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Biosorption of heavy metals

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Biosorption of heavy metals
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  Bahi Jalili Seh-BardanRadziah OthmanSamsuri Abd WahidFardin Sadegh-ZadehAminudin Husin Faculty of Agriculture, Department ofLand Management, Universiti PutraMalaysia, Serdang, Selangor, Malaysia Research Article Biosorption of Heavy Metals in Leachate Derivedfrom Gold Mine Tailings Using  Aspergillus fumigatus  Leachate derived from bioleaching process contains high amount of metals that must be removed before discharging the water.  Aspergillus fumigatus  was isolated from a goldmine tailings and its ability to remove of As, Fe, Mn, Pb, and Zn from aqueous solutionsand leachate of bioleaching processes was assessed. Batch sorption experiments werecarried out to characterize the capability of fungal biomass (FB) and iron coated fungal biomass (ICFB) to remove metal ions in single and multi-solute systems. The maximumsorption capacity of FB for As(III), As(V), Fe, Mn, Pb, and Zn were 11.2, 8.57, 94.33, 53.47,43.66, and 70.4mg/g, respectively, at pH 6. For ICFB, these values were 88.5, 81.3, 98.03,66.2, 50.25, and 74.07mg/g. Results showed that only ICFB was found to be moreeffective in removing metal ions from the leachate. The amount of adsorbed metalsfrom the leachate was 2.88, 21.20, 1.91, 0.1, and 0.08mg/g for As, Fe, Mn, Zn, and Pb,respectively. The FT-IR analysis showed involvement of the functional groups of the FBinthemetalionssorption.Scanningelectronmicroscopyrevealedthatsurfacemorpho-logicalchangedfollowingmetalionsadsorption.Thestudyshowedthattheindigenousfungus  A. fumigatus  was able to remove As, Fe, Mn, Pb, and Zn from the leachate of goldmine tailings and therefore the potential for removing metal ions from metal-bearingleachate. Keywords:  Bioleaching process; Fungal biomass; Metal ions; Sorption isotherm; Wastewatertreatment Received:   March 16, 2012;  revised:   May 18, 2012;  accepted:   August 2, 2012 DOI:  10.1002/clen.201200140 1 Introduction Some extraction processes for metals involving bioleaching of solidmaterials such as minerals [1–3], ore [4, 5], and wastes [6–8] havecome into use only fairly recently. Leachate derived from bioleach-ing process contain high amount of metals that must be removed before discharging the water. Chemical precipitation, ion exchange,solvent extraction, adsorption, and reverse osmosis processes arefrequently used methods to remove metals from wastewater [9].However, there are several disadvantages to these methods, suchas unpredictable metal ions removal, high capital, and operationalcost [10]. On the other hand, application of biosorption has beenexplored for three decades [11]. Biosorption, which includes heavy metal uptake by microorganisms, is a promising and attractivetechnology for heavy metal pollution control [12]. The main advan-tagesofbiosorptionarereusabilityofthebiomaterial,lowoperatingcost, short operation time, and no production of secondary com-pounds, which might be toxic [13]. Fungal biomass (FB) has beenrecognized as a promising low-cost adsorbent for heavy metalremoval from aqueous solutions [14]. Many studies have reportedthe capability of FB to adsorb cationic metal ions from solutionscontaining single or multiple solutes [15–22]. Raw untreated bio-mass may not always be effective in the removal of all heavy metals.Biomass can be pretreated using physical or chemical means withthe objective of increasing the metal biosorption capacity of the biomass [12].  