboringWest Bengal,India, have suffered from widespread contamination of As in thedrinking water extracted from shallow tube-wells (STW). Morethan half of those wells were seen to contain >10 mg L�1 As, knownas the guideline value of drinking water set by the World HealthOrganization (WHO) (Khan et al., 2010).

In light of the current status of As pollution, its dietary intake isproblematic due to the high potential for bio-accumulation (Zhaoet al., 2010). Because As can be involved in diverse disease pro-cesses through interfering with or altering many different mecha-nisms (e.g., cell signaling, cell cycle control, oxidative stress, DNA

vironment & Energy, Sejong0 9151.

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repair, etc) (Liu et al., 2001), its poisoning poses a growing globalhealth risk (Tripathi et al., 2008). In general, the inorganic forms ofAs (such as trivalent arsenite (As(III)) and pentavalent arsenate(As(V)) are more prevalent and toxic than the organic forms interrestrial environments. As(III) has an affinity for sulfhydrylgroups existing in cysteine residues to exert detrimental effects ongeneral protein metabolism with high toxicity (Rai et al., 2011). Assuch, it can act as an endocrine disruptor at very low, environ-mentally relevant concentrations (Kaltreider et al., 2001). Arsenite-stimulated generation of reactive oxygen species (ROS) was provento damage proteins, lipids, and DNA. As(V) is a phosphate analoguecapable of being incorporated into ATP through the replacement ofphosphate at binding sites (Ali et al., 2012). Such substitutionsaccompanied by inhibition of oxidative phosphorylation can add tothe toxicity of As(V). In aerobic soils, arsenate (As(V)) is the moststable form of As, which interferes with essential cellular processesas an analogue of phosphate such as oxidative phosphorylation andATP biosynthesis.

Human intervention has been an important contributor to themobilization of As, e.g., through the mining of mineral resources,combustion of fossil fuels, and use of arsenical pesticides, herbi-cides, and additives (to livestock feed for poultry). Such significantcontamination of As tends to be observed with its concentrationsexceeding 1000 mg L�1 from various places throughout the world

Table 1Status of As contamination in natural groundwater and soil systems in various countries.

Order Country Region Soil Asconcentration

GroundwaterAs level (ppb)

Provisionalguideline value forAs concentrationin drinking water(ppb)

Reference

1 Afghanistan Ghazni(Metropolitan area)

e 10e500 10 (WHO) Mukherjee et al. (2006);Nriagu et al. (2007)

2 Argentina Encon and SanJosé de Jáchal

e 9e357 10 (WHO) Barringer (2013); Nriagu et al. (2007); O’Reillyet al. (2010)

La Pampa e 3e13263 Australia Victoria

(Around thegold-mining regions)

e 1e12(Groundwater)

10 (WHO) Mukherjee et al. (2006); Nordstrom (2002 );Nriagu et al. (2007)

1e73(Drinking-water)1-220(Surface water)

4 Bangladesh Noakhali 3.6e26 mg/kg(Meghna River)

<1e4730 50 (WHO) Gunduz et al. (2010); Nordstrom (2002 );Nriagu et al. (2007); Smedley and Kinniburgh(2002); Chakraborti et al. (2010)

5 Belgium Zenne River e Up to 30 10 (WHO) Brunt et al. (2004); Nriagu et al. (2007)6 Brazil Minas Gerais

(Southeast-ern Brazil)200e860 mg/kg 0.4e350

(Surface water)10 (WHO) Bundschuh et al. (2012); Mukherjee et al.

(2006); Nordstrom (2002)7 Cambodia Prey Veng and Kandal e Up to 900 10 (WHO) Nriagu et al. (2007); Sthiannopkao et al. (2008)

Mekong delta 1e16108 Canada Nova Sco-tia

(Halifax county)e 1.5 to 738.8 10 (WHO) Mukherjee et al. (2006); Nriagu et al. (2007)

9 Chile Esquiña Up to 489 mg/kg(Río Caritaya region)

12.2e74.0 10 (WHO) Brunt et al. (2004); Bundschuh et al. (2012);Nriagu et al. (2007)

10 China e <50e4440 50 Rahman et al. (2009)11 Finland Southwest Finland e 17e980 10 (WHO) Bundschuh et al. (2012); Mukherjee et al.

(2006); Nordstrom (2002)<0.05e6412 Germany Northern Bavaria e <10e150 10 (WHO) Nordstrom (2002 ); Nriagu et al. (2007);

Smedley and Kinniburgh (2002)13 Ghana Obuasi

(Gold-mining area)e <1e175 10 (WHO) Nordstrom (2002 ); Nriagu et al. (2007)

14 Greece Fairbanks(Mine tailings)

e Up to 10,000 10 (WHO) Nriagu et al. (2007); Smedley and Kinniburgh(2002)

15 Hungary Danube Basin e <2e176 10 (WHO) Nriagu et al. (2007);Smedley and Kinniburgh(2002)

16 India 16e417 mg/kg(Central India)

10e3200 50 (WHO) Das et al. (2013); Nordstrom (2002 ); Nriagu etal. (2007); Smedley and Kinniburgh (2002);Srivastava and Sharma (2013)Uttar Pradesh 5.40e15.43 ppm

(Uttar Pradesh)43.75e620.75

17 Iran Kurdistan e Up to 290 10 (WHO) Mukherjee et al. (2006); Nordstrom (2002 )18 Japan Fukuoka prefecture

(Southern region)e 1e293 10 (WHO) Mukherjee et al. (2006); Nordstrom (2002)

19 Laos e e <0.5e278 50 Chanpiwat et al. (2011); Nriagu et al. (2007)20 Mexico Lagunera 2215e2675 mg/g

(Highly polluted area)8e620 25 Nordstrom (2002 ); Nriagu et al. (2007);

Smedley and Kinniburgh (2002)21 Mongolia Hetao Basin e 0.6-572 10 (WHO) Khan and Ho (2011)22 Nepal Rupandehi e Up to 2620 50 Halsey (2000); Nriagu et al. (2007); Rahman et

al. (2009)23 Pakistan Muzaffar-garh

(South western Punjab)e 50-250 50 Khan and Ho (2011); Mukherjee et al. (2006);

Nordstrom (2002)Up to 90624 Poland Lower Silesia,

(Southwestern Poland)Up to 18100 mg/kg(Highly polluted area)

10 (WHO) Karczewska et al. (2007)

25 Romania Transylvania(Northwestern parts)

e <2e176 10 (WHO) Brunt et al. (2004); Mukherjee et al. (2006);Nriagu et al. (2007)

26 Spain Duero Cenozoic Basin 23 mg/kg (Mean) 40.8 (Mean) 10 (WHO) Gómez et al. (2006)27 Switzerland Jura mountains and Alps e Up to 170 50 Mukherjee et al. (2006); Nordstrom (2002)28 Taiwan e e 10e1820 10 (WHO) Nordstrom (2002 ); Nriagu et al. (2007);

Smedley and Kinniburgh (2002)29 Thailand Ron Phibun - 1- >5000 10 (WHO) Nordstrom (2002 ); Nriagu et al. (2007);

Smedley and Kinniburgh (2002)30 Turkey Simav plain (Kutahya) Up to 660 mg/kg

(Highly polluted area)Up to 561.5(Average 99.1)

10 (WHO) Gunduz et al. (2010)

31 UnitedKingdom

Cornwall 2e17 mg/kg(Bioaccessible)

11e80 20 Mukherjee et al. (2006); Nordstrom (2002 );Palumbo-Roe et al. (2005)

32 USA Tulare Lake Average 280 mg/kg(Hawaii)

Up to 2600 10 (USEPA) Brunt et al. (2004); Cutler et al. (2013); Nriaguet al. (2007); Twarakavi and Kaluarachchi(2006); Welch et al. (2000)

33 Vietnam Red River delta(Northern Vietnam)

e <1e3050 10 (WHO) (2002); Nriagu et al. (2007); Rahman et al.(2009); Smedley and Kinniburgh (2002)

Mekong delta(Southern Vietnam)

1e845

S. Rahman et al. / Journal of Environmental Management 134 (2014) 175e185176

S. Rahman et al. / Journal of Environmental Management 134 (2014) 175e185 177

(Table 1); this level is far beyond the guideline of WHO (e.g.,10 mg L�1) (Tuli et al., 2010). In addition, the irrigation of agriculturalsoils with As-contaminated groundwater (e.g., in many South-EastAsian countries) must have contributed greatly to the accumulationof As in both soils and plants. The transfer of As to the food chainwill ultimately remain as long-term risks to human and ecologicalsystems (Tuli et al., 2010). Therefore, attention needs to be drawn tounderstand the environmental fate and toxicity of As to organisms.

In this review, a solution is sought to help relieve the problem ofAs pollution based on a comprehensive survey of both recent andprevious efforts directed to the remediation or prevention of Aspollution (Srivastava et al., 2011). In addition, we will discuss hownatural plants respond to As toxicity, types of bio-organism natu-rally tolerant to As toxicity, and their detoxification mechanism.Our discussion is extended further to suggest the scope in whichfuture work should be directed to help remove As in a more effi-cient way with the aid of biological means.

2. Survey of As pollution status

Because As in groundwater and aquifers is mobilized (e.g., hy-draulic fracturing), its contamination can be propagated defectivelyinto the groundwater system (Murcott, 2012). Hence, its contami-nation can influence a large population of people. In fact, more than137 million people (70 countries) were estimated to suffer from Asintake via drinking water (Ravenscroft, 2007). In the case of soil,there are also numerous pathways to propagate the contaminationof As. Themajor sources of its contamination in soil are identified toinclude many man-made activities: the use of pesticide, mining,smelting, tanning, wood preservation, and solid waste (Davis et al.,2001).

The distribution of As in the water system is generally repre-sented as arsenite and arsenate, while it exists as metal oxides (Al,Fe, and Mn oxides) and short-range ordered aluminosilicates(allophane, ferrihydrite, and imogolite) in the soil system (Violanteet al., 2008). As summarized in Table 1, the concentrations of As insoil/water systems measured from various locations in the worldare summarized. It shows that provisional guideline values for Asconcentration in drinking water are commonly set at 10 ppb,although it can go up to 50 ppb. The results of this comparisonconfirm that As contamination is a widespread phenomenon andsevere enough to exceed such guideline values. In fact, peopledrinking As-rich water over long periods are reported to suffer fromsevere health problems in many countries in the world.

