Removing Heavy Metals in Water: The Interaction of Cactus Mucilageand Arsenate (As (V))Dawn I. Fox,† Thomas Pichler,‡ Daniel H. Yeh,§ and Norma A. Alcantar†,*†Department of Chemical & Biomedical Engineering, 4202 E Fowler Ave, University of South Florida, Tampa, Florida 33620, UnitedStates‡Department of Geosciences, University of Bremen, Bremen, Germany§Department of Civil & Environmental Engineering, 4202 E Fowler Ave, University of South Florida, Tampa Florida 33620, UnitedStates

*S Supporting Information

ABSTRACT: High concentrations of arsenic in groundwater continue topresent health threats to millions of consumers worldwide. Particularly, affectedcommunities in the developing world need accessible technologies for arsenicremoval from drinking water. We explore the application of cactus mucilage,pectic polysaccharide extracts from Opuntia f icus-indica for arsenic removal.Synthetic arsenate (As (V)) solutions were treated with two extracts, a gellingextract (GE) and a nongelling extract (NE) in batch trials. The arsenicconcentration at the air−water interface was measured after equilibration. TheGE and NE treated solutions showed on average 14% and 9% increases inarsenic concentration at the air−water interface respectively indicating that themucilage bonded and transported the arsenic to the air−water interface. FTIRstudies showed that the −CO groups (carboxyl and carbonyl groups) and −OH(hydroxyl) functional groups of the mucilage were involved in the interactionwith the arsenate. Mucilage activity was greater in weakly basic (pH 9) and weakly acidic (pH 5.5) pH. This interaction can beoptimized and harnessed for the removal of arsenic from drinking water. This work breaks the ground for the application ofnatural pectic materials to the removal of anionic metallic species from water.

■ INTRODUCTIONContamination of groundwater with arsenic from naturalleaching of arsenic bearing minerals is an environmentalphenomenon, which affects millions of people in different partsof world. However, the health impact is most severe in EastAsia where approximately 100 million people in the BengalBasin of Bangladesh and West Bengal, India are exposed to thedetrimental health effects of long-term consumption of waterfrom contaminated wells.1 The majority of the affectedcommunities have no access to conventional water treatment.The World Health Organization (WHO) recommended thatthe maximum concentration of arsenic in drinking water shouldnot exceed 10 μg/L.2 This large scale arsenic poisoning hasfueled research into accessible technologies for arsenic removalwhich need to be inexpensive, robust, reliable, and easy tomaintain, while requiring little or no fossil fuel for operation.Plant-based materials are especially attractive since they are

renewable, biodegradable, and can be sustainably managed, allof which contribute to making them suitable for accessibletechnologies. Pectins and pectinaceous plant wastes have beenstudied extensively as sorbents for the removal of heavy metalcations from wastewater.3−13 Citrus peels, sugar beet pulp andother fruit wastes have been used to sorb a number of divalentheavy metal pollutants including Cu2+, Cd2+, Co2+, Pb2+, Ni2+,Fe2+, Zn2+, and Sr2+. In several instances, carboxylic and

hydroxyl functional groups of these materials were identified asactive sites for metal sorption.3,7,14,15

Building on the demonstrated affinity of pectins andpectinaceous plant materials for metal sorption, cactus mucilageand cactus pectin extracted from the pads of the Opuntia f icus-indica, were investigated in this work as a low cost material forarsenic removal. The two cactus extracts are distinguishable bythe ability of the cactus pectin to form gels in the presence ofCa2+ ions, and is referred to as the gelling extract (GE). Thecactus mucilage, a pectic polysaccharide is referred to as thenongelling extract (NE).16 Several researchers have shown thatwhile both extracts contain arabinose, galactose, xylose,rhamnose, and galacturonic acid, the major difference betweenthem is that GE is mainly comprised of galacturonic acid.17−21

McGarvie and Parolis22 proposed a polygalacturonic acid andrhamnose backbone for the NE structure with branched sidechains of galactose and rhamnose; the branches beingcomposed of arabinose, and xylose. Cardenas et al.16 reportedthat the gelling extract consisted mainly of poly-D-galacturonic

Received: June 27, 2011Revised: February 9, 2012Accepted: March 8, 2012Published: March 8, 2012