Aspergillus fumigatus  was chosen as the biosorbentmaterialbecauseit is natural,easily available and thus cost-effective biomassfordissolvedmetalionsandtherelativelackofinformationrelatedtothesorptionabilitiesofthisstrain.Inordertoevaluatetheefficiency of   A. fumigatus  biomass to remediate metals contaminatedleachate derived from bioleaching of gold mine tailings the follow-ing experiments were carried out: (i) to investigate the effect of  various factors on the biosorption metal ions by FB and iron coatedfungalbiomass(ICFB),suchaspH,biomassamount,andcontacttimeinsingle-solutesystem,(ii)toinvestigatethebiosorptionofthemetalions by FB and ICFB in multi-solute system, (iii) to investigate the biosorption of the metal ions in gold mine leachate by ICFB. 2 Materials and methods 2.1 Preparation of biosorbent Fungus  A. fumigatus  (accession no. GU566217) was isolated from goldmine tailings itself [22]. The fungus was cultured by shake flask method in growth medium consisting (in g/L): sucrose (20), peptone Correspondence:  O. Radziah, Faculty of Agriculture, Department of Land Management, Universiti Putra Malaysia, 43400 Serdang, Selangor,Malaysia E-mail:  radziah@agri.upm.edu.my   Abbreviations: FTIR  , Fourier transforms infrared;  FB , fungal biomass; ICFB , iron coated fungal biomass;  PZC , point of zero charge 356  2012 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim www.clean-journal.com Clean – Soil, Air, Water 2012,  41  (4), 356–364  (10), NaCl (0.2), CaCl 2  2H 2 O (0.1), KCl (0.1), K  2 HPO 4  (0.5), NaHCO 3 (0.05), MgSO 4  (0.25), FeSO 4  7H 2 O (0.0005) [10]. The pH of the growthmedium was adjusted to 5.0 using 1N HCl before autoclaving.100mL of this medium were transferred into a series of 250-mLconical flasks and the flasks were covered with aluminum foiland subsequently autoclaved for 15min at 121 8 C and 15Ib/in 2 . The solution was allowed to cool to room temperature before it was inoculated with  A. fumigatus  strain, and shaken at a speed of 125rpmonarotaryshaker.Thebiomasswasharvestedafter5daysof cultivation by filtering through a 160-mm sieve. Then, it was washedthoroughly with deionized water until the filtrate was clear. The washed biomass was autoclaved for 30min at 121 8 C and 15Ib/in 2 ,allowedtocool,washedwithdeionizedwater,andfinallydriedinanoven at 60–70 8 C for approximately 36h. The dried biomass was thenmade into fine size powder using a mortar and pestle. The powdered biomass sieved through a 400-mm sieve, termed the FB was used for biosorption experiments. An amount of 20g of FB was given in aporcelain pot and mixed with 80mL of a solution containing 60gFe(NO 3 ) 3  9H 2 O(adjustedtopH11withNaOH).Themixturewasovendried for about 3h at 80 8 C, then raised to 110 8 C for 24h [15]. Thedried solid was washed several times with de-ionized water untilthe runoff was clear. The coated biomass was then dried at 100 8 Cand powdered in mortar and pestle. The powdered biomass residueobtained was termed ICFB. 2.2 Surface charge of fungal biomass  The net surface charge of FB and ICFB was measured by measuringtheir zeta potential ( z  ) using a zeta potential meter, ZM-77 (Zeta-Meter,NewYork,USA).Four-hundredmilligramsofFBandICFBweresuspended in 180mL of 1mM KNO 3 , and after pH adjustment withdilute HNO 3  or NaOH, the suspensions were diluted to the desiredconcentration. The pH range studied was from 2 to 9. 2.3 Preparation of metal solutions 2.3.1 Single metal solutions preparation Different metal concentrations (e.g., 25, 50, 75, 100, 150, 175, and200mg/L) were prepared from standard solutions. Standard solutionof each metal ion was prepared in buffer solutions. 2.3.2 Multiple metal solutions preparation  A multi-solute system containing a mixture of As, Fe, Mn, Pb, and Zn waspreparedusing2.5  10  4 to3.5  10  3 Mofeachmetalandthenmixed in equal proportions. 2.4 Biosorption experiment in single-solutesystem Biosorption studies were done using FB and ICFB as a function of  various parameters such as pH and time. 2.4.1 Effect of pH  The effect of pH on biosorption of As(III), As(V), Fe, Mn, Pb, and Zn(100mg/L) by the FB was studied by preparing 25mL metal solutionin buffer solutions with a pH value between 3 and 8. The buffersolution for pH 3–5 was prepared with different ratios of acetic acidandsodiumacetate[23].Trisbufferwasusedtopreparebuffersolutionhaving a pH between 6 and 8. The metal solutions were then equili- brated with 25mg of either the FB or ICFB for 6h on a rotary shaker.Subsequently, the samples were centrifuged at 9000rpm for 10min,and the supernatant was analyzed for the residual concentrations of the metal ions. The final pH values were plotted and the pH of thesolution which had the highest amount of metals adsorbed, waschosen for further batch equilibrium experiments. 