3. Natural plant response to As toxicity

If plants are exposed to an excess quantity of As either in soil orin hydroponic cultures, they can exhibit a multitude of symptomssuch as (a) inhibition of seed germination and seedling growth, (b)decreases in shoot growth, plant height, chlorophyll content, andtillering, (c) reductions in leaf area and photosynthesis, and (d)lower yields of fruit and grain (Liu et al., 2012). Because As inducesthe formation of ROS, it can disturb the redox state and affect theenergy homeostasis of plants (Srivastava et al., 2011). The produc-tion of ROS results from either one of two pathway types (Foyer andNoctor, 2005): (1) the formation of singlet oxygen through theexcitation of O2 and (2) the formation of superoxide radical (O2�),hydrogen peroxide (H2O2), and hydroxyl radical (HO�) through thetransfer of one, two, and three electrons to O2, respectively. Anincrease in ROS production leads to oxidative stress due to thecombined effects of membrane lipid peroxidation, protein oxida-tion, and DNA damage (Rai et al., 2011; Srivastava et al., 2011).

If As enters a plant body, plant modulates a number of pathwaysto handle As stress (Mishra et al., 2008b). This modulation proceeds

to control the cellular concentration of free metalloid ion to aminimum level (primary detoxification, e.g., thiol mediatedcomplexation (Bleeker et al., 2006)) and to reduce damage causedby free ions (Srivastava et al., 2007). Abercrombie et al. (2008)demonstrated that As(V) exposure should repress the genesinduced by phosphate starvation due to its role as a chemicalanalogue of phosphate. These authors thus concluded that plantshave evolved an As(V)-sensing system that acts against thephosphate-sensing mechanism (Abercrombie et al., 2008). Plantsrespond to oxidative stress by increasing either the production oflow-molecular-weight antioxidants (glutathione (GSH) and ascor-bate (ASC)) or the activity of antioxidant enzymes (superoxidedismutase (SOD), ascorbate peroxidase (APX), and catalase (CAT)).There are other metabolites (i.e., proline and phenolics) with thepotential of the antioxidant function. GSH is also known to play acentral role in As detoxification inside the plants through chelationeither by itself or in the form of its polymers, phytochelatins(Hossain et al., 2012).

4. Types of bio-organisms for As treatment

4.1. Prokaryotes

Among diverse microorganisms capable of developing diversemachineries for detoxification, there is a prokaryotic single-celledorganism in which DNA is not contained in a nucleus (bacteriumor archaean) (Taggart and Starr, 2009). Microorganisms havedeveloped a number of strategies to counteract As toxicity: (a)active extrusion (of As); (b) intracellular chelation (in eukaryotes)by various metal-binding peptides; and (c) transformation intoorganic forms with reduced toxicity and compartmentalization(Tsai et al., 2009).

Evolution of many specific As uptake transporters is yet sug-gested to be insufficient due to the extreme toxicity of As (Stolzet al., 2006). However, because As could potentially act as anelectron donor or acceptor, it can be an active component of theelectron transport chain in some bacteria (Tsai et al., 2009). AsAs(III) and As(V) share the similar structures, they tend to be takenup using the glycerol and phosphate transporter, respectively(Rosen and Liu, 2009). Identification of GlpF homologs as a memberof glycerol channels was already made in Leishmania major(Gourbal et al., 2004) or Pseudomonas putida; all of them are ex-pected to facilitate the transport of As(III) across their cell mem-branes (Tsai et al., 2009).

Based on phylogenetic analyses made by a highly conservedgenetic marker (the 16S rRNA gene), Héry et al. (2008) suggestedthe possibility that the Sulfurospirillum and Geobacter speciesshould be involved in arsenate respiration under anaerobic condi-tions to convert As(V) to As(III). If mobilized, it can either beextruded via an arsenite carrier protein or via an arsenite effluxpump ArsB which is affected by membrane potential for energy orthe energy provided by the ATPase ArsA via ATP hydrolysis (Deyet al., 1996). Likewise, the majority of prokaryote systems areknown to employ the ArsA/B system. Because the affinity for As(III)is reduced via cysteine residue mutations, the activation of ArsA byAs(III) is suspected to proceed via metal-thiolate complex formedamong the three cysteine residues and As(III) (Silver and Phung,2005).

4.2. Eukaryotes

The cellular structure of Eukaryotes is explained by a nucleusand other membrane-enclosed organelles (protist, plant, fungus, oranimal) (Taggart and Starr, 2009). Once As enters the cells, a seriesof detoxification steps can proceed to reduce the acute cytotoxic

Table 2List of As tolerant organisms occurring naturally.

Order Organisms Proteins, genes or pathways involvein tolerance mechanism

References

A. Prokaryotesi. Bacteria

1 Leishmania major GlpF homologs Gourbal et al. (2004)2 Pseudomonas putida GlpF homologs Tsai et al. (2009)3 Shewanella sp. strain ANA-3 Respiratory arsenate reductase activity Páez-Espino et al. (2009)4 Sulfurospirillum barnesii Respiratory arsenate reductase activity Páez-Espino et al. (2009)5 Desulfosporosinus sp. strain Y5 Respiratory arsenate reductase activity Páez-Espino et al. (2009)6 Wollinella succinogenes Respiratory arsenate reductase activity Páez-Espino et al. (2009)7 Alkaliphilus metalliredigens Respiratory arsenate reductase activity Páez-Espino et al. (2009)8 Clostridium sp. strain OhILAs Respiratory arsenate reductase activity Páez-Espino et al. (2009)9 Alkaliphilus oremlandii Respiratory arsenate reductase activity Páez-Espino et al. (2009)10 Sulfurospirillum barnessi Respiratory arsenate reductase activity Páez-Espino et al. (2009)11 S. arsenophilum Respiratory arsenate reductase activity Páez-Espino et al. (2009)12 Desulfotomaculum auripigmentum Respiratory arsenate reductase activity Páez-Espino et al. (2009)13 Herminiimonas arsenicoxydans (Aerobic condition) As(lll) oxidase Duquesne et al. (2008); Richey et al. (2009)14 Thiomonas spp. (Aerobic condition) As(lll) oxidase Duquesne et al. (2008); Richey et al. (2009)15 Rhizobium sp. strain NT26 (Aerobic condition) As(lll) oxidase Duquesne et al. (2008); Richey et al. (2009)16 Alkalilimnicola ehrlichii (Anaerobic condition) As(lll) oxidase Duquesne et al. (2008); Richey et al. (2009)17 Staphylococcus sp. NBRIEAG-8 Volatilization Srivastava et al. (2012)

ii. Rhizobacteria18 Bacillus Arsenate reductase homologs

(ArsC, ArsB and ACR3)Cavalca et al. (2010)

19 Achromobacter Arsenate reductase homologs Cavalca et al. (2010)20 Brevundimonas Arsenate reductase homologs Cavalca et al. (2010)21 Microbacterium Arsenate reductase homologs Cavalca et al. (2010)22 Ochrobactrum Arsenate reductase homologs Cavalca et al. (2010)23 Ancylobacter dichloromethanicum strain As3-1b Arsenate reductase Cavalca et al. (2010)

B. Eukaryotesi. Yeast

24 Saccharomyces cerevisiae ARR1, ARR2, ARR3 Mukhopadhyay et al. (2000)25 S. pombe Arr2p (arsenate reductase) Mukhopadhyay et al. (2000)

ii. Plant26 Arabidopsis AtAsr/AtACR2 (Arsenate reductase) Bleeker et al. (2006)27 Holcus HlAsr (Arsenate reductase) Dhankher et al. (2006)28 Pteris PvACR2 (Arsenate reductase) Ellis et al. (2006)29 Leguminous plants GSH, PCs, hPCs Grill et al. (2007); Li et al. (2005)30 Hydrilla verticillata Thiol metabolites Tuli et al. (2010)

S. Rahman et al. / Journal of Environmental Management 134 (2014) 175e185178

effects. Three contiguous gene clusters (ARR1, ARR2, and ARR3) areknown to have themost comprehensive mechanism of As tolerancein yeast. On the other hand, themain route of As(V) uptake in plantsproceeds through the phosphate transporters as a phosphateanalogue, whereas As(III) is transported in the neutral As(OH)3form through aquaglyceroporins (Meharg and Jardine, 2003). Incase of rice, the silicon transporter Lsi1 (OsNIP2;1) is amajor uptakepathway for As(III) (Ma et al., 2008).

By modifying the genes responsible for the As(III) uptake sys-tem, genetic engineering may be applied to alter the mitigationtrend of As contained inwaters and soils. Restricting the influx of Asmight be an important mechanism to avoid toxicity. In fact, severalmetallicolous plants, such as Holcus lanatus and Cytisus striatus, arereported to improve As tolerance by the constitutive suppression ofhigh-affinity phosphate/As(V) transport (Bleeker et al., 2003). Theenzyme arsenate reductase (AR) which includes Arabidopsis(AtAsr/AtACR2), Holcus (HlAsr), and Pteris (PvACR2) can processdetoxification through the reduction of As(V) to As(III) (Bleekeret al., 2006; Ellis et al., 2006). Hence, the plant’s tolerance to Ascan be expanded by stimulating the AR activity in plants (such asHolcus lanatus) (Bleeker et al., 2006; Grill et al., 2007). As shown inTable 2, Leguminous plants are reported to synthesize homo-PCs(hPCs) under As stress (Grill et al., 2007). Many studies havealready pointed the pivotal role of these compounds to overcomeAs toxicity (Li et al., 2005). Various studies on sporophytes of Pterisvittata have also shown that As is translocated to the shoot mainly

as As(V) stored in the fronds as inorganic As(III) (Pickering et al.,2006). In contrast, Duan et al. (2005) found AR activity exclu-sively in the roots of P. vittata and concluded that As should betranslocated mainly in its reduced form. A final step in detoxifica-tion is thus likely to involve As sequestration in the vacuoles of rootand shoot tissue (Tripathi et al., 2007).