Article

pubs.acs.org/est

© 2012 American Chemical Society 4553 dx.doi.org/10.1021/es2021999 | Environ. Sci. Technol. 2012, 46, 4553−4559

acid. For both of these pectic polysaccharides the mainfunctional groups are carbonyl, carboxyl, and hydroxyl groups.Despite the widespread application of plant pectins to the

removal of cationic heavy metal contaminants, they have notbeen used with anionic contaminants. This is possibly due toconcerns that the electrostatic repulsion would hinderinteraction between the polyanionic pectins and anionic metalcontaminants and lead to low loading capacity. However,electrostatic challenges are not the only determining factor ininteraction, as evidenced by natural organic matter (NOM)binding with arsenic species.23−26 NOM, particularly humicacids, share carboxylic and alcohol functional groups with pecticpolysaccharides and as such the latter are also expected to beable to bind arsenic species in solution.While cactus mucilage has been explored for water

purification,27,28 our research group was the first todemonstrate an interaction between cactus mucilage andarsenic.29,30 Solutions of arsenate (As (V)), which were treatedwith mucilage showed differences in arsenic concentration atthe air−water interface over time. These concentrationdifferences were attributed to the mucilage binding the arsenicand transporting it either toward or away from the air−waterinterface.The current work looks at the interaction of the cactus

mucilage with As(V), using a combination of batch tests andmolecular spectroscopy. ATR-FTIR and UV-Vis spectroscopyshowed that the −CO groups (carboxyl and carbonyl groups)and −OH (hydroxyl) functional groups of the mucilage wereinvolved in reacting with arsenate. The gelling extract (GE)performed better on average than the nongelling extract (NE)and the pH was shown to affect the mucilage performance.The vision for this technology is to develop low-cost arsenic

removal filters for household point-of-use applications as well ascommunity level treatment for low-income communities. Thesimplicity of the mucilage extraction makes its manufacturewidely accessible. Potentially, this work will add to the overlapof water remediation materials and natural products since thematerial may become a new water treatment material and alsoexpands the use for pectinaceous carbohydrate polymers.

■ MATERIALS AND METHODSMucilage was extracted from the modified stems (pads) of theOpuntia f icus-indica cactus. Fresh pads were obtained from theprivate nursery of Dr. Norma Alcantar in Tampa, Florida, U.S.The plants were grown from pads originally purchased fromLiving Stones Nursery, Tucson AZ. Water intake wascontrolled to ensure they all grew at the same rate. No othercontrols were necessary since different growing conditions onlyaffect the mucilage and pectin content of the pads.31 There wasno significant variation from plant to plant.All chemicals used were analytical grade or better and

purchased from Fisher Scientific (Pittsburgh, PA).Mucilage Extraction. Cactus Pad Preparation. Two

mucilage fractions were extracted from the cactus pads; a pecticgelling extract (GE) and a nongelling extract (NE). The NEextraction was done following a modification of the methodused by Goycoolea et al.18 The pads were first cleaned byremoving thorns and brown spots, washed, dried, and weighed.The pads were diced and heated for 20 min at 80−85 °C in 1%NaCl solution (1:1 mass to volume ratio) in order to inactivateenzymes. After cooling, the mixture was liquidized for 45−50 sat the highest speed in a commercial blender (Osterizer), thenneutralized with 1 M sodium hydroxide (NaOH). The mixture

was then centrifuged (Fisher Scientific accuSpin 400) at 4000rpm for 10 min to separate the liquid from the solids. Thesupernatant, containing the NE was decanted leaving the solidresidue for GE extraction.

Nongelling Extract (NE) Preparation. Sodium chloride(NaCl) was added to the liquid supernatant produced in thepad preparation step to obtain a final 1 M NaCl concentration.The liquid was then filtered using Whatman 41 filter paper. Byvisual observation, if the liquid were too viscous to flow easilythrough the Whatman 41 filter, then a knitted polyester clothfilter (Polx 1200, Berkshire Corp., Great Barrington, MA) wasused. NE was precipitated from the filtrate using acetone orisopropanol in a 2:3 ratio of supernatant to solvent. Theprecipitate was washed with ethanol−water mixtures in agraded series (70%, 80%, 90%, 95% ethanol and absoluteethanol) to remove any remaining impurities. The precipitatewas left to dry at room temperature overnight, followed by anovernight drying in an air oven (Yamato DX-41, Japan). Thematerial was pulverized with a ceramic mortar and pestle andstored in a closed container at room temperature.