2.4.2 Effect of contact time  Twenty-five milligrams of FB or ICFB was added to100-mL flaskscontaining 50mL of solution with 25, 50, 75, 100, 150, 175, and200mg of (As(III), As(V), Fe, Mn, Pb, and Zn) per liter, respectively. Allthe sorption experiments were carried out in 0.1M acetate buffersolution with optimum pH at which maximum biosorption of themetal ion occurred. The solution mixture was equilibrated on arotary shaker for 6h. Thereafter, the solution was filtered througha 0.45- m m filter membrane. Filtrates were analyzed for the concen-tration of metals ions. The results obtained in this step were appliedin the further experiments. 2.5 Adsorption isotherms  Twenty-five milligrams of FB or ICFB were added to 50mL of asolution containing 25, 50, 75, 100, 150, 175, and 200mg/L of (As(III), As(V), Fe, Mn, Pb, and Zn), respectively, in a centrifuge tube. All thesorptionexperimentswere carriedout in0.1Macetatebuffersolution at pH 6.0. The solution mixture was equilibrated on rotary shaker for 6h. After equilibration, the solution was filtered througha 0.45- m m filter membrane.Filtrates were analyzed to determine theconcentration of metals ions. The amount of metal bound by the biosorbent was calculated asfollows: Q  e  ¼ v ð C  i  C  f  Þ m  (1) where  Q  e  is the metal uptake (mg metal/g biosorbent),  v  is the liquidsamplevolume(mL), C  i istheinitialconcentrationofthemetalinthesolution (mg/L),  C  f   is the final (equilibrium) concentration of themetal in the supernatant (mg/L), and  m  is the amount of the added biosorbent on a dry basis (mg). TheLangmuirsorptionisothermhasbeenappliedfortheestimationof maximum metal uptake ( Q  max ) at different initial metal concen-trations. The Langmuir isotherm can bewritten innon-linear form as: Q  e  ¼  Q  max bC  f  ð 1 þ bC  f  Þ  (2)Here  Q  e  is the amount of metal adsorbed per unit weight of adsor- bent (mg/g),  C  f   is the equilibrium metal concentration (mg/L),  Q  max  ismonolayer biosorption capacity of sorbent, and  b  is the Langmuirconstant (L/mg). For fitting the experimental data, the Langmuirmodel was linearized as:1 Q  e ¼  1 Q  max þ  1 Q  max b    1 C  f     (3)If the adsorption data follow a Langmuir pattern, a plot of 1/ Q  e  with 1/ C  f   should yield a straight line. Constants  b  and  Q  max  can becalculated from the slope and intercept. Biosorption of Heavy Metals in Leachate 357  2012 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim www.clean-journal.com Clean – Soil, Air, Water 2013,  41  (4), 356–364  2.6 Biosorption experiment in multi-solute system  To determine the adsorption characteristics of the metal ions inmulti-solute system by FB and ICFB, the initial concentration of theeach metal ion was the same and varied between 2.5  10  4 and3.5  10  3 M. The experiments were carried out at pH 6 and the biomass concentration was fixed at 500mg/L. The experimentalprocedure was the same as that used for single solute system. 2.7 Preparation of leachate Leachate was prepared as follows; ten flasks (250mL), each contain-ing 1g of mine tailing, 100mL sucrose medium, and 1mL fungalspore suspension were shaken at 150rpm for 30 days [22]. Themixture was then centrifuged, and the supernatants were collectedand stored. The supernatant was called the ‘‘leachate’’. The color of the leachate was dark brown and its pH was 3.77. Aliquot samples of the leachate were analyzed for As, Fe, Mn, Pb, and Zn. 2.8 Biosorption of metal ions from leachatesamples using ICFB  The efficiency of the ICFB in adsorbing of As, Fe, Mn, Pb, and Zn wasdetermined in batch experiments. A volume of 45mL of the leachate was first mixed with 25mg of biomass. After adjusting the pH of thesamples to 6 using a few drops of NaOH solution (1M), the total volume was made up to 50mL and shaken for 6h. The mixture wascentrifuged, and the collected supernatant was analyzed for heavy metals. The number of times the leachate would have to be treated with fresh ICFB to achieve complete removal of the metal ions wasdetermined. A volume of 50mL of the leachate was first mixed with25mg of ICFB and left to stand for 6h. The mixture was centrifuged,and the collected supernatant was mixed with 25mg of fresh ICFB. This procedure was repeated four times. 