Removal of Cadmium ions from aqueous solutions by microorganisms of activated sludge

REMOVAL OF CADMIUM IONS FROM AQUEOUS

SOLUTIONS BY MICROORGANISMS OF ACTIVATED SLUDGE

1_{Bulent Ecevit University, Department of Environmental Engineering, Zonguldak, 67100, Turkey} 2_{Gunluler Waste Collection and Recycling Company, Zonguldak, 67100, Turkey}

ABSTRACT

In this study, the utilization of dried activated sludge for removal of Cd2+ _{from aqueous solution in a batch} sys-tem was investigated. Initial pH, biosorbent dosage, con-tact time, and initial metal concentration parameters were selected to determine optimal process conditions. The bi-osorption mechanism was examined by SEM, FTIR and EDX results. The optimum conditions for Cd2+ _biosorption were found to be 6.0, 120 min., 1.2 g.L-1 _{and 80 mg.L}-1_, respectively for initial pH, contact time, biosorbent dosage and initial Cd2+ _{concentration. Langmuir and Freundlich} isotherms were used to model the biosorption equilibrium data, and it was determined that the system followed the Langmuir isotherm, and the sorption capacity of the bio-sorbent was found to be 15.43 mg.g-1_{. Biosorption} fol-lowed a pseudo-second-order rate model. Two main mech-anisms of Cd2+ _{biosorption onto the dried activated sludge} were adsorption to the C-H bonds and ion exchange with Na+_{, K}+ _{and Ca}2+ _ions.

KEYWORDS:

Cadmium removal, Biosorption, Adsorption Kinetics

1. INTRODUCTION

Wastewater discharges into the aquatic environment have been on the increase as a result of urbanization. Most of these discharges contain several toxic substances, espe-cially heavy metals. The presence of heavy metals in the environment causes major concern because of their toxicity and bio-accumulation tendency [1].

There are several techniques developed for the re-moval of heavy metals from wastewater such as chemical precipitation, solvent extraction, membrane separation, re-verse osmosis, evaporation, electrolysis and ion exchange. These techniques are not cost effective and metal recovery capacities are insufficient [2-4]. Adsorption onto activated carbon is effectively used for the removal of heavy metals. However, high regeneration costs and losses in the appli-

* Corresponding author

cation processes limit its large scale usage [3]. Many re-searchers have focused on cheap and easily applicable al-ternative materials instead of activated carbon [3]. Biomass is one of the promising alternative sorption materials due to several advantages including reduced cost, environmen-tal acceptability, regenerability and simple application [5]. For example, some biological materials (biosorbents) such as agricultural wastes, sugar beet pulp, fungi, algae, bacte-ria and yeasts can be used for heavy metal removal from industrial wastewater, effectively [5-9].

Biosorbents can be used either in alive or dead form. However, living cells suffer from heavy metals toxicity which causes cell death. Besides, COD and BOD concen-trations raise in the wastewater due to the nutrient addition in order to supply the necessary nutrient requirements of living cells [10-12]. However, dead biomass is not affected by heavy metals toxicity; it is cheap and easily controlled. In addition, non-living biosorbents can be regenerated and reused [10,13]. Therefore, dead biomass may be consid-ered more appropriate for heavy metal removal. There is a growing interest in use of activated sludge (which is mix-ture of bacteria, fungi, yeast, algae and protozoa) as a bio-sorbent [3, 7, 10, 14-16].

Biosorption processes include extracellular mass transfer of metal onto the binding regions of biomass and diffusion into the particulates. These processes are gener-ally fast and reversible [17]. Extracellular polymeric sub-stances protect living cells from metal toxicity via some mechanisms such as ion exchange, complexation with neg-atively charged groups, adsorption and precipitation [15, 17-19]. Interaction between metals and biomass is related with biopolymers of biomass or functional groups located in the cell wall. These functional groups are; carboxylic, amino, phosphate and sulphate groups [7]. Physicochemi-cal properties of these organic compounds can be modified by changing solution characteristics. Therefore, some pa-rameters such as pH, ionic strength, redox potential, metal concentration, complexing properties of anions, are known as important factors in the biosorption process [20].