Gelling Extract (GE) Preparation. The GE extractionprocedure was an adaptation of a method developed byTurquois et al.32 The differences we used to improve our yieldwere separating by centrifugation and vacuum filtration, using adifferent dosage of chelating agent and a shorter sequesteringtime, and using acetone as the precipitating solvent.The solid residue from the cactus pad preparation was mixed

with 7.5 g/L sodium hexametaphosphate [(NaPO3)6] in 50mM NaOH, in a 1:1 mass-to-volume ratio of residue tosolution. The mixture was stirred for 1 h, then vacuum filteredwith cloth to obtain the filtrate, which contains the dissolvedGE. The filtrate pH was lowered to 2.0 by titration withhydrochloric acid (HCl) and refrigerated overnight (∼5 °C) inorder to precipitate the GE. The precipitate was separated bycentrifugation and resuspended in sufficient DI water to coverit. The pH was adjusted to 8.0 with 1 M NaOH to redissolvethe precipitate. The resulting solution was purified by filteringthrough a 1.2 μm and a 0.45 μm membrane. The GE wasreprecipitated with acetone or isopropanol in a 2:3 liquid-to-solvent ratio, then washed and dried in the same manner as forNE.

Batch Experiments. As(V) solutions, 10 mL of 60−80 μg/L As, were treated with GE and NE in 15 mL centrifuge tubesto attain final mucilage concentrations of 5−100 mg/L. Anequilibration time of 20 h was established in previousunpublished work. After 36 h equilibration, 1 mL samplealiquots were removed from the air−water interface using anautomatic pipet. The total As concentration was determined byHydride Generation−Atomic Fluorescence Spectroscopy (HG-AFS). Two types of control experiments were run; As (V)solutions without mucilage, and mucilage solutions withoutAs(V), with all other test conditions and concentrations keptconstant. The As(V) stock solution used for experiments wasprepared by dissolving solid sodium arsenate in sufficientdeionized water to bring the final concentration to 1000 μg/L.The stock solution was continuously aerated using an aquariumaerator, which maintained the dissolved arsenic in the oxidizedarsenate form. This was done to represent the natural aerationof groundwater when pumped above ground. When pH was avariable, pH was adjusted using sodium hydroxide andhydrochloric acid.Results were reported in terms of increase in As

concentration, calculated according to the following:

Environmental Science & Technology Article

dx.doi.org/10.1021/es2021999 | Environ. Sci. Technol. 2012, 46, 4553−45594554

= −

×

percent increase (test solution concentration control

solution concentration)

/control solution concentration 100%

Twenty experiments were run with samples in triplicate orbetter. Statistically significant difference between mucilage-treated solutions and untreated controls was determined usingStudent’s t test paired two sample for means, with α = 0.1.Total Organic Carbon (TOC). Ten mL samples of 100 μg/

L As were treated with 50 mg/L GE in 15 mL centrifuge tubes.Sample aliquots were taken from the top and bottom of thetubes for TOC determination. The TOC of the bulk solutionwas calculated as the difference between TOC of the entiresolution and that of the top and bottom combined. TOC wasmeasured using a TOC analyzer TOC−V equipped with anautomatic sample injector (Shimadzu, Japan). Potassiumhydrogen phthalate standard solution was used for calibrationof the system. The TOC detection limit was 50 μg/L.Attenuated Total Reflection Fourier Transform Infra-

red (ATR-FTIR) Studies. Mucilage films were prepared tocharacterize the functional groups by Attenuated TotalReflection (ATR). Mucilage films were prepared by pipetting100 μL of a 5 g/L mucilage suspension directly onto a zincselenide (ZnSe) crystal for use with a horizontal ATR accessory(Pike Technologies, Madison WI, USA). The suspension wasallowed to air-dry before observing the spectra. Films were alsoprepared to observe the interaction of mucilage with arsenic,made from solutions containing 10 mg/L As(V) and 5 g/Lmucilage. ATR-FTIR spectra for the samples were observedusing a Nicolet 6700 spectrometer (Thermo Fisher, MadisonWI, USA), using 100 scans at a resolution of 4 cm−1. Theexperiment was repeated three times.