2.9 Fourier transforms infrared (FTIR)spectroscopy of UFB and ICFB beforeand after biosorption Infrared (IR) spectra analysis of FB, ICFB, and ICFB after As(III) and As(V) adsorption, ICFB after metal ions adsorption, FB after metalions adsorption, were obtained using a Fourier transform infraredspectrometer (Perkin Elmer FTIR 1600, USA). For IR studies, 5mg of  biomass were encapsulated in 400mg of KBr. 2.10 Scanning electron microscopy of fungalbiomass  The surface morphology of biomass was visualized with a scanningelectronicmicroscope(JEOL,JSM-6400V, Japan).TheSEM enabledthedirect observation of the surface microstructures of the biomass indifferent forms. Analyses were carried out at an accelerating voltageof 20keV. 2.11 Determination of heavy metals  The metal concentrations were analyzed using graphite furnaceabsorption spectrophotometer (GFAAS, Perkin-Elmer Z5000, USA)and atomic absorption spectrophotometer (AAS Perkin-Elmer5100PC, USA). 2.12 Statistical analyses  All experimental data were subjected to ANOVA procedure anddifferences between means were determined using Tukey’s test at5%confidencelevel.ThestatisticalanalyseswereperformedwiththeStatistix statistical software package [24]. 3 Results and discussion 3.1 Surface charge of fungal biomass  The surface charge of the FB and ICFB at various pH conditions ispresented in Fig. 1. The net surface charge of FB was negative in pHrange of 3–9, which is in agreement with statement by Huang et al.[25]thatthesurfacechargeoffungalorganisms isnormallynegativeina pH range of3–10.The fungal cell wallcontainsreactive carboxylgroups, which carry negative charges. In the case of ICFB, at pH > 6,the net surface charge was negative. Loading of Fe oxyhydroxides onthe solidcanlead to the formation of goethiteandhematite orsomeother iron oxides depending on the preparation method and time[26].Thepointofzerocharge(PZC)ofironoxidesisinthepHrangeof 6–10 [27]. Therefore, it could be expected that ICFB has negativecharge in the pH range of 6–9. 3.2 Biosorption experiment in single metal system 3.2.1 Effect of solution pH It is well known that pH is a critical parameter in the biosorption of heavy metal ions [28]. The effect of pH on the biosorption of metalions by both FB and ICFB was studied at pH 3–8 and the results arepresented in Fig. 2a and b. For FB, the biosorption of As(V) decreased with increasing pH value. Maximum amount of 9.6mg/g As(v) wasachieved at pH 3. Trivalent As removal behavior was much differentfromthatobservedforAs(V),thatis,thebiosorptionofAs(III)reachedmaximum of 13.2 at pH 6.In the case of ICFB, the removal of As(V) and As(III) was maximal of 88 and 82mg/g, respectively, at pH 6 and then remained constant with increasing pH values. It can be concluded from Fig. 2 that ICFB Figure 1.  Surface charge of FB and ICFB at different pH values. Verticalbars denote standard deviation,  n  ¼ 3.358 B. Jalili Seh-Bardan et al.  2012 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim www.clean-journal.com Clean – Soil, Air, Water 2013,  41  (4), 356–364  removed higher amount As than FB. The greater removal of all As species by ICFB is due to the inclusion of Fe onto the surfaceof ICFB. Fe(III) is considered to be adsorbed on the surface of the FB by cation exchange mechanism and the As is adsorbed by the Fe(III) oxyhydroxides that is bound to the surface of FB by adsorption [29]. Arsenic species such as As(V) and As(III) tend toadsorb at oxyhydroxide surface by forming complexes with thesurface sites [30]. The adsorption is specific, which may involvethe replacement of surface hydroxyl groups by the adsorbing ligand. At a higher pH, OH  ions in the solution increase and compete withthe As(III) or As(V) ions, thereby reducing the adsorption of both As(III) and As(V) [13]. The maximum biosorption of Fe and Mn by FB was 95 and 52mg/gat pH around 7, respectively. Maximum amounts of 69mg/g Zn and38mg/g of Pb were removed at pH 6. In the case of ICFB, the maxi-mum biosorption of Fe, Mn, Pb, and Zn was 98, 60, 53, and 73mg/gat pH 6 was achieved by FB. The results show that for both FB andICFB, as the pH of the solution increased the removal of cationicmetal ions increased and they reached a maximum value at pH 6–7.On the other hand, there was a slight decrease in metal ion removalat pH 8. This was due to the decreasing competition between protonand metal species for the surface sites as the positive surface chargedecreased [9]. The slight decrease in metal removal at pH 8 could bedue to metal hydroxides precipitation. Based on these results, pH 6 was used in the following studies. 