Amount of adsorbate on adsorbent, at fixed tempera-ture, is a function of concentration and this function is called the adsorption isotherm. Adsorption isotherms are also representative for biosorption processes [15, 21, 22].

It is not likely to infer mechanisms of biosorption from iso-therms [17]. In order to understand the mechanisms of bi-osorption, the physical and chemical changes on the sur-face of the biosorbent also have to be understood.

Activated sludge is an abundant, freely available mat-ter because it is a by-product of wastewamat-ter treatment pro-cesses. Utilization of activated sludge can significantly re-duce the cost of heavy metal removal from wastewater. The objective of the present work is to investigate the biosorp-tion potential of the dried activated sludge for the removal of cadmium (Cd2+_{) from the aqueous solution. Optimum} biosorption conditions were determined as the function of contact time, initial pH, biosorbent dosage and the initial metal concentrations. Physical and chemical properties of biosorbent, surface structure before and after biosorption, changes in functional groups were also analyzed. In addi-tion, Langmuir and Freundlich models were used to de-scribe equilibrium isotherms. In order to define kinetic con-stants of the biosorption, Lagergren and Ho kinetic models were applied to the experimental data.

2. MATERIALS AND METHODS

2.1 Preparation of biosorbent

A reactor was set up for activated sludge production in the laboratory. The reactor was filled with 5 L of domestic wastewater and continuously aerated by air pumps. Microor-ganism production was enhanced by the addition of a nutrient solution into the reactor at a loading rate of 5 mL.L-1_.day-1_.

Microorganism growth was observed for two weeks. At the end of two weeks, two third of the activated sludge flocs was removed from the reactor and centrifuged at 3000 rpm for 5 min. More wastewater was added to remaining activated sludge in the reactor to maintain the microorganism growth. For the preparation of biosorbent, the centrifuged material was dried overnight in an oven at 60°C. It was then grounded into powder and sieved to size ≤ 150 μm. The prepared biosorbent was stored in a desiccator for all ex-periments.

2.2 Characterization of the biosorbent

Elemental composition of the biosorbent was deter-mined using Leco TruSpec (CHNS) elemental analyzer while the specific functional groups in the biosorbent were identified using PerkinElmer Frontier FTIR (Fourier Trans-form Infra-Red) spectroscopy system. The surface morphol-ogy of the biosorbent was examined using FEI Quanta FEG450 SEM/EDX (scanning electron microscopy/ en-ergy dispersive x-ray spectroscopy) system. All these anal-yses were conducted on the biomass samples before and after the adsorption process.

2.3 Biosorption experiments

Biosorption tests in this study were performed at room temperature. Stock Cd2+ _{solution used in the tests} was prepared by dissolving analytical-grade anhydrous

cadmium (II) chloride salt (Merck, Germany) in deion-ized water (18.2 µS.cm-1_{). A total of 0.05 g biosorbent in} 50 mL volume of the stock solution (initial concentrations ranged from 25 to 175 mg.L-1_{) was adjusted to desired pH} value with 1.0 mol.L-1 _{HCl and NaOH solutions, and was} agitated until equilibrium state was reached using an incu-bator shaker (Gerhardt, Germany) at 125 rpm and room temperature (25°C). Sample solution, which was in equi-librium state, was centrifuged at 5000 rpm for 20 minutes and biomass was separated from the liquid. Cd2+ _{amount in} the supernatant was analyzed by atomic adsorption spec-trophotometer (AAS) (1100B, Perkin Elmer, USA). Ad-sorbed metal quantity was calculated by the following equation:

M

C

C

V

qe

_

(



)

where qe (mg.g-1) is the equilibrium adsorption capac-ity, C0 and Ce are the initial and equilibrium concentrations (mg.L-1_{) of Cd}2+ _{in solution, V (L) is the volume and M (g)} is the weight of dry biosorbent. Removal efficiencies in the experiments were determined by the following expression:

0 0

(%)

C

C

C

Efficiency





Biosorption isotherm is an important component for the clarifying of adsorption mechanism. In order to deter-mine the equilibrium state of the biosorption, experiment results were applied to the well known Langmuir (Eq.3) and Freundlich (Eq.4) adsorption isotherms.

b

q

C

q

q

C









1

1

C

n

K

q

log

1

log

log





where ݍ௠௔௫ (mg.g-1) is the amount of Cd2+ adsorbed

per unit mass of the biosorbent, ݊, ܭ௙ (L.g-1) and ܾ (L.mg-1)

values are constants.