The possibly important role of maize as a phytoremediator ofsoil As has been proposed (Ding et al., 2011; Liu et al., 2012). In fact,As concentrations in the four different tissues were found in theorder of leaves > stems > bracts > kernels (Liu et al., 2012). Hence,the As accumulation in different tissues in maize is likely controlledby different molecular mechanisms. The quantitative trait loci(QTLs) will be useful for selecting inbred lines and hybrids thatcontain low As in their kernels. Even if As is present uniformly insoil, total As levels can vary greatly in grains of different genotypes(Liu et al., 2006). The uptake and speciation of As in rice is thusaffected sensitively by differences in both environmental and ge-notype conditions (Norton et al., 2009).

4.3. Engineered microbes

The development of genetically engineered (GE) bacteria is onepractical option for bioremediation, as the toxic form of As can beconverted into a non-toxic form via enzyme-mediated redox re-actions (Singh et al., 2011). GE microbes can also be used symbi-otically with genetically engineered plants or naturally occurring

S. Rahman et al. / Journal of Environmental Management 134 (2014) 175e185 179

As tolerant plants to synergistically remove As or its toxic effectssuch as Escherichia coli strain expressing the As specific Fucus ves-iculosus metallothionein (fMT) and an As transporter GlpF (Singhet al., 2010). Increases in PC production can be induced further bythe co-expression of a feedback desensitized g-glutamyl cysteinesynthetase (GshI) or an As transporter GlpF (Table 3). A combina-tion of these engineering steps with an As efflux deletion E. colistrain or by creating recombinant E. coli expressing the human MT(hMT-1A) gene improved bioaccumulation of heavy metals (Maet al., 2011; Singh et al., 2008). There was also an effort to fuseglutathione S-transferase (GST) gene with the human MT to up-grade the protein stability (Huang et al., 2009). To increase MTexpression efficiency and metal binding capacity, outstanding re-sults were obtained from the recombinant E. coli integrated withmultiple hMT-1A genes in a series (Huang et al., 2009).

A number of expressing metal-binding peptides (such as humanMTs) have been reported in engineering microbes for the removalof cadmium (or mercury). However, they are yet not effectiveenough for As due to their relatively low specificity and/or affinity(Tsai et al., 2009). The metalo-regulatory protein (ArsR) nonethe-less offers immense potential of bioremediation of As by GE bac-teria, e.g., high affinity and selectivity. Kostal et al. (2004) reportedthat over-expression of ArsR genes in E. coli could increase thebioaccumulation of metallic As. Thus, such application in geneticmanipulated bacteria can effectively promote the cellular accu-mulation of As through provision of a highly selective As bindingligand; this will in turn greatly facilitate the selective removal of Asby bacteria (Singh et al., 2011).

4.4. Aquatic macrophytes

It is reported that submerged plants have fairly enhancedaccumulation capacity of As than emergent and terrestrial plants(Bergqvist and Greger, 2012). It is also noted that the As accumu-lation in plants is greatly reflected by the habitat properties (typesand density) and the soil content of As. In light of these factors, thepossibility of submerged plants and/or gymnosperms as the tool forphytoremediation of As has been intensively studied in recentyears. Some marine algae exhibited a high capacity for biosorptionand bioconcentration of metals and metalloids and have therefore

Table 3Engineered organisms with enhanced arsenic tolerance and remediation capacity.

Order Organisms Modifications Foldincrease

References

A. Prokaryotes1 E. coli Mutation in GlpF 10 Tsai et al. (2009)2 E. coli Expression of

fMT and GlpF26e30 Singh et al. (2008)

3 E. coli(As effluxabsent)

Expression ofSpPCS, GshI, GlpF

80 Singh et al. (2010)

4 E. coli Expressing the GSTfused trimeric hMT-1A

3 Ma et al. (2011);Singh et al. (2008)

5 E. coli ArsR over expression 60 Kostal et al. (2004)6 E. coli arsM (Coloned from

R. palustris)e Yuan et al. (2008)

7 Sphingomonasdesiccabilis

arsM (Coloned fromR. palustris)

10 Liu et al. (2011)

8 Bacillusidriensis

arsM (Coloned fromR. palustris)

10 Liu et al. (2011)

B. Eukaryotes9 Arabidopsis

thalianaExpression of theGSH1 gene

�10 Guo et al. (2008)

10 A. thaliana Over expressionof g-ECS

2e5 Li et al. (2006b);Li et al. (2005)

11 S. cerevisiae Over expressionof Arr3p

4 Bobrowicz et al. (1997)

been proposed as phytoremediation media in polluted aquaticsystems. Several aquatic macrophytes capable of hyper-accumulating As have thus been recommended in the treatment ofAs contaminated waters (Rubio et al., 2010). Marine macrophytesare thus considered potent option for the remediation of As-contaminated aquatic systems. In fact, some species of aquaticmacrophytes have already been demonstrated to accumulate aformidable amount of As fromwater (Mishra et al., 2008a; Tripathiet al., 2008; Zhang et al., 2008). Among the many species of theLemnaceae family, Lemna gibba L. and L. minor L. are the onesinvestigated most intensively in phytoremediation and ecotoxi-cology (Mkandawire and Dudel, 2007). Certain other aquaticmacrophyte candidates for phytoremediation are listed in Table 1Sin Supplementary Material. Because some trees and shrubs showlow As accumulation, they are thus of interest with respect tophytoextraction with the relatively high biomass production andeasily harvestable plant parts (Bergqvist and Greger, 2012).

In addition to macrophytes, Srivastava et al. (2011) identifiedother plants like Portulaca tuberose, Portulaca oleracea, Eclipta alba,Limnanthes spp. and Lemna gibba as the potent As-accumulators.They investigated the As removal efficiency of Hydrill averticillatafrom simulated As contaminated water in field conditions (Tuliet al., 2010). They observed significant As accumulation (72% oftotal As supplied) but with little toxic effects in terms of the level ofhydrogen peroxide and lipid peroxidation. It can be accounted forby the enhanced level of thiol metabolites (cysteine and gluta-thione) and enzymatic antioxidants (guaiacol peroxidase, catalase,and ascorbate peroxidase) (Srivastava et al., 2011). King et al. (2008)reported Eucalyptus cladocalyx, in particular as an ideal candidatefor the extended phytostabilization, e.g., mine tailings. Tripathiet al. (2012a) suggested the promising roles of one fern species(Marsilea) and some aquatic plants (Eichhornia crassipes andCyperus difformis) to treat As contaminated paddy fields.

The uptake of As species in aquatic macrophytes has been pro-posed to be regulated by the following three mechanisms (Rahmanand Hasegawa, 2011): (a) active uptake (with the help of phosphatetransporters), (b) passive uptake (with the help of aqua-glyceroporins), and (c) physicochemical adsorption (in root). Plantsmainly uptake As (V) through a phosphate uptake transporter(Wang et al., 2011; Zhao et al., 2009). Physicochemical adsorptionon root surfaces is also proposed as an alternative uptake pathwayfor the As species (Rahman et al., 2008). In the case of As(III), plantuptake proceeds in the form of dimethylarsinic acid (DMAA) andmonomethylarsonic acid (MMAA) via a passive mechanismthrough the aquaglyceroporin channels (Rahman and Hasegawa,2011; Zhao et al., 2009). It may be also possible to infer that As(V)should be predominantly adsorbed on precipitated iron oxides onthe roots of aquatic plants for further accumulation (Rahman et al.,2008).

Arsenic detoxification mechanisms in aquatic plants are ex-pected to be comparable to those of the terrestrial plants (Rahmanand Hasegawa, 2011). Following the uptake, As(V) is reduced effi-ciently to As(III) in plant cells. As speciation in plant tissues showsthat the As(III) oxidation state is prevalent, despite their commonexposure to As(V). Note that the former has high binding affinity tosulphhydryl (eSH) groups of peptides such as glutathione (GSH) andphytochelatins (PCs), whereas the latter does not (Zhao et al., 2009).The reduction of As(V) to As(III) can thus be mediated by GSH andenzymes as the part of plant’s detoxification mechanisms (Bleekeret al., 2006). Upon uptake, As(V) and As(III) have been reported toproduce reactive oxygen species (ROS) inside the plant cells (Mehargand Hartley-Whitaker, 2002). Plants are suspected to control theproduction of ROS by various enzymes and cellular compounds(Mittler, 2002). GSH can act as an antioxidant needed for the syn-thesis of metalloid chelating ligands (Srivastava et al., 2007). As(III)

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was also found to induce the activities of cysteine synthase and c-glutamyl cysteine synthetase (Srivastava et al., 2010).

The eventual fate of the plants loaded with a high quantity of Asis a vital issue in the phytoremediation. If the phytoremediatingplants are not disposed of properly, they will turn out to be anothersource of As contamination in the environment. To date, studiesabout the management skills needed to properly dispose phytor-emediating media are yet relatively insufficient. Rahman andHasegawa (2011) proposed a theory on the treatment of phytor-emediating plants, including the production of charcoal, liquid fuel(such as ethanol production through fermentation), briquettes, andbiogases. Nonetheless, all of these options have particular down-sides and risks.

5. As detoxification mechanism of bio-organisms

5.1. Enzyme-mediated redox reaction

Oxidization of As(III) is an important treatment technique for Asbecause As(V) is less soluble and can be removed much moreeffectively by physico-chemical methods (Leist et al., 2000). As(V)can either precipitate with iron [Fe(III)] or be removed viaadsorption on ferrihydrite. As the oxidation process may be medi-ated by microbial activities, it can contributes to the naturalremediation of As; such phenomena have been observed occa-sionally in some contaminated environments (Lièvremont et al.,2009; Oremland and Stolz, 2005; Sharma and Sohn, 2009). Totreat As from contaminated waters, researchers commonly reliedon the precipitation or adsorption of the As(V) produced by bacteria(Lièvremont et al., 2009). In the course of a detoxification process,As(III) can be oxidized to As(V) by different prokaryote types undereither aerobic (e.g., Herminiimonas arsenicoxydans, Thiomonas spp.,or Rhizobium sp. strain NT26) or anaerobic conditions (e.g., Alka-lilimnicola ehrlichii) (Richey et al., 2009).