■ RESULTS AND DISCUSSIONEffect of Mucilage Type and Concentration. Both GE-

and NE-treated solutions showed higher concentrations of Asat the air−water interface than the control solution, shown inFigure 1. The observed increase in As concentration wasindependent of the mucilage concentration. However, bothextracts showed considerable variation in performance.The GE showed an average 14% increase in As concentration

at the air−water interface, while the NE showed an average 9%increase. Twenty experiments were run with two or moreconcentration levels for both GE and NE mucilage fractions.Each determination was done in triplicate or better. As such,more than 240 replicates are represented in Figure 1. 94% ofthe NE trials and 81% of the GE trials showed mucilage activityin transporting the As to the air−water interface. For bothextracts, 56% of the trials showed mucilage activity greater thanthe average performance of each extract. We observed thatsometimes the GE was able to separate up to 50% of the arsenicin the water, and other times, it only separated about 5%. Webelieve this variance is due to the difference in the performanceexpected in natural materials. GE showed a wider responserange and higher maximum increase of 34% than NE, whichhad a maximum increase of 17%, indicating that the increase inconcentration is extract dependent. GE was consequentlychosen for further experiments as the more reactive/responsiveextract.One probable reason for the lack of response to increasing

mucilage concentration could be that at higher concentrations,the mucilage tends to aggregate and form larger molecular

ensembles.33 Aggregation may be hindering the mucilage’sinteraction with the As (V) ions. This hypothesis requiresfurther investigation, since aggregation may also account for thesignificant variability in the mucilage performance. Further, theimplication is that lower concentrations of both GE and NEmay be more effective at transporting As(V) ions to the air−water interface, which will result in lower water treatment costsif mucilage technology is used.On a mass basis, the 14% average increase of As

concentration shown by GE with concentrations rangingfrom 5−100 mg/L converts to 2.8 to 0.14 mg As/g mucilagetransported from the bulk solution to the air−water interface.These results are comparable to some plant-based biosorbentsfor As as shown in Table 1.

These results present an unexplored interaction betweenpectic polysaccharides and metal oxyanions. Since the mucilageis not a source of As, the increase of As concentration at theair−water interface directly shows the mucilage interaction withAs.Pectins have been extensively shown to interact with metal

cations; however, interaction of cactus mucilage with As(V) hasonly been demonstrated by our group.30 In the current study,we explore how the mucilage interacts with the As (V) in orderto extend the technological application of pectins to treatingnew anionic metallic water pollutants, and give insight into howthe interaction may be optimized. The transport of the arsenicto the air−water interface is thought to occur due to an increasein the hydrophobicity of the mucilage. Our proposedmechanism is that the hydrophilic mucilage binds to the

Figure 1. As concentrations at air−water interface of mucilage-treatedsolutions relative to untreated control solutions as a function ofmucilage extract and concentration.

Table 1. Arsenic Sorption Capacity of Selected Sorbents

sorbent capacity (mg/g) source

Acacia nilotica powdered stem 50.8 34Sorghum biomass 2.765 35waste tea fungal biomass 0.55 36human hairs 0.012 37cactus mucilage 2.8 - 0.14 this study

Environmental Science & Technology Article

dx.doi.org/10.1021/es2021999 | Environ. Sci. Technol. 2012, 46, 4553−45594555

As(V) ions by using its ionizable hydroxyl, carboxyl, andcarbonyl groups. Normally, these ionizable groups would havebeen used to stabilize the mucilage in the bulk of the aqueoussolution by attracting counterions. On interaction with As thegroups are no longer available and, thus destabilized and morehydrophobic, the mucilage-As complex is repelled to the air−water interface.TOC Analysis. TOC analysis was done to determine the

distribution of the mucilage in the solutions in order todefinitively link the mucilage to the transport of As to the air−water interface. As shown in Figure 2, the TOC concentration

in the entire solution, which correlates to the total mucilageconcentration, does not change on addition of As. However,the distribution of mucilage in the solution does change in thepresence of As. We determined the TOC in the bulk solutionby subtracting the TOC of the combined top and bottom of thesolution from that of the entire solution. Figure 2 shows a largerproportion of TOC in the bulk of the control solutions than inthe mucilage-treated As solutions. This means that mucilagemigrated from the bulk of the solution primarily to the air−water interface due to the presence of As.Effect of pH. Three batch trials were run in triplicate or

better at pH 5, 5.5, 6, 7, 8, and 9 to investigate the effect of pHon the interaction between mucilage and arsenic. We chosethese pH values to reflect the pH of natural waters. Note thatpH 5.5 is the initial solution pH.As shown in Figure 3, only at pH 5.5 and 9, were small but

statistically significant differences observed between mucilage-treated solutions and nonmucilage treated controls. Further,significant difference was observed between the mucilage-treated solutions at these two pH levels. These results indicatethat solution pH does affect the interaction between the GEand arsenate and further, gives insight into the nature of theinteraction. GE, an anionic polyelectrolyte, becomes increas-ingly negatively charged with increasing pH due to ionization of−OH groups from alcoholic and carboxylic groups.16,20,33