3.2.2 Effect of contact time Kinetic experiments were conducted to determine the equilibriumtime required for the uptake of metal ions by the FB. The metalconcentrations were analyzed at different time intervals. The bio-sorption of the metals at different times are shown in Fig. 3. The biosorption of As(III) and As(V) using FB increased slowly astime passed and reached saturation in 4h. For ICFB, the saturationlevel of As(III) and As(V) were reached at about 2h. Adsorption of Asspecies was low for FB and exhibited negligible increase with time.Biosorption of Fe, Mn, Pb, and Zn increased rapidly to about 1hand thereafter rose slowly before attaining saturation value in 4h, when FB was used. The amount of adsorbed metals in the first hour was 81, 66, 20, and 81% of maximum biosorption of Fe, Mn, Pb, andZn, respectively. For ICFB, Fe biosorption kinetic was faster in theinitial stage and 90% of maximum biosorption of Fe was achievedduring first half-hour and equilibrium time was 2h. In the case of Mn, Pb, and Zn about 83, 55, and 88% of maximum biosorption,respectively, was achieved within 1h and the equilibrium timeneeded for biosorption of Mn, Pb, and Zn by ICFB was 3h. Theplotsshow that kineticsofbiosorptionofmetalionsconsistedof two stages; fast stage of binding process which is due to equi-librium uptake and slow stage of binding process which couldcontributeto relativelysmallamountoftotalmetalbiosorption[10]. The equilibrium times reported in the previous literature varied widely, depending on the biosorbent systems. For example, Say et al.[11] studied the biosorption of Cd, Pb, Hg, and As(III) on  Penicillium purpurogenum . They found that equilibrium was achieved in 4h for Figure 2.  Effect of pH on adsorption of metal ions on the FB (a) andICFB (b) from aqueous solutions: initial concentration of heavy metal ion,100mg/L; biomass concentration 500mg/L. Vertical bars denote standarddeviation,  n  ¼ 3. Figure 3.  Effect of biomass concentration on adsorption of metal ions ontheFB(a)andICFB(b)fromaqueoussolutions:atoptimumpHvaluesandinitial concentration of metal ion, 100mg/L. Vertical bars denote standarddeviation,  n  ¼ 3.Biosorption of Heavy Metals in Leachate 359  2012 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim www.clean-journal.com Clean – Soil, Air, Water 2013,  41  (4), 356–364  all metals ions. Sathishkumar et al. [31] reported that the equi-librium time for As(III) in Fe-treated  A. fumigatus  biomass and auto-claved biomass was 2.25 and 2.5h, respectively. They found a 2.5-hequilibrium time for As(V) with both  A. fumigatus  biomass and auto-claved biomass. Murugesan et al. [32] investigated As biosorption with pretreated waste tea FB. They reported that Fe-treated andautoclaved FB removed 100% of As(III) after 30min contact timeand 77% of As(V) after 90min contact time. Equilibrium timerequired by   Aspergillus niger   biomass was 8h for Pb, Cd, Cu, andNi[10].Severalparametersdeterminetheequilibriumsorptiontime,such as agitation rate, physical properties of the adsorbent, amountof sorbent, properties of in sorbate-ions, initial concentration of sorbate, and presence of competing ions[11]. Therefore, it is difficultto compare the adsorption rates reported. An equilibration time of 6hwas usedinfurtherbiosorptionexperiments, toensurecompleteachievement of equilibrium. 