In nature, microorganisms are capable of carrying out theoxidation of As(III) with the enzyme As(III) oxidase, a member ofthe DMSO reductase family (Ellis et al., 2001). Most arsenite oxi-dases work as a hetero-dimer by utilizing Fe andMo in the catalysis(Ellis et al., 2001). Likewise, bacteria carrying aox genes (e.g., Alpha-,Beta-, or Gamma-proteobacteria phylum) were identified from 25bacterial and archaeal genera isolated from many arsenic-rich en-vironments (Heinrich-Salmeron et al., 2011). Although the intra-cellular reduction of As(V) can proceed with the aid of the arsenatereductase, some bacteria (e.g., Shewanella sp. strain ANA-3) are alsocapable of reducing arsenate during the anaerobic respiration(Krafft and Macy, 1998). Note that a number of facultative aerobicgenera (e.g., Bacillus) have also been identified from some pyritecinder-polluted soils (Corsini et al., 2010). They generally containeda putative arsenate reductase and/or arsenite efflux pump, e.g., thepresence of ArsC and/or ArsB genes (Corsini et al., 2010). Somestrains showed the ability to reduce arsenate through an intracel-lular detoxification, while other strains were able to oxidize arse-nite; hence, bacteria may easily alter the oxidation state of soil As(Corsini et al., 2010).

Under the reducing conditions (e.g., flooded soils with readilyutilizable carbon sources), As can be mobilized by facultative aer-obic microbes (Corsini et al., 2010). As a candidate for GM bacteria,the existence of those facultative aerobic microbes can be a double-edged sword. Many microorganisms have developed diversemechanisms through which they can resist As. In the course of suchdevelopment, As is utilized as part of their ordinary physiology, e.g.,for respiration and as an electron donor (Silver and Phung, 2005).Apart from altering the redox state, some microbes can alsomethylate inorganic As species (Qin et al., 2006) or demethylate itsorganic counterparts (Silver and Phung, 2005). A number of

microbial isolates such as Ancylobacterdichl oromethanicum strainAs 3-1b were able to reduce arsenate to oxidize arsenite. Conse-quently, the oxidation of arsenite can also be observed in the strainunder chemoautotrophic conditions (Heinrich-Salmeron et al.,2011).

5.2. Biovolatilization

Biovolatilization of As is a natural bioremediation process bywhich As is removed from soil or water reservoirs (Jakob et al.,2010; Liu et al., 2011). The formation of volatile As is an enzy-matic process of organic and inorganic arsenicals through a com-bination of reduction (of As(V) to As(III)) and a series of methylationreactions (forming arsines, mono-, di-, and tri-methylarsine).Particularly both aerobic and anaerobic microorganisms (e.g., bac-teria and microscopic fungi) are responsible for the evolution ofvolatile arsenicals. However, in a previous study, the rate of Asvolatilization induced by soil microbial communities was limited(0.0005e10% of total As content) (Liu et al., 2011). A number offactors (including forms and concentration of As, soil moisture, soiltemperature, organic materials, and other elements) are respon-sible for As volatilization. Beside these factors, microbial growthand their capacity for As volatilization vary genetically. For thisreason, genetically engineered organisms with improved methyl-ating capability of As would be a potential candidate for thebioremediation of As.

Staphylococcus sp. NBRIEAG-8 is capable of up taking and vola-tilizing As. These bacteria express ars genes and 8 new up-regulated proteins, which may have played an important role inreducing As toxicity (Srivastava et al., 2012). Likewise, many otherGram-negative and -positive bacteria can exhibit a resistancemechanism against As with the aid of the ars operon (typicallyarsRDABC) encoded either on the chromosome or on plasmids (Xuet al., 1998). The role of arsA, arsR, and arsB in such mechanismswas also identified and discussed (Srivastava et al., 2012; Zhouet al., 2000). In both cases of ars operon (arsRBC or arsRDABC),there are two necessary components: (i) the reduction of As(V) toAs(III) by a reductase enzyme (ArsC) and (ii) an As(III) expulsionpump (ArsB), which subsequently extrude As(III) (Tsai et al., 2009).

An E. coli expressing arsenite S-adenosyl methionine methyltransferase gene (arsM) cloned from Rhodopseudomonas palustriswas reported to convert more toxic inorganic As to less toxic vol-atile trimethyl arsine (TMAs) through methylation (Yuan et al.,2008). Another study demonstrated that As from the contami-nated soil could be removed through volatilization by GE bacteria,with the expression of arsM gene (Liu et al., 2011). These speciesexpressed arsM (isolated from Rhodopseudomonas palustris) inSphingomonas desiccabilis and Bacillus idriensis to attain a 10-foldincrease of methylated As gas relative to its wild form in aqueoussystem. During a 30-day period, about 2.2e4.5% of As (w42 mg/kg)in contaminated soil was removed via bio-volatilization induced bythis GE bacteria expressing arsM gene (Liu et al., 2011). Thesefindings suggest that over expression of arsM genes in Sphingo-monas desiccabilis and B. idriensis can lead to manifold increases inmethylated As gas compared to the activity of wild type (WT)strain. Thus, this volatilization approach using the GE bacteria issuggested as a potent tool for the removal or suppression of Ascontamination (Singh et al., 2011).

5.3. Intracellular chelation

Arsenite can be converted into inactive complexes by bindingitself to many types of intracellular chelating proteins or peptidescontaining thiol ligands (e.g., GSH, PCs, and MTs) (Ngu et al., 2008).Among those ligands, GSH is well known for its role as a major

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reservoir of non-protein thiols (Noctor, 2006). Consequently, thepresence of such thiol ligand is important in both arsenate reduc-tion and arsenite transport into the vacuoles (Wysocki et al., 2003).Over-expression of the Saccharomyces cerevisiae GSH1 gene (whichencoded a g-glutamyl cysteine synthetase (g-ECS)), the firstenzyme in the GSH biosynthesis pathway (Foyer and Noctor, 2005),elevated the tolerance and accumulation of As in Arabidopsisthaliana (Guo et al., 2008). MTs belonged to a family of cysteine-richproteins with the unique ability to form stable metal-thiolateclusters with their two metal-bindings, cysteine-rich domains, asthemajormetal-binding ligands in animals (Morris et al., 1999). It isnoteworthy that As-binding MTs in the alga Fucus vesiculosus havenot been isolated from bacteria (Merrifield et al., 2004), whereasPCs are widely found in plants and yeasts as small enzymaticallysynthesized cysteine-rich peptides (Wünschmann et al., 2007).

5.4. Extrusion

The reduction or suppression of arsenite cytotoxicity byS. cerevisiae is known to proceed via two different pathways. One isthrough the arsenite extrusion pump Arr3p, which can transportthe As(III)eGSH complexes outside the cell through cell membrane.In addition, tolerance against As can be activated by such overexpression of Arr3p in yeast (Bobrowicz et al., 1997) or via thetransport of GSH-conjugated arsenite into the vacuole in themembrane efflux pump (Ghosh et al., 1999). The Ycf1p proteinassociated with the vacuolar membrane is a member of the ABCtransporter super family to allow the ATP-dependent transport of awide range of GSH-conjugated substrates (such as As(GS)3) into thevacuole (Tsai et al., 2009).

5.5. Transformation of As into an organic form

In natural waters, As is mostly found in its inorganic forms suchas As(III) or As(V), while the former is well known for enhancedmobility and toxicity relative to the latter (Tsai et al., 2009).Elemental As is not common, and organic As is only found inextremely reducing environments (Bentley and Chasteen, 2002).Because of its multiple oxidation states (�3, 0, þ3, and þ5), theirmobilization becomes complicated under various environmentalconditions. In that case, its remediation also becomes a delicatetask. In general, the dominant range of As is distinguished betweenlow (As(V)) and high pH range (As(III)). The form of As(III) salt suchas As(OH)3, which is more toxic and difficult to remove can also beprevalent under reducing conditions (Smedley and Kinniburgh,2002). In addition, nitrate can also affect As cycling, as it can beinvolved in the oxidation of ferrous iron to produce As-sorbingparticles (Senn and Hemond, 2002). A number of microorganismshave been shown to methylate As to give rise to monomethyl,dimethyl, and/or tri-methyl derivatives (Qin et al., 2006). As thesemethylated As species are volatile, they can be rapidly released intothe atmosphere.

6. Considerations on improving the efficiency ofphytoremediation

6.1. Expression of eukaryotic genes

As over expression of phytochelatin synthase (PCS) has proven,an increase in the synthesis of chelators such as GSH and PCs isconsidered a highly effective approach to remediate metals andmetalloids (Grill et al., 2007). Li et al. (2005) already demonstratedthat the constitutive over expression of AtPCS1 resulted in a sub-stantial increase in As resistance, with a 20e100 fold greaterbiomass in transgenic plants after exposure to As, while leaving to

Cd hypersensitivity. Cytosolic over expression of the AtPCS1 genewas found to increase As tolerance of transgenic plants (Picaultet al., 2006). The g-ECS over expression in A. thaliana exposed toAs showed a 3- to 20-fold increase in the production of g-EC, GSH,and PCS (Li et al., 2006b, 2005). This probably increased productionof g-EC, GSH, and PCS making A. thalianamore resistance to As. Theresults of these studies suggest that amultigenic approach based onoptimizing g-ECS, GS, and PCS activitymight help plants experiencea multifold increment of tolerance with the accumulation of themetalloid. The detoxification of As through reduction of As(V)makes AR function as another logical target for genetic engineering(Fig 1) (Bleeker et al., 2006; Duan et al., 2005).

To improve As tolerance and accumulationwithout affecting thephosphate metabolism, the over expression of ARmay be limited tothe roots with the simultaneous up-regulation of the As(III) che-lation capacity, root-to-shoot transport, and subsequent vacuolarsequestration. Tong et al. (2004) reported that more substratewould be sequestered (without large amounts of chelating peptide)by increasing the vacuolar transport capacity. An increasedexpression of sulfate transporters might also account for notableaccumulation of As in Brassica juncea (Tripathi et al., 2012b). It wasconcluded that the As detoxification processes should operatethrough the following steps: (i) perception of the stress inducedupon As exposure bymodulating the signaling mechanisms and (ii)activation of the detoxification processes (via stimulation of sulfateassimilation pathways) for effective complexation of As. Some ofthe responses induced upon exposure to As actually mimic thoseseen under sulfur depletion conditions. Because As-induced stresscan be perceived through As-mediated changes in sulfur status,such mechanism opens the possibility for application tobiotechnology.