2.5 Biosorption kinetics

Biosorption kinetics is a useful tool to explain the fac-tors affecting sorption mechanism and efficiency. Sorption process is related with the nature of the adsorbent, physical and chemical properties of the adsorbate and operating con-ditions of the process. It is important to know the kinetics data in order to determine the effective step of the adsorp-tion [23].

In order to investigate the mechanisms of adsorption, there are numerous kinetic models such as first-order and order reversible ones, and first-order and second-order irreversible ones. On the other hand, reaction second-orders based on the capacity of the adsorbent have also been pre-sented, such as Lagergren’s pseudo-first-order equation

(Eq. 5) and Ho’s pseudo-second-order expression (Eq. 6) [24, 25].





 

303

.

2

log

log

_q

_q

_q

k

t









q

t

q

k

q

t







1

equilib-rium and at time ݐ, respectively and ݇ଵ (L.min-1) and ݇ଶ

(g.mg-1_.min-1_{) are reaction rate constants of the models,} re-spectively.

First one of these models is based on the assumption that the rate of occupation of adsorption sites is propor-tional to the number of unoccupied sites. [5] Second model assumes that biosorption capacity is proportional to the number of occupied active sites on the biosorbent. Here, rate limiting step is chemisorption. Several chemical inter-actions contribute to chemisorption such as electron shar-ing or the exchange between biosorbent and adsorbate, complexation, coordination and chelation. [26].

3. RESULTS AND DISCUSSION

3.1 Effect of the contact time

The contact time between adsorbent and adsorbate has great importance in adsorption process. In general, the bi-osorption capacity and the removal efficiency of metal ions become higher when the contact time is prolonged. In this study, to determine the effect of the contact time, Cd2+ con-centrations were analysed after biosorption experiments for different contact times (15, 30, 45, 60, 75, 90, 105, 120, 140 minutes).

The results in Fig.1 (A) showed that equilibrium was established within a contact time of 120 min. and sorption did not change with further increase of contact time up to 20 min. The probability of confrontation between Cd2+ _ions and active sites on the dry biomass increased with increas-ing contact time. Thus, concentration of Cd2+ _ions de-creased in solution at equilibrium. However, metal adsorp-tion decreased over time due to the occupaadsorp-tion of all active points or reduction in the number of unoccupied active sites. When whole capacity of the adsorbent was used, ad-sorption reached equilibrium.

Time, (min.) 0 20 40 60 80 100 120 140 Cd 2+ r e m o v a l, (C /C 0 ) 0,0 0,2 0,4 0,6 0,8 1,0 pH value 2 3 4 5 6 7 8 9 Cd 2+ r e m o v a l, ( % ) 0 20 40 60 80 100 (A) (B) Initial Cd2+ concentration, (mg.L-1 ) 0 50 100 150 200 Cd 2+ r e m o v a l, (% ) 0 20 40 60 80 100 Biosorbent concentration, (g.L-1 ) 0,0 0,5 1,0 1,5 2,0 2,5 Cd 2+ r e m o val , (% ) 0 20 40 60 80 100 (C) (D)

FIGURE 1 - Effect of contact time (Cd2+ _{= 100 mg.L}-1_{, biosorbent = 1.0 g.L}-1_{, pH = original solution pH) (A), Effect of pH (Cd}2+ _{= 100 mg.L}-1_,

biosorbent = 1.0 g.L-1_{, contact time = 120 min.) (B), Effect of initial Cd}2+ _{concentration (pH = 8, biosorbent = 1.0 g.L}-1_{, contact time = 120 min.)}

3.2 Effect of pH

The interaction between the metal ions and the func-tional groups present on the biomass depends on the nature of the biosorbent as well as the aqueous chemistry of the metal ions. It is well known that pH is one of the major pa-rameters controlling the metal sorption of the biosorbents.