The As(V) oxyanion is polyprotic and changes protonationlevel with pH. In weakly acidic conditions, such as pH 5.5, itexists as dihydrogen arsenate H2AsO4

−, while in weakly basicconditions (such as pH 9) it exists as hydrogen arsenateHAsO4

2−.38 Our proposed mechanism of interaction is viahydrogen bonded bridging between the protons associated withthe As species and the ionized carbonyl and carboxyl groups onthe mucilage. At lower pH, the mucilage is less ionized, butthere is a higher number of protons on the H2AsO4

−. At higherpH, the mucilage is more ionized, but the arsenate has lessprotons. The mucilage appears to work equally well in bothscenarios.The activity in these pH regions versus the lack of activity

over the pH range from 6 to 8 may be due to poorer chargetransfer while the pH is in the neutral region. The mucilage istherefore expected to perform better in solutions with higherionic strength to facilitate charge transfer.

FTIR Insight into Mucilage Interaction with Arsenic.ATR-FTIR spectra provide a chemical fingerprint of materialsby correlating their absorption frequencies with knownabsorption frequencies of bonds. The spectra of both GE andNE, shown in Figure 4, depict the characteristic groupfrequencies of pectic polysaccharides; that is, carboxylic acid,carboxylate, ether, and alcohol groups.In the GE spectrum, there are four main features: the first is

the broad band at 3350 cm−1 which corresponds to OHstretching of alcohol and carboxylic acid −OH groups involvedin intermolecular hydrogen bonding. The second is two bandsat 1609 and 1416 cm−1 corresponding to the antisymmetric andsymmetric COO− stretch characteristic of carboxylic acid salts.Third, the bands at 1250 and 1140 cm−1 correspond to C−O−C ether stretch. Lastly, two strong bands at 1140 and 1100cm−1 are due to C−O stretch of secondary alcohols and C−O−H stretch in cyclic alcohols, respectively.Significant similarities exist between the spectra of GE and

NE; however, four notable differences distinguish NE from GE.A more pronounced band is observed at 2929 cm−1 for the CHstretching. Further, NE shows the expected carbonyl COstretch at 1727 cm−1 that is absent in GE. The most intense

Figure 2. Variation in mucilage concentration (reported as TotalOrganic Carbon) with time and position in water column.

Figure 3. As concentrations at air−water interface of mucilage-treatedsolutions (GE) relative to untreated control solutions as a function ofinitial solution pH.

Environmental Science & Technology Article

dx.doi.org/10.1021/es2021999 | Environ. Sci. Technol. 2012, 46, 4553−45594556

band for NE occurs at 1041 cm−1 due to HC−O−H stretch ofcyclic alcohols. The most notable difference between the twoextracts is seen in the region 1250 to 850 cm−1. Coimbra et al.39

showed that the intensity of the bands at 1100 and 1018 cm−1

correlated with the uronic acid content of pectic polysacchar-ides; on this basis, GE is deduced to have a higher uronic acidcontent than NE.In FTIR absorbance spectroscopy, peak shifts and intensity

changes are important for inferring chemical interaction. Peakshifts signify a change in the chemical environment of afunctional group. The coupled appearance and disappearance ofabsorption bands indicate a reaction involving the correspond-ing functional group. On reaction with the As (V) oxyanion,significant changes occur in the spectra of GE and NE; shownin Figure 5. These changes indicate the participation of thecarbonyl, carboxyl, and hydroxyl functional groups in theinteraction with As (V).

The OH band of GE at 3350 cm−1 was shifted higher to 3364cm−1 indicating a change in the hydrogen bonding networkprobably due to the direct involvement of the alcohol andcarboxylic −OH groups. The 1609 cm−1 band shifted to 1640cm−1 further corroborating hydrogen bonding as an interactionmechanism.40 This shift is shown more clearly in Figure 6. Theappearance of band at 1733 cm−1 coupled with the decreasedintensity of the 1640 cm−1 band indicate that the −CO fromcarboxylic acid is the binding site for the As (V) oxyanion.Similar changes were observed in the spectrum of NE after

reaction. An analogous band at 1615 cm−1 shifted to 1645 cm−1

indicating hydrogen bonding. This band’s intensity decreasedwhile the band at 1727 cm−1 assigned to CO stretch shiftedto 1735 cm−1 and increased in intensity (see Figure 6),providing further proof that the CO group was a binding sitefor arsenate.Having established that the major functionality in the pectic

polysaccharides are carbonyl, carboxyl, and hydroxyl groups, we

Figure 4. ATR-FTIR spectra of GE before (l) and after reaction with As (r).