Tu and Ma (2002) also observed that Ca supplementationresulted in an increase in the level of both total and inorganic As,specifically As(III). It was thus suggested that Ca should play acentral role in the uptake, transport, reduction, or complexation ofAs. In that way, Ca can enhance the rate of As accumulation; butsuch a hypothesis needs to be validated further. Li et al. (2006a)stressed the relationship between Ca with As due to their cooper-ative relationship in complexation. Rai et al. (2011) showed that Casupplementation can lead to a better complexation of the accu-mulated As, e.g., in the form of Ca arsenate and Ca arsenite in B.juncea callus. They also showed that, in the presence of external Ca,thiol metabolismwas stimulated. Hence, a major response of otherantioxidants was not required, while the reverse was true to As(V)-alone treatment. These authors also reported a significantly higherMAPK3 expression in As(V) þ Ca treated callus than As(V) onlytreated callus. This opens up other possible pathway for geneticengineers to manipulate plants and create an As tolerant hyper-accumulator.

To restrict As contamination of edible plant parts such as cerealgrain, preventing root-to-shoot translocation would suffice. How-ever, as this strategy should fail for obvious reasons for root crops,an almost complete cessation of As uptake would be required.Another route for increasing food safety may be to promote thetranslocation of As to shoots and its subsequent volatilization intothe atmosphere (Tripathi et al., 2008).

6.2. Expressing prokaryotic homolog genes

The employment of some microbial genes capable of bio-volatilization was made to treat environments contaminated withsome toxic metals like mercury and selenium (LeDuc and Terry,2005; Meagher and Heaton, 2005). Consequently, such ap-proaches can also be attested to reduce the buildup of As in edibleplant parts such as grains. A high level of root As(III) extrusion

Fig. 1. Systematic approach to engineer plant cell for As remediation (Dhankher et al., 2002; Guo et al., 2008; Li et al., 2004; Picault et al., 2006; Pomponi et al., 2006; Schwartz et al.,2010; Song et al., 2003; Tsai et al., 2009). Matching symbols ( , , and ) indicate that these genes work synergistically.

S. Rahman et al. / Journal of Environmental Management 134 (2014) 175e185182

capacity through ArsAB- and ACR3-like mechanisms in the plasmamembrane, coupled to the action of gene products (such as ArsM inshoot tissue), which may promote As volatilization, would bedesirable in this respect.

As(III) efflux has been reported in many plant species (Su et al.,2010). However, as of yet, no specific As efflux pathway has beenidentified in plants. The ArsAB operon encodes As efflux trans-porters in the form of antiporters and ABC transporters to pumpAs(III) out of the cell. In yeast, the ACR3 antiporter removes As(III)from the cytosol to the external medium; and the ABC transporterMRP2 is believed to deliver complexed As(III) into the bile ofmammals for subsequent secretion via the feces (Ali et al., 2012;Maciaszczyk-Dziubinska et al., 2011). According to a recent study,some NIPs are found to be capable of bidirectional transport tocontribute to the removal of As from the symplast (Isayenkov andMaathuis, 2008). Ali et al. (2012) and Maciaszczyk-Dziubinskaet al. (2011) heterologously expressed ScACR3 in A. thaliana fromthe yeast S. cerevisiae. ScACR3 is a plasma membrane-located, Hþ

gradient-driven antiporter that forms the primary As(III) effluxmechanism in yeast. No ACR3 homologues have been found inhigher plants. Indriolo et al. (2010) observed that the heterologousexpression of ScACR3 helped improve plant tolerance of As(III) andAs(V), at both the cellular and whole plant level: the rooteshootpartitioning of As is affected by controlling the As efflux to theexternal medium. The effects of the heterologous expression ofScACR3 are affected by a host of variables, including plant species,developmental stage, tissue complexity, etc. However, overall, ifone can utilize well-characterized As transporters from bacteriaand fungi, it is a highly valuable asset for the future improvement of

crops. The growth potential of crops in environments where As ispresent at or above toxic levels can be significantly improved bysuch approach. Nonetheless, further adjustment may be required,for example, in the form of tissue-specific promoters to avoidpotentially harmful effects such as enhanced root-to-shoot trans-location of As. Although such translocation is undesirable for foodcrops, it can also be applied to increase the phytoremediation ca-pacities of plant.

7. Conclusions

In this study, a review is provided to describe how As toxicityaffects biological media and how to resolve such problem. Manyresearchers have been conducted to reduce the As concentrationfrom the natural resources over the past decades. Several authorsput a great deal of efforts into explaining the mechanisms of Asmineral formation and accumulation by some plants and aquaticorganisms from groundwaters and soils exposed to the high level ofAs. However, it is yet difficult to explain fully how such waters areformed and should be treated. Bio-remediation can be an effectiveway to breakdown As contamination with the aid of potent tools(i.e., genetic engineering). Many plants and microorganisms canbreakdown inorganic As naturally, but this is not sufficient on theglobal scale. Therefore, as a means to resolve this problem, we candevelop engineered microorganisms or transgenic plants byinserting the As resistant and metabolic enzyme encoding geneswith the help of genetic engineering. Here, we present a systematicapproach to engineer As remediating plant cell. Better knowledgeon the metabolism and detoxification pathway of As and other

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heavy metals in both eukaryotes and prokaryotes will help futureresearchers deal with the environmental problem of As withmaximum efficiency.

Acknowledgments

This research was supported by the Basic Science ResearchProgram through the National Research Foundation of Korea (NRF)funded by the Ministry of Science, ICT and Future Planning (GrantNo. 2013-004624). The experimental work reported herein wasconducted at the authors’ previous affiliation: Department ofEnvironment & Energy, Sejong University, Seoul, Korea 143-747.

Appendix A. Supplementary data

Supplementary data related to this article can be found at http://dx.doi.org/10.1016/j.jenvman.2013.12.027.

References

Abercrombie, J., Halfhill, M., Ranjan, P., Rao, M., Saxton, A., Yuan, J., Stewart, C.N.,2008. Transcriptional responses of Arabidopsis thaliana plants to As (V) stress.BMC Plant Biol. 8, 87.

Ali, W., Isner, J.C., Isayenkov, S.V., Liu, W., Zhao, F.J., Maathuis, F.J., 2012. Heterolo-gous expression of the yeast arsenite efflux system ACR3 improves Arabidopsisthaliana tolerance to arsenic stress. New. Phytol. 194, 716e723.

Barringer, J.L., Reilly, P.A., 2013. Arsenic in groundwater: a summary of sources and thebiogeochemical and hydrogeologic factors affecting arsenic occurrence andmobility. Curr. Perspect. Contam.Hydrol.WaterResour. Sustain. Chapter 4, 83e116.

Bentley, R., Chasteen, T.G., 2002. Microbial methylation of metalloids: arsenic,antimony, and bismuth. Microbiol. Mol. Biol. Rev. 66, 250e271.

Bergqvist, C., Greger, M., 2012. Arsenic accumulation and speciation in plants fromdifferent habitats. Appl. Geochem. 27, 615e622.

Bleeker, P.M., Hakvoort, H.W., Bliek, M., Souer, E., Schat, H., 2006. Enhanced arsenatereduction by a CDC25-like tyrosine phosphatase explains increased phytoche-latin accumulation in arsenate-tolerant Holcus lanatus. Plant J. 45, 917e929.

Bleeker, P.M., Schat, H., Vooijs, R., Verkleij, J.A.C., Ernst, W.H.O., 2003. Mechanisms ofarsenate tolerance in Cytisus striatus. New. Phytol. 157, 33e38.

Bobrowicz, P., Wysocki, R., Owsianik, G., Goffeau, A., Ulaszewski, S., 1997. Isolation ofthree contiguous genes, ACR1, ACR2 and ACR3, involved in resistance to arseniccompounds in the yeast Saccharomyces cerevisiae. Yeast 13, 819e828.

Brunt, R., Vasak, L., Griffioen, J., 2004. Arsenic in Groundwater: Probability ofOccurrence of Excessive Concentration on Global Scale. IGRAC.

Bundschuh, J., Litter, M.I., Parvez, F., Román-Ross, G., Nicolli, H.B., Jean, J.-S., Liu, C.-W., Lopez, D., Armienta, M.A., Guilherme, L.R., 2012. One century of arsenicexposure in Latin America: a review of history and occurrence from 14 coun-tries. Sci. Total Environ. 429, 2e35.

Cavalca, L., Zanchi, R., Corsini, A., Colombo, M., Romagnoli, C., Canzi, E., Andreoni, V.,2010. Arsenic-resistant bacteria associated with roots of the wild Cirsiumarvense (L.) plant from an arsenic polluted soil, and screening of potential plantgrowth-promoting characteristics. Syst. Appl. Microbiol. 33, 154e164.

Chakraborti, D., Rahman, M.M., Das, B., Murrill, M., Dey, S., Chandra Mukherjee, S.,Dhar, R.K., Biswas, B.K., Chowdhury, U.K., Roy, S., Sorif, S., Selim, M., Rahman, M.,Quamruzzaman, Q., 2010. Status of groundwater arsenic contamination inBangladesh: a 14-year study report. Water Res. 44, 5789e5802.

Chanpiwat, P., Sthiannopkao, S., Cho, K.H., Kim, K.-W., San, V., Suvanthong, B.,Vongthavady, C., 2011. Contamination by arsenic and other trace elements of tube-well water along the Mekong River in Lao PDR. Environ. Pollut. 159, 567e576.

Cutler, W.G., Brewer, R.C., El-Kadi, A., Hue, N.V., Niemeyer, P.G., Peard, J., Ray, C.,2013. Bioaccessible arsenic in soils of former sugar cane plantations, Island ofHawaii. Sci. Total Environ. 442, 177e188.

Corsini, A., Cavalca, L., Crippa, L., Zaccheo, P., Andreoni, V., 2010. Impact of glucoseon microbial community of a soil containing pyrite cinders: role of bacteria inarsenic mobilization under submerged condition. Soil. Biol. Biochem. 42, 699e707.