In this study, the effect of solution pH on the biosorp-tion was investigated in pH range of 3.0-8.0. In the experi-ments, pH 8.0 was taken as the upper limit to avoid possi-ble hydroxide precipitation. As seen in Fig.1 (B), biosorp-tion rate of Cd2+ _{in the solution increased by increasing the} initial pH of the solution, and decreased sharply under the initial pH value 4. According to these results, it can be con-cluded that optimum initial pH range for biosorption of Cd2+ _{is between 6.0 and 8.0. The low removal efficiencies} seen under initial pH of 6 can be attiributed to competition of a large number of protons with the metal cations for ac-tive exchange sites on the biomass.

3.3 Effect of initial metal concentration

The influence of the initial Cd2+ _{concentrations on} ad-sorption was investigated by changing the concentrations (175, 150,120,100, 80, 60, 40, 25 mg.L-1_{) at the initial pH 8} and the contact time 120 min.

As it is seen from Fig.1 (C), when the initial metal con-centrations increased up to 20 mg.L-1_{, removal efficiency} increased aggressively up to 90%, and then the efficiency decreased slightly. These results can be explained on the basis that at the lower initial concentrations, metal ions eas-ily reach and bind onto the active sites but at higher con-centrations, the available active sites for the sorption

be-ome less in comparison to the moles of metal ion present in solution. [27]

3.4 Effect of biosorbent concentration

The biosorbent concentration experiments were per-formed at various biomass doses from 0.3 to 2.0 g.L-1_{. As} it is seen from Fig.1 (D), the Cd2+ _{removal efficiency} rap-idly increases from 44% to 80% by increasing used bio-sorbent dose from 0.3 to 1.2 g.L-1_{, respectively. Several} re-searchers also reported that the increase in the biosorbent dosage results in more adsorption sites which in turn leads to higher removal efficiencies [2]. In other words, the pres-ence of high amounts of biosorbent in solution causes a rapid surface biosorption. Increase in the sorption with the increase in the biosorbent dose can be attributed to in-creased sorbent surface area of mesopores and the availa-bility of more sorption sites. Thus, active sites needed for Cd2+ _{uptake can be rapidly filled. The decreasing metal} re-moval at high biosorbent dosage could be explained by considering a partial cell aggregation. This results in the three dimensional structure of the cell wall and the internal linkages between the reactive groups (COO- _{and NH}

3+), thus reducing Cd2+ _{diffusion through the structure and the} accessibility of the active sites for the sorption [28].

In this work, Langmuir and Freundlich isotherms were used to optimize biosorption process parameters. Experi-ments were carried out at initial pH 8.0, 1.2 g.L-1 bio-sorbent dose and 120 min contact time. Initial Cd2+ con-centrations varied from 25 to 175 mg.L1_{. The changes in} equilibrium concentrations for various initial metal concen-trations were given in Fig.2 and the obtained isotherm pa-rameters and correlation coefficients were listed in Table 1.

Ce 0 10 20 30 40 50 Ce / q e 0,0 0,1 0,2 0,3 0,4 Log Ce 0,2 0,4 0,6 0,8 1,0 1,2 1,4 1,6 1,8 L og q e 1,0 1,2 1,4 1,6 1,8 2,0 2,2 2,4 (a) (b)

FIGURE 2 - (a) Langmuir and (b) Freundlich isotherms for the Cd2+ _biosorption.

TABLE 1 - Langmuir and Freundlich isotherm parameters for biosorption of Cd2+ _ions.

Langmuir Isotherm Freundlich Isotherm

qmax (mg/g) b (L.mg-1) R2 Kf (L.g-1) 1/n R2

The fact that metal biosorption can be modeled by Langmuir and Freundlich model, have been identified by many researchers [3, 29-30]. Similarly, in our results seen in Fig.2, the correlation coefficients obtained from both Langmuir and Freundlich isotherms are higher than 95%. However, Langmuir model results are relatively better than the Freundlich model judging by higher R2 _{values. This} provides an initial indication that the governing mechanism is chemisorption with high possibility of monolayer ad-sorption of cadmium ions occurring on the surface of the biosorbent.