Figure 5. ATR-FTIR spectra of GE (l) and NE (r) after reaction with As.

Environmental Science & Technology Article

dx.doi.org/10.1021/es2021999 | Environ. Sci. Technol. 2012, 46, 4553−45594557

deduced that mucilage binds As using these groups. At thispoint, we propose it occurs through a combination ofmechanisms: hydrogen bonding between the protons of theOH groups on mucilage and O groups of arsenate, andelectrostatic attraction or complexation between the positivemetal center of As (V) and the electron-rich CO groups of themucilage on account of the tetrahedral geometry of the arsenateoxyanion.41 FTIR data show that for both GE and NE,hydrogen bonding and binding at the carbonyl and carboxylCO sites were important. Further, other researchers usingentirely different biosorbents with similar functional groupshave also reported the involvement of CO and OH groups inAs binding.35,42,43

Taken together, these findings suggest that the interaction ofthe mucilage with As increases the hydrophobicity of themucilage by occupying its ionizable groups, which would havestabilized it in the bulk of the aqueous suspension. Themucilage-As complex is consequently repelled to the air−waterinterface on account of increased hydrophobicity, resulting inthe observed increase in As at the air−water interface.In order to realize the mucilage’s potential as a complexant

for arsenic, further work is needed in designing an efficientheterogeneous contacting system which will allow easyseparation of the mucilage-As complex.

■ ASSOCIATED CONTENT*S Supporting InformationUV−vis method, discussion and figures. This material isavailable free of charge via the Internet at http://pubs.acs.org.

■ AUTHOR INFORMATIONCorresponding Author*Tel: 1 813 974 8009; fax: 1 813 974 3651; e-mail: norma@usf.edu.NotesThe authors declare no competing financial interest.

■ ACKNOWLEDGMENTSThe authors would like to acknowledge support provided fromNSF-Rapid Grants Nos. CBET-1034849 and 1057897 to

complete the work presented in this manuscript. We wouldalso like to acknowledge funding from the University of SouthFlorida Sustainable Healthy Communities Grant and financialsupport for one of the authors (DIF) from the SchlumbergerFoundation Faculty for the Future Grant. We also thank KevinYoung and Dr. Alessandro Anzalone for providing cactusmucilage and initial data for control experiments.

■ REFERENCES(1) Ahmed, M. F.; Ahuja, S.; Alauddin, M.; Hug, S. J.; Lloyd, J. R.;Pfaff, A.; Pichler, T.; Saltikov, C.; Stute, M.; Van Geen, A. Ensuringsafe drinking water in Bangladesh. Science 2006, 314 (5806), 1687−1688.(2) WHO Arsenic in Drinking Water. http://www.who.int/mediacentre/factsheets/fs210/en (September 30, 2009),(3) Schiewer, S.; Balaria, A. Biosorption of Pb2+ by original andprotonated citrus peels: Equilibrium, kinetics, and mechanism. Chem.Eng. J. 2009, 146 (2), 211−219.(4) Mata, Y. N.; Blazquez, M. L.; Ballester, A.; Gonzalez, F.; Munoz,J. A. Sugar-beet pulp pectin gels as biosorbent for heavy metals:Preparation and determination of biosorption and desorptioncharacteristics. Chem. Eng. J. 2009, 150 (2−3), 289−301.(5) Schiewer, S.; Patil, S. B. Modeling the effect of pH on biosorptionof heavy metals by citrus peels. J. Hazard. Mater. 2008, 157 (1), 8−17.(6) Schiewer, S.; Patil, S. B. Pectin-rich fruit wastes as biosorbents forheavy metal removal: Equilibrium and kinetics. Bioresour. Technol.2008, 99 (6), 1896−1903.(7) Balaria, A.; Schiewer, S. Assessment of biosorption mechanismfor Pb binding by citrus pectin. Sep. Purif. Technol. 2008, 63 (3), 577−581.(8) Arslanoglu, H.; Altundogan, H. S.; Tumen, F. Preparation ofcation exchanger from lemon and sorption of divalent heavy metals.Bioresour. Technol. 2008, 99 (7), 2699−2705.(9) Nawirska, A. Binding of heavy metals to pomace fibers. FoodChem. 2005, 90 (3), 395−400.(10) Serguschenko, I. S.; Kovalev, V. V.; Bednyak, V. E.;Khotimchenko, Y. S. A comparative evaluation of metal-bindingactivity of low-esterified pectin from the seagrass Zostera marina andother sorbents. Biologiya Morya (Vladivostok) 2004, 30 (1), 83−85.(11) Melo, J. S.; D’Souza, S. F. Removal of chromium bymucilaginous seeds of Ocimum basilicum. Bioresour. Technol. 2004,92 (2), 151−155.