Das, S., Jean, J.-S., Kar, S., 2013. Bioaccessibility and health risk assessment of arsenicin arsenic-enriched soils, Central India. Ecotoxicol. Environ. Saf. 92, 252e257.

Davis, A., Sherwin, D., Ditmars, R., Hoenke, K.A., 2001. An analysis of soil arsenicrecords of decision. Environ. Sci. Technol. 35, 2401e2406.

Dey, S., Ouellette, M., Lightbody, J., Papadopoulou, B., Rosen, B.P., 1996. An ATP-dependent As (III)-glutathione transport system in membrane vesicles ofLeishmania tarentolae. Proc. Natl. Acad. Sci. U S A 93, 2192e2197.

Dhankher, O.P., Li, Y., Rosen, B.P., Shi, J., Salt, D., Senecoff, J.F., Sashti, N.A.,Meagher, R.B., 2002. Engineering tolerance and hyperaccumulation of arsenic inplants by combining arsenate reductase and gamma-glutamylcysteine synthe-tase expression. Nat. Biotechnol. 20, 1140e1145.

Dhankher, O.P., Rosen, B.P., McKinney, E.C., Meagher, R.B., 2006. Hyperaccumulationof arsenic in the shoots of arabidopsis silenced for arsenate reductase (ACR2).Proc. Natl. Acad. Sci. 103, 5413e5418.

Ding, D., Li, W.H., Song, G.L., Qi, H.Y., Liu, J.B., Tang, J.H., 2011. Identification of QTLsfor arsenic accumulation in Maize (Zea mays L.) using a RIL population. PLoSOne 6, e25646.

Duan, G., Kamiya, T., Ishikawa, S., Arao, T., Fujiwara, T., 2012. Expressing ScACR3 inrice enhanced arsenite efflux and reduced arsenic accumulation in rice grains.Plant Cell. Physiol. 53, 154e163.

Duan, G.L., Zhu, Y.G., Tong, Y.P., Cai, C., Kneer, R., 2005. Characterization of arsenatereductase in the extract of roots and fronds of Chinese brake fern, an arsenichyperaccumulator. Plant Physiol. 138, 461e469.

Duquesne, K., Lieutaud, A., Ratouchniak, J., Muller, D., Lett, M.C., Bonnefoy, V., 2008.Arsenite oxidation by a chemoautotrophic moderately acidophilic Thiomonassp.: from the strain isolation to the gene study. Environ. Microbiol. 10, 228e237.

Ellis, D.R., Gumaelius, L., Indriolo, E., Pickering, I.J., Banks, J.A., Salt, D.E., 2006.A novel arsenate reductase from the arsenic hyperaccumulating fern Pterisvittata. Plant Physiol. 141, 1544e1554.

Ellis, P.J., Conrads, T., Hille, R., Kuhn, P., 2001. Crystal structure of the 100 kDaarsenite oxidase from Alcaligenes faecalis in two crystal forms at 1.64 Å and2.03 Å. Struct. Lond. Engl. 9, 125e132, 1993.

Foyer, C.H., Noctor, G., 2005. Oxidant and antioxidant signalling in plants: a re-evaluation of the concept of oxidative stress in a physiological context. PlantCell. Environ. 28, 1056e1071.

Ghosh, M., Shen, J., Rosen, B.P., 1999. Pathways of As(III) detoxification in Saccha-romyces cerevisiae. Proc. Natl. Acad. Sci. U S A 96, 5001e5006.

Gómez, J., Lillo, J., Sahun, B., 2006. Naturally occurring arsenic in groundwater andidentification of the geochemical sources in the Duero Cenozoic Basin, Spain.Environ. Geol. 50, 1151e1170.

Gourbal, B., Sonuc, N., Bhattacharjee, H., Legare, D., Sundar, S., Ouellette, M.,Rosen, B.P., Mukhopadhyay, R., 2004. Drug uptake and modulation of drugresistance in Leishmania by an aquaglyceroporin. J. Biol. Chem. 279, 31010e31017.

Grill, E., Mishra, S., Srivastava, S., Tripathi, R., 2007. Role of Phytochelatins in Phy-toremediation of Heavy Metals, Environmental Bioremediation Technologies.Springer, pp. 101e146.

Guo, J., Dai, X., Xu, W., Ma, M., 2008. Overexpressing GSH1 and AsPCS1 simulta-neously increases the tolerance and accumulation of cadmium and arsenic inArabidopsis thaliana. Chemosphere 72, 1020e1026.

Gunduz, O., Simsek, C., Hasozbek, A., 2010. Arsenic pollution in the groundwater ofSimav Plain, Turkey: Its impact on water quality and human health. Water, Air,Soil. Pollut. 205, 43e62.

Halsey, P.M., 2000. Arsenic Contamination Study of Drinking Water in Nepal.Massachusetts Institute of Technology.

Heinrich-Salmeron, A., Cordi, A., Brochier-Armanet, C., Halter, D., Pagnout, C.,Abbaszadeh-Fard, E., Montaut, D., Seby, F., Bertin, P.N., Bauda, P., Arsene-Ploetze, F., 2011. Unsuspected diversity of arsenite-oxidizing bacteria asrevealed by widespread distribution of the aoxB gene in prokaryotes. Appl.Environ. Microbiol. 77, 4685e4692.

Héry, M., Gault, A.G., Rowland, H.A., Lear, G., Polya, D.A., Lloyd, J.R., 2008. Molecularand cultivation-dependent analysis of metal-reducing bacteria implicated inarsenicmobilisation in south-east asian aquifers. Appl. Geochem. 23, 3215e3223.

Hossain, M.A., Piyatida, P., da Silva, J.A.T., Fujita, M., 2012. Molecular mechanism ofheavy metal toxicity and tolerance in plants: central role of glutathione indetoxification of reactive oxygen species and Methylglyoxal and in heavy metalchelation. Bot. J. 2012, 1e37.

Huang, Y., Su, Z., Li, Y., Zhang, Q., Cui, L., Su, Y., Ding, C., Zhang, M., Feng, C., Tan, Y.,2009. Expression and purification of glutathione transferase-small ubiquitin-related modifier-metallothionein fusion protein and its neuronal and hepaticprotection against D-galactose-induced oxidative damage in mouse model.J. Pharmacol. Exp. Ther. 329, 469e478.

Indriolo, E., Na, G., Ellis, D., Salt, D.E., Banks, J.A., 2010. A vacuolar arsenite trans-porter necessary for arsenic tolerance in the arsenic hyperaccumulating fernPteris vittata is missing in flowering plants. Plant Cell. 22, 2045e2057.

Isayenkov, S.V., Maathuis, F.J., 2008. The Arabidopsis thaliana aquaglyceroporinAtNIP7;1 is a pathway for arsenite uptake. FEBS Lett. 582, 1625e1628.

Jakob, R., Roth, A., Haas, K., Krupp, E.M., Raab, A., Smichowski, P., Gomez, D.,Feldmann, J., 2010. Atmospheric stability of arsines and the determination oftheir oxidative products in atmospheric aerosols (PM10): evidence of thewidespread phenomena of biovolatilization of arsenic. J. Environ. Monit. 12,409e416.

Kaltreider, R.C., Davis, A.M., Lariviere, J.P., Hamilton, J.W., 2001. Arsenic alters thefunction of the glucocorticoid receptor as a transcription factor. Environ. HealthPersp. 109, 245e251.

Karczewska, A., Bogda, A., Krysiak, A., 2007. Arsenic in soils in the areas of formermining and mineral processing in Lower Silesia, southwestern Poland. TraceMetals Other Contam. Environ. 9, 411e440.

Khan,M.A., Ho, Y.-S., 2011. Arsenic in drinkingwater: a reviewon toxicological effects,mechanism of accumulation and remediation. Asian J. Chem. 23, 1889e1901.

Khan, K.A., Stroud, J.L., Zhu, Y.G., McGrath, S.P., Zhao, F.J., 2010. Arsenic bioavail-ability to rice is elevated in Bangladeshi paddy soils. Environ. Sci. Technol. 44,8515e8521.

King, D.J., Doronila, A.I., Feenstra, C., Baker, A.J., Woodrow, I.E., 2008. Phytostabili-sation of arsenical gold mine tailings using four Eucalyptus species: growth,arsenic uptake and availability after five years. Sci. Total Environ. 406, 35e42.

Kostal, J., Yang, R., Wu, C.H., Mulchandani, A., Chen, W., 2004. Enhanced arsenicaccumulation in engineered bacterial cells expressing ArsR. Appl. Environ.Microbiol. 70, 4582e4587.

S. Rahman et al. / Journal of Environmental Management 134 (2014) 175e185184

Krafft, T., Macy, J.M., 1998. Purification and characterization of the respiratoryarsenate reductase of Chrysiogenes arsenatis. Eur. J. Biochem 255, 647e653.

LeDuc, D.L., Terry, N., 2005. Phytoremediation of toxic trace elements in soil andwater. J. Ind. Microbiol. Biotechnol. 32, 514e520.

Leist, M., Casey, R., Caridi, D., 2000. The management of arsenic wastes: problemsand prospects. J. Hazard. Mater. 76, 125e138.

Li, W.-X., Chen, T.-B., Huang, Z.-C., Lei, M., Liao, X.-Y., 2006a. Effect of arsenic onchloroplast ultrastructure and calcium distribution in arsenic hyper-accumulator Pteris vittata L. Chemosphere 62, 803e809.

Li, Y., Dankher, O.P., Carreira, L., Smith, A.P., Meagher, R.B., 2006b. The shoot-specificexpression of g-glutamylcysteine synthetase directs the long-distance transportof thiol-peptides to roots conferring tolerance to mercury and arsenic. PlantPhysiol. 141, 288e298.

Li, Y., Dhankher, O.P., Carreira, L., Lee, D., Chen, A., Schroeder, J.I., Balish, R.S.,Meagher, R.B., 2004. Overexpression of phytochelatin synthase in Arabidopsisleads to enhanced arsenic tolerance and cadmium hypersensitivity. Plant Cell.Physiol. 45, 1787e1797.