It can be concluded from the results that the governing mechanisms of Cd2+ _{biosorption by using dry activated} sludge are both chemical and physical sorptions. Phy-sisorption is a result of Van der Waals forces and adsorbed molecules are not fixed on a specific site. In contrast, chemisorption is a result of the chemical interaction with the adsorbent, and the movement of the adsorbed mole-cules is not possible [7,15]. Adsorbate that is bonded with chemisorption usually does not accumulate more than a molecular layer. Chemisorption changes only according to the specific sites and functional groups. Thus, chemisorption degree is different for each biomass. Due to the broad diver-sity of microorganisms, there is a heterogeneous structure in the activated sludge. Cadmium ions may be adsorbed by chemical or physical binding onto the heterogeneous regions of biosorbent surface as a monolayer. This explains both the surface heterogeneity and the monolayer uptake.

3.5 Biosorption kinetics

In order to investigate the adsorption kinetics of Cd2+ on the biosorbent, pseudo-first-order and pseudo-second-order models were taken into consideration.

It can be seen from the results presented in Fig.3 and Table 2 that, correlation coefficients of both kinetic models are higher than 94%. However, the use of pseudo-second-order kinetics for the Cd2+ _{sorption by dried activated} sludge may be more appropriate due to having slightly high correlation coefficient.

3.6 FTIR analysis

Fig.4 shows the FTIR spectra of biosorbent before and after adsorption of cadmium ions. The FTIR spectra of raw and experimented biomass were taken in the range of 450– 4000 cm−1 _{and functional groups responsible for the} bio-sorption were investigated.

The cell walls of microorganisms contain large mole-cules (peptidoglycan) combined with teichoic acid and pol-ysaccharides. These molecules and intracellular substances can adsorb heavy metals. Especially, functional groups such as carboxylate (COO-), hydroxyl (-OH), and others (-NH), (-C-N), (-C-O), (-C-H), (-C=O) are responsible for the sorption. Peak values on FTIR spectrum higher than 1500 define the organic bond structures that can chemically adsorb heavy metals.

Time, (min.) 0 20 40 60 80 100 120 Lo g ( q e -q t ) 0,0 0,5 1,0 1,5 2,0 2,5 a) Time, (min.) 0 20 40 60 80 100 120 t / q t 0,0 0,5 1,0 1,5 b)

FIGURE 3 - (a) Pseudo-first-order, and (b) Pseudo-second-order models

TABLE 2 - Pseudo-first-order and pseudo-second-order kinetics parameters for Cd2+ _biosorption

Pseudo-first-order Pseudo-second-order

qe (mg.g-1) 10.36 qe (mg.g-1) 9.157

k1 (min.-1) 0.38 k2 (g.(mg. min)-1 0.0038

(A)

(B)

FIGURE 4 - The FTIR spectras of biosorbent before (A) and after (B) the biosorption.

TABLE 3 - The changes in biosorbent structure before and after the biosorption study.

Analysis Before biosorption After biosorption

Multipoint BET, m2_.g-1 _(R2_{=0,99) 8,786 13,432}

Langmuir surface area, m2_.g-1 _(R2_{=0,99) 13,739 19,831}

Pore volume , cc.g-1 (for pore diameter < 1.94 nm)

2.900x10-3 _4.868x10-3

Average pore diameter, nm 1.320 1.450

Density, g.cc-1 _{2.0936 1.3236}

Cd2+_{, mg.kg}-1 _{22.560 24 060}

Elemental analysis (C-H-N-S), (%) 7.39-3.72-1.75-3.16 6.47-3.39- 1.62-3.83

Volatile solids, (%) 41 34

3.7 Surface analysis results

In order to find out the changes in biosorbent structure before and after the biosorption process, some surface and elemental analyses were conducted