Figure 6. ATR-FTIR spectra of GE (l) and NE (r) after reaction with As (expanded view of region 1500−2000 cm−1).

Environmental Science & Technology Article

dx.doi.org/10.1021/es2021999 | Environ. Sci. Technol. 2012, 46, 4553−45594558

(12) Harel, P.; Mignot, L.; Sauvage, J. P.; Junter, G. A. Cadmiumremoval from dilute aqueous solution by gel beads of sugar beet pectin.Ind. Crops Prod. 1998, 7 (2−3), 239−247.(13) Dronnet, V. M.; Renard, C.; Axelos, M. A. V.; Thibault, J. F.Characterisation and selectivity of divalent metal ions binding by citrusand sugar beet pectins. Carbohydr. Polym. 1996, 30 (4), 253−263.(14) Pehlivan, E.; YanIk, B. H.; Ahmetli, G.; Pehlivan, M. Equilibriumisotherm studies for the uptake of cadmium and lead ions onto sugarbeet pulp. Bioresour. Technol. 2008, 99 (9), 3520−3527.(15) Siew, C. K.; Williams, P. A.; Young, N. W. G. New insights intothe mechanism of gelation of alginate and pectin: Charge annihilationand reversal mechanism. Biomacromolecules 2005, 6 (2), 963−969.(16) Cardenas, A.; Goycoolea, F. M.; Rinaudo, M. On the gellingbehaviour of “nopal” (Opuntia f icus indica) low methoxyl pectin.Carbohydr. Polym. 2008, 73 (2), 212−222.(17) Amin, E. S.; Awad, O. M.; El-Sayed, M. M. The mucilage ofOpuntia f icus-indica Mill. Carbohydr. Res. 1970, 15, 159−161.(18) Goycoolea, F. M.; Cardenas, A. Pectins from Opuntia spp: AShort Review. J. Profess. Assoc. Cactus Devel. 2003, 5.(19) McGarvie, D.; Parolis, H. The mucilage of Opuntia f icus-indica.Carbohydr. Res. 1979, 69 (1), 171−179.(20) Medina-Torres, L.; Brito-De La Fuente, E.; Torrestiana-Sanchez, B.; Katthain, R. Rheological properties of the mucilagegum (Opuntia f icus indica). Food Hydrocolloids 2000, 14, 417−424.(21) Trachtenberg, S.; Mayer, A. M. Composition and properties ofOpuntia f icus-indica mucilage. Phytochemistry 1981, 20 (12), 2665−2668.(22) McGarvie, D.; Parolis, H. Methylation analysis of the mucilageof Opuntia f icus-indica. Carbohydr. Res. 1981, 88 (2), 305−314.(23) Buschmann, J.; Kappeler, A.; Lindauer, U.; Kistler, D.; Berg, M.;Sigg, L. Arsenite and arsenate binding to dissolved humic acids:Influence of pH, type of humic acid and aluminum. Environ. Sci.Technol. 2006, 40, 6015−6020.(24) Lin, H.-T.; Wang, M. C.; Li, G.-C. Complexation of arsenatewith humic substance in water extract of compost. Chemosphere 2004,56, 1105−1112.(25) Mukhopadhyay, D.; Sanyal, S. K. Complexation and releaseisotherm of arsenic in asenic-humic/fulvic equilibrium study. Aust. J.Soil Res. 2004, 42, 815−824.(26) Redman, A. D.; Macalady, D. L.; Ahmann, D. Natural organicmatter affects arsenic speciation and sorption onto hematite. Environ.Sci. Technol. 2002, 36, 2889−2896.(27) Buttice, A. L.; Stroot, J. M.; Lim, D. V.; Stroot, P. G.; Alcantar,N. A. Removal of sediment and bacteria from water using greenchemistry. Environ. Sci. Technol. 2010, 44 (9), 3514−3519.(28) Miller, S. M.; Fugate, E. J.; Craver, V. O.; Smith, J. A.;Zimmerman, J. B. Toward understanding the efficacy and mechanismof Opuntia spp. as a natural coagulant for potential application in watertreatment. Environ. Sci. Technol. 2008, 42 (12), 4274−4279.(29) Young, K.; Pichler, T.; Anzalone, A.; Alcantar, N. Mucilage ofOpuntia Ficus-Indica for Use As a Flocculant of Suspended Particulatesand Arsenic; Wiley: New York, 2008.(30) Young, K.; Anzalone, A.; Pichler, T.; Picquart, M.; Alcantar, N.In The Mexican Cactus As a New Environmentally Benign Material forthe Removal of Contaminants in Drinking Water(31) Materials Research Society Symposium Proceedings, 2006;2006.(32) Valdivia, B. C. P.; Urdaneta, B. A. S. Nopalito and cactus pear(Opuntia spp.) polysaccharides: Mucilage and pectin. Proceedings of theVth International Congress on Cactus Pear and Cochineal 2004, 728,241−247.(33) Turquois, T.; Rinaudo, M.; Taravel, F. R.; Heyraud, A.Extraction of highly gelling pectic substances from sugar beet pulp andpotato pulp: Influence of extrinsic parameters on their gellingproperties. Food Hydrocolloids 1999, 13 (3), 255−262.(34) Cardenas, A.; Higuera-Ciapara, I.; Goycoolea, F. M. Rheologyand aggregation of cactus (Opuntia f icus-indica) mucilage in solution. J.Profess. Assoc. Cactus Devel. 1997, 2, 152−159.