3.2.3 Adsorption isotherms Figures 4and 5 show thebiosorptioncapacityof As(III),As(V), Fe, Mn,Pb, and Zn onto the FB and ICFB. For both biosorbent, biosorptioncapacity of the biomass first increased with increasing the equi-librium concentration of metal ions and reached a saturation value which was around 100mg/L for all heavy metal species. This can beattributed to the high availability of metal ions at the solution/ biomass interface, which in turn results in enhanced adsorptioncapacity.Whenthesurfaceactivesiteshavebeencompletelycovered with metal ions, the adsorption has reached a limit, which can bedescribed by the maximum biosorption capacity. The values of   Q  max (mg/g biomass) and  b  (L/mg) for the various metal studied are: As(III):11.2, 0.12; As(V): 8.57, 0.026;Fe: 94.33, 0.33; Mn: 53.47, 0.14; Pb: 43.66,0.03; and Zn: 70.4, 0.13, respectively, for FB. For ICFB, the values of  Q  max  (mg/g dry biomass) and  b  (L/mg) were estimated to As(III): 88.5,0.36; As(V): 81.3, 0.19; Fe: 98.03, 0.32; Mn: 66.2, 0.16; Pb: 50.25, 0.04;and Zn: 74.07, 0.24, respectively. A higher value of   Q  max  implies higher uptake by the biomass. A large value of   b , the affinity constant, is desirable. Therefore,consideration of   Q  max  together with  b  establishes the trend in metaluptake, namely: Fe > Zn > Mn > Pb >  As(III) >  As(V) for FB andFe >  As(III) >  As(V) > Zn > Mn > Pb for ICFB. This study showed that the  Q  max  values for As(III) and As(VI) withICFBweresignificantlylargerthanthecorrespondingvalueswithFB. The  Q  max  values with ICFB increased slightly for Fe, Mn, Pb, and Zn, when ICFB. The higher removal of As species from solution usingICFB may be due to reaction with iron oxides. Trivalent As isstable at pH 0–9 as neutral H 3  AsO 3 , while H 2  AsO 3  , HAsO 32  , and AsO 33  exist as stable species in the pH intervals of 9–12, 12–13, and13–14, respectively. For pentavalent As, the corresponding stablespecies and pH values are: H 3  AsO 4  (pH 0–2), H 2  AsO 4  (pH 2–7),HAsO 42  (pH 7–12), and AsO 43  (pH 12–14) [23]. At pH 6, As(V) may  be adsorbed on ICFB ( > SOH) through the following reactionsince H 2  AsO 4  is predominant: > SOH þ 3H 2  AsO 4  þ 2H þ !  > S ð H 2  AsO 4 Þ 3 þ 2H 2 OIn the case of As(III) removal using ICFB, could be shown as below,since H 3  AsO 3  is predominant: > SOH þ H 3  AsO 3 þ 2H þ !  > S ð H 2  AsO 3 Þþ 2H 2 ORegarding Fig. 1, in the solution with a pH of 6 and higher, thesurfaceactivesitesaredeprotonated,resultinginnegativelychargedsites and the adsorption of metal cations on iron oxide couldpossibly take place via electrostatic interaction with the negatively charged sites on iron oxide surface [33]. The difference in the amount of cationic metal ions adsorbedcould be due to the difference in the hydrated ionic radii in thesolutions [34]. Ions having a smaller ionic radius could be morequickly adsorbed onto a fixed area of adsorbent [35]. The presentstudy reveals that in the single metal solution, the biosorption of Fe bythebiomasswasgreaterthanthatoftheothermetals.Ionicradiusof Fe (63pm) was the smallest followed by Zn (88pm), Mn (89pm), Pb(133pm). Ionic radius based on higher biosorption of Fe followed by other metals agreed well with the findings of [35]. Say et al. [11] used  P. purpurogenum for heavymetaladsorption. Themaximumamountsof adsorption achieved was 35.6mg/g for As(III), 70.4mg/g for Hg,110.4mg/g for Cd, and 252.8mg/g for Pb at initial metal concen-tration of 500mg/L. Sag and Kutsal [36] used  Zoogloea ramigera  micro-organisms for heavy metal adsorption. The maximum adsorption of Pb was 86.9mg/g Pb dry weight of   Z. ramigera  at initial Pb concen-tration of 200mg/L. Ozer et al. [37] investigated the biosorption of Fe(III), Pb, and Cd ions onto dry mycelium of   Rhizopus arrhizus .Maximum adsorption was found to be 78mg/g for Fe(III), 71mg/gfor Pb, and 62mg/g for Cd. Figure 4.  Effect of initial metal ion concentration on As(III), As(V), Fe, Mn,Pb, and Zn adsorption by FB. Vertical bars denote standard deviation, n  ¼ 3. Figure 5.  Effect of initial metal ion concentration on As(III), As(V), Fe, Mn,Pb, and Zn adsorption by ICFB. Vertical bars denote standard deviation, n  ¼ 3.360 B. Jalili Seh-Bardan et al.  2012 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim www.clean-journal.com Clean – Soil, Air, Water 2013,  41  (4), 356–364
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