Li, Y., Dhankher, O.P., Carreira, L., Lee, D., Chen, A., Schroeder, J.I., Balish, R.S.,Meagher, R.B., 2005. Overexpression of phytochelatin synthase in Arabidopsisleads to enhanced arsenic tolerance and cadmium hypersensitivity. Plant Cell.Physiol. 46, 387.

Lièvremont, D., Bertin, P.N., Lett, M.-C., 2009. Arsenic in contaminated waters:biogeochemical cycle, microbial metabolism and biotreatment processes. Bio-chimie 91, 1229e1237.

Liu, J., Chen, H., Miller, D.S., Saavedra, J.E., Keefer, L.K., Johnson, D.R., Klaassen, C.D.,Waalkes, M.P., 2001. Overexpression of glutathione S-transferase II and multi-drug resistance transport proteins is associated with acquired tolerance toinorganic arsenic. Mol. Pharmacol. 60, 302e309.

Liu, S., Zhang, F., Chen, J., Sun, G., 2011. Arsenic removal from contaminated soil viabiovolatilization by genetically engineered bacteria under laboratory condi-tions. J. Environ. Sci. 23, 1544e1550.

Liu, W., Zhu, Y.G., Hu, Y., Williams, P., Gault, A., Meharg, A., Charnock, J.,Smith, F.A., 2006. Arsenic sequestration in iron plaque, its accumulation andspeciation in mature rice plants (Oryza sativa L.). Environ. Sci. Technol. 40,5730e5736.

Liu, Z., Li, W., Qi, H., Song, G., Ding, D., Fu, Z., Liu, J., Tang, J., 2012. Arsenic accu-mulation and distribution in the tissues of inbred lines in maize (Zea mays L.).Genet. Resour. Crop Ev. 59, 1705e1711.

Ma, J.F., Yamaji, N., Mitani, N., Xu, X.-Y., Su, Y.-H., McGrath, S.P., Zhao, F.-J., 2008.Transporters of arsenite in rice and their role in arsenic accumulation in ricegrain. Proc. Natl. Acad. Sci. U S A 105, 9931e9935.

Ma, Y., Lin, J., Zhang, C., Ren, Y., Lin, J., 2011. Cd(II) and As(III) bioaccumulation byrecombinant Escherichia coli expressing oligomeric human metallothioneins.J. Hazard. Mater. 185, 1605e1608.

Maciaszczyk-Dziubinska, E., Migocka, M., Wysocki, R., 2011. Acr3p is a plasmamembrane antiporter that catalyzes As(III)/Hþ and Sb(III)/Hþ exchange inSaccharomyces cerevisiae. BBA e Biomembr. 1808, 1855e1859.

Meagher, R.B., Heaton, A.C., 2005. Strategies for the engineered phytoremediation oftoxic element pollution: mercury and arsenic. J. Ind. Microbiol. Biotechnol. 32,502e513.

Meharg, A.A., Hartley-Whitaker, J., 2002. Arsenic uptake and metabolism in arsenicresistant and nonresistant plant species. New. Phytol. 154, 29e43.

Meharg, A.A., Jardine, L., 2003. Arsenite transport into paddy rice (Oryza sativa)roots. New. Phytol. 157, 39e44.

Merrifield, M.E., Ngu, T., Stillman, M.J., 2004. Arsenic binding to Fucus vesiculosusmetallothionein. Biochem. Biophys. Res. Commun. 324, 127e132.

Mishra, S., Srivastava, S., Tripathi, R.D., Trivedi, P.K., 2008a. Thiol metabolism andantioxidant systems complement each other during arsenate detoxification inCeratophyllum demersum L. Aquat. Toxicol. 86, 205e215.

Mishra, V.K., Upadhyay, A.R., Pathak, V., Tripathi, B., 2008b. Phytoremediation ofmercury and arsenic from tropical opencast coalmine effluent through natu-rally occurring aquatic macrophytes. Water Air Soil. Pollut. 192, 303e314.

Mittler, R., 2002. Oxidative stress, antioxidants and stress tolerance. Trends PlantSci. 7, 405e410.

Mkandawire, M., Dudel, E.G., 2007. Are Lemna spp. effective phytoremediationagents. Biorem. Biodiv. Bioavail. 1, 56e71.

Morris, C.A., Nicolaus, B., Sampson, V., Harwood, J.L., Kille, P., 1999. Identificationand characterization of a recombinant metallothionein protein from a marinealga, Fucus vesiculosus. Biochem. J. 338, 553.

Mukherjee, A., Sengupta, M.K., Hossain, M.A., Ahamed, S., Das, B., Nayak, B., Lodh, D.,Rahman, M.M., Chakraborti, D., 2006. Arsenic contamination in groundwater: aglobal perspective with emphasis on the Asian scenario. J. Health, Popul. Nutr.24, 142e163.

Mukhopadhyay, R., Shi, J., Rosen, B.P., 2000. Purification and characterization ofAcr2p, the Saccharomyces cerevisiae arsenate reductase. J. Biol. Chem. 275,21149e21157.

Murcott, S., 2012. Arsenic Contamination in the World: an International Source-book. IWA Publishing, London.

Ngu, T.T., Easton, A., Stillman, M.J., 2008. Kinetic analysis of Arsenicemetalation ofhuman metallothionein: significance of the two-domain structure. J. Am. Chem.Soc. 130, 17016e17028.

Noctor, G., 2006. Metabolic signalling in defence and stress: the central roles ofsoluble redox couples. Plant Cell. Environ. 29, 409e425.

Nordstrom, D.K., 2002. Worldwide occurrences of arsenic in ground water. Sci. Mag.Wash., 2143e2145.

Norton, G.J., Duan, G., Dasgupta, T., Islam, M.R., Lei, M., Zhu, Y., Deacon, C.M.,Moran, A.C., Islam, S., Zhao, F.-J., Stroud, J.L., McGrath, S.P., Feldmann, J.,Price, A.H., Meharg, A.A., 2009. Environmental and genetic control of arsenicaccumulation and speciation in rice grain: comparing a range of commonCultivars grown in contaminated sites across Bangladesh, China, and India.Environ. Sci. Technol. 43, 8381e8386.

Nriagu, J.O., Bhattacharya, P., Mukherjee, A.B., Bundschuh, J., Zevenhoven, R.,Loeppert, R.H., 2007. Arsenic in soil and groundwater: an overview. In: ProsunBhattacharya, A.B.M.J.B.R.Z., Richard, H.L. (Eds.), Trace Metals and Other Con-taminants in the Environment. Elsevier, pp. 3e60.

Oremland, R.S., Stolz, J.F., 2005. Arsenic, microbes and contaminated aquifers.Trends Microbiol. 13, 45e49.

O’Reilly, J., Watts, M.J., Shaw, R.A., Marcilla, A.L., Ward, N.I., 2010. Arsenic contam-ination of natural waters in San Juan and La Pampa, Argentina. Environ. Geo-chem. Health 32, 491e515.

Páez-Espino, D., Tamames, J., de Lorenzo, V., Cánovas, D., 2009. Microbial responsesto environmental arsenic. Biometals 22, 117e130.

Palumbo-Roe, B., Cave, M., Klinck, B., Wragg, J., Taylor, H., O’Donnell, K., Shaw, R.,2005. Bioaccessibility of arsenic in soils developed over Jurassic ironstones ineastern England. Environ. Geochem. Health 27, 121e130.

Picault, N., Cazalé, A.C., Beyly, A., Cuiné, S., Carrier, P., Luu, D.T., Forestier, C.,Peltier, G., 2006. Chloroplast targeting of phytochelatin synthase in Arabi-dopsis: effects on heavy metal tolerance and accumulation. Biochimie 88,1743e1750.

Pickering, I.J., Gumaelius, L., Harris, H.H., Prince, R.C., Hirsch, G., Banks, J.A., Salt, D.E.,George, G.N., 2006. Localizing the biochemical transformations of arsenate in ahyperaccumulating fern. Environ. Sci. Technol. 40, 5010e5014.

Pomponi, M., Censi, V., Di Girolamo, V., De Paolis, A., di Toppi, L.S., Aromolo, R.,Costantino, P., Cardarelli, M., 2006. Overexpression of Arabidopsis phytochelatinsynthase in tobacco plants enhances Cd2þ tolerance and accumulation but nottranslocation to the shoot. Planta 223, 180e190.

Qin, J., Rosen, B.P., Zhang, Y., Wang, G., Franke, S., Rensing, C., 2006. Arsenic detoxifi-cation and evolution of trimethylarsine gas by a microbial arsenite S-adeno-sylmethionine methyltransferase. Proc. Natl. Acad. Sci. U S A 103, 2075e2080.

Rahman, M.A., Hasegawa, H., 2011. Aquatic arsenic: phytoremediation using floatingmacrophytes. Chemosphere 83, 633e646.

Rahman, M.A., Hasegawa, H., Ueda, K., Maki, T., Rahman, M.M., 2008. Influence ofEDTA and chemical species on arsenic accumulation in Spirodela polyrhiza L.(duckweed). Ecotoxicol. Environ. Saf. 70, 311e318.

Rahman, M.M., Naidu, R., Bhattacharya, P., 2009. Arsenic contamination ingroundwater in the Southeast Asia region. Environ. Geochem. Health 31, 9e21.

Rai, A., Tripathi, P., Dwivedi, S., Dubey, S., Shri, M., Kumar, S., Tripathi, P.K.,Dave, R., Kumar, A., Singh, R., Adhikari, B., Bag, M., Tripathi, R.D., Trivedi, P.K.,Chakrabarty, D., Tuli, R., 2011. Arsenic tolerances in rice (Oryza sativa) have apredominant role in transcriptional regulation of a set of genes includingsulphur assimilation pathway and antioxidant system. Chemosphere 82,986e995.

Ravenscroft, P., 2007. Predicting the global distribution of arsenic pollution ingroundwater. In: Royal Geographical Society Annual International Conference.Cambridge University, Royal Geographic Society, London, England.

Richey, C., Chovanec, P., Hoeft, S.E., Oremland, R.S., Basu, P., Stolz, J.F., 2009. Respi-ratory arsenate reductase as a bidirectional enzyme. Biochem. Biophys. Res.Commun. 382, 298e302.