(35) Baig, J. A.; Kazi, T. G.; Shah, A. Q.; Kandhro, G. A.; Afridi, H. I.;Khan, S.; Kolachi, N. F. Biosorption studies on powder of stem ofAcacia nilotica: Removal of arsenic from surface water. J. Hazard.Mater. 2010, 178, 941−948.(36) Haque, N. M.; Morrison, G. M.; Perrusquia, G.; Gutierrez, M.;Aguilera, A. F.; Cano-Aguilera, I.; Gardea-Torresdey, J. L. Character-istics of arsenic adsorption to sorghum biomass. J. Hazard. Mater.2007, 145, 30−35.(37) Mamisahebei, S.; Jahed Khaniki, G. R.; Torabian, A.; Nasseri, S.;Naddafi, K. Removal of arsenic from an aqueous solution by pretreatedwaste tea fungal biomass. Iran. J. Environ. Health Sci. Eng. 2009, 4 (2),85−92.(38) Wasiuddin, N. M.; Tango, M.; Islam, M. R. A novel method forarsenic removal at low concentrations. Energy Sources 2002, 24, 1031−1042.(39) Benjamin, M. M., Water Chemistry.: Waveland Press: IL, 2002; p668.(40) Coimbra, M.; Barros, A.; Barros, M.; Rutledge, D.; Delgadillo, I.Multivariate analysis of uronic acid and neutral sugars in whole pecticsamples by FTIR. Carbohydr. Polym. 1998, 37, 241−248.(41) Vidyasagar, A.; Smith, H. L.; Majewski, J.; Toomey, R. G.Continuous and discontinuous volume-phase transitions in surface-tethered, photo-crosslinked poly(N-isopropylacrylamide) networks.Soft Matter 2009, 5 (23), 4733−4738.(42) Cotton, F. A.; Wilkinson, G. Advanced Inorganic Chemistry, 6thed.; Wiley: New York, 1999.(43) Pandey, P. K.; Choubey, S.; Verma, Y.; Pandey, M.;Chandrashekhar, K. Biosorptive removal of arsenic from drinkingwater. Bioresour. Technol. 2009, 100, 634−637.(44) Kamala, C. T.; Chu, K. H.; Chary, N. S.; Pandey, P. K.; Ramesh,S. L.; Sastry, A. R. K.; Chandra Shekhar, K. Removal of arsenic(III)from aqueous solutions using fresh and immobilized plant biomass.Water Res. 2005, 39, 2815−2826.

Environmental Science & Technology Article

dx.doi.org/10.1021/es2021999 | Environ. Sci. Technol. 2012, 46, 4553−45594559