Rosen, B.P., Liu, Z., 2009. Transport pathways for arsenic and selenium: a minire-view. Environ. Int. 35, 512e515.

Rubio, R., Ruiz-Chancho, M., López-Sánchez, J., 2010. Sample pre-treatment andextraction methods that are crucial to arsenic speciation in algae and aquaticplants. Trends Anal. Chem. 29, 53e69.

Schwartz, M.S., Benci, J.L., Selote, D.S., Sharma, A.K., Chen, A.G., Dang, H., Fares, H.,Vatamaniuk, O.K., 2010. Detoxification of multiple heavy metals by a half-molecule ABC transporter, HMT-1, and coelomocytes of Caenorhabditis ele-gans. PLoS One 5, e9564.

Senn, D.B., Hemond, H.F., 2002. Nitrate controls on iron and arsenic in an urbanlake. Science 296, 2373e2376.

Sharma, V.K., Sohn, M., 2009. Aquatic arsenic: toxicity, speciation, transformations,and remediation. Environ. Int. 35, 743e759.

Silver, S., Phung, L.T., 2005. Genes and enzymes involved in bacterial oxidation andreduction of inorganic arsenic. Appl. Environ. Microbiol. 71, 599e608.

Singh, J.S., Abhilash, P., Singh, H., Singh, R.P., Singh, D., 2011. Genetically engineeredbacteria: an emerging tool for environmental remediation and future researchperspectives. Gene 480, 1e9.

Singh, S., Kang, S.H., Lee, W., Mulchandani, A., Chen, W., 2010. Systematic engi-neering of phytochelatin synthesis and arsenic transport for enhanced arsenicaccumulation in E. coli. Biotechnol. Bioeng. 105, 780e785.

Singh, S., Mulchandani, A., Chen, W., 2008. Highly selective and rapid arsenicremoval by metabolically engineered Escherichia coli cells expressing Fucusvesiculosus metallothionein. Appl. Environ. Microbiol. 74, 2924e2927.

Smedley, P., Kinniburgh, D., 2002. A review of the source, behaviour and distribu-tion of arsenic in natural waters. Appl. Geochem. 17, 517e568.

Song, W.-Y., Sohn, E.J., Martinoia, E., Lee, Y.J., Yang, Y.-Y., Jasinski, M., Forestier, C.,Hwang, I., Lee, Y., 2003. Engineering tolerance and accumulation of lead andcadmium in transgenic plants. Nat. Biotechnol. 21, 914e919.

Srivastava, S., Mishra, S., Dwivedi, S., Tripathi, R., 2010. Role of thiol metabolism inarsenic detoxification in Hydrilla verticillata (Lf) Royle. Water Air Soil. Pollut.212, 155e165.

S. Rahman et al. / Journal of Environmental Management 134 (2014) 175e185 185

Srivastava, S., Mishra, S., Tripathi, R., Dwivedi, S., Trivedi, P., Tandon, P., 2007. Phytoche-latins and antioxidant systems respond differentially during arsenite and arsenatestress in Hydrilla verticillata (Lf) Royle. Environ. Sci. Technol. 41, 2930e2936.

Srivastava, S., Sharma, Y., 2013. Arsenic occurrence and accumulation in soil andwater of eastern districts of Uttar Pradesh, India. Environ. Monit. Assess. 185,4995e5002.

Srivastava, S., Shrivastava, M., Suprasanna, P., D’Souza, S.F., 2011. Phytofiltration ofarsenic from simulated contaminated water using Hydrilla verticillata in fieldconditions. Ecol. Eng. 37, 1937e1941.

Srivastava, S., Verma, P.C., Singh, A., Mishra, M., Singh, N., Sharma, N., Singh, N.,2012. Isolation and characterization of Staphylococcus sp. strain NBRIEAG-8from arsenic contaminated site of West Bengal. Appl. Microbiol. Biotechnol.95, 1275e1291.

Sthiannopkao, S., Kim, K., Sotham, S., Choup, S., 2008. Arsenic and manganese intube well waters of Prey Veng and Kandal Provinces, Cambodia. Appl. Geochem.23, 1086e1093.

Stolz, J.F., Basu, P., Santini, J.M., Oremland, R.S., 2006. Arsenic and selenium in mi-crobial metabolism. Annu. Rev. Microbiol. 60, 107e130.

Stroud, J.L., Norton, G.J., Islam, M.R., Dasgupta, T., White, R.P., Price, A.H.,Meharg, A.A., McGrath, S.P., Zhao, F.-J., 2011. The dynamics of arsenic in fourpaddy fields in the Bengal delta. Environ. Pollut. 159, 947e953.

Su, Y.-H., McGrath, S., Zhao, F.-J., 2010. Rice is more efficient in arsenite uptake andtranslocation than wheat and barley. Plant Soil. 328, 27e34.

Taggart, R., Starr, L., 2009. Biology: The Unity and Diversity of Life. CengageBrain.com.Tong, Y.-P., Kneer, R., Zhu, Y.-G., 2004. Vacuolar compartmentalization: a second-

generation approach to engineering plants for phytoremediation. TrendsPlant Sci. 9, 7e9.

Tripathi, M.K., Mishra, A.S., Misra, A.K., Vaithiyanathan, S., Prasad, R., Jakhmola, R.C.,2008. Selection of white-rot basidiomycetes for bioconversion of mustard(Brassica compestris) straw under solid-state fermentation into energy substratefor rumen micro-organism. Lett. Appl. Microbiol. 46, 364e370.

Tripathi, P., Dwivedi, S., Mishra, A., Kumar, A., Dave, R., Srivastava, S., Shukla, M.K.,Srivastava, P.K., Chakrabarty, D., Trivedi, P.K., 2012a. Arsenic accumulation innative plants of West Bengal, India: prospects for phytoremediation but con-cerns with the use of medicinal plants. Environ. Monit. Assess. 184, 2617e2631.

Tripathi, R.D., Srivastava, S., Mishra, S., Singh, N., Tuli, R., Gupta, D.K.,Maathuis, F.J.M., 2007. Arsenic hazards: strategies for tolerance and remediationby plants. Trends Biotechnol. 25, 158e165.

Tripathi, R.D., Tripathi, P., Dwivedi, S., Dubey, S., Chatterjee, S., Chakrabarty, D.,Trivedi, P.K., 2012b. Arsenomics: omics of arsenic metabolism in plants. Front.Physiol. 3, 275.

Tsai, S.-L., Singh, S., Chen, W., 2009. Arsenic metabolism by microbes in nature andthe impact on arsenic remediation. Curr. Opin. Chem. Biol. 20, 659e667.

Tu, C., Ma, L.Q., 2002. Effects of arsenic concentrations and forms on arsenic uptakeby the hyperaccumulator ladder brake. J. Environ. Qual. 31, 641e647.

Tuli, R., Chakrabarty, D., Trivedi, P.K., Tripathi, R.D., 2010. Recent advances in arsenicaccumulation and metabolism in rice. Mol. Breed. 26, 307e323.

Twarakavi, N.K.C., Kaluarachchi, J.J., 2006. Arsenic in the shallow ground waters ofconterminous United States: assessment, health risks, and costs for MCLcompliance. J. Am. Water Resour. Assoc. 42, 275e294.

Violante, A., Gaudio, S., Pigna, M., Pucci, M., Amalfitano, C., 2008. Sorption anddesorption of arsenic by soil minerals and soils in the presence of nutrients andorganics. In: Huang, Q., Huang, P., Violante, A. (Eds.), Soil Mineral Microbe-Organic Interactions. Springer, Berlin Heidelberg, pp. 39e69.

Wang, X., Ma, L.Q., Rathinasabapathi, B., Cai, Y., Liu, Y.G., Zeng, G.M., 2011. Mecha-nisms of efficient arsenite uptake by arsenic hyperaccumulator Pteris vittata.Environ. Sci. Technol. 45, 9719e9725.

Welch, A.H., Watkins, S.A., Helsel, D.R., Focazio, M.J., 2000. Arsenic in Ground-waterResources of the United States. US Geological Survey Fact Sheet, FS-063.

Wünschmann, J., Beck, A., Meyer, L., Letzel, T., Grill, E., Lendzian, K.J., 2007. Phy-tochelatins are synthesized by two vacuolar serine carboxypeptidases inSaccharomyces cerevisiae. FEBS Lett. 581, 1681e1687.

Wysocki, R., Clemens, S., Augustyniak, D., Golik, P., Maciaszczyk, E., Tamás, M.J.,Dziadkowiec, D., 2003. Metalloid tolerance based on phytochelatins is notfunctionally equivalent to the arsenite transporter Acr3p. Biochem. Biophys.Res. Commun. 304, 293e300.

Xu, C., Zhou, T., Kuroda, M., Rosen, B.P., 1998. Metalloid resistance mechanisms inprokaryotes. J. Biochem 123, 16e23.

Yuan, C., Lu, X., Qin, J., Rosen, B.P., Le, X.C., 2008. Volatile arsenic species releasedfrom Escherichia coli expressing the AsIII S-adenosylmethionine methyl-transferase gene. Environ. Sci. Technol. 42, 3201e3206.

Zhang, X., Lin, A.-J., Zhao, F.-J., Xu, G.-Z., Duan, G.-L., Zhu, Y.-G., 2008. Arsenicaccumulation by the aquatic fern Azolla: comparison of arsenate uptake,speciation and efflux by A. caroliniana and A. filiculoides. Environ. Pollut. 156,1149e1155.

Zhao, F.J., Ago, Y., Mitani, N., Li, R.Y., Su, Y.H., Yamaji, N., McGrath, S.P., Ma, J.F., 2010.The role of the rice aquaporin Lsi1 in arsenite efflux from roots. New. Phytol.186, 392e399.

Zhao, F.J., Ma, J.F., Meharg, A.A., McGrath, S.P., 2009. Arsenic uptake and metabolismin plants. New. Phytol. 181, 777e794.

Zhou, T., Radaev, S., Rosen, B.P., Gatti, D.L., 2000. Structure of the ArsA ATPase: thecatalytic subunit of a heavy metal resistance pump. EMBO J. 19, 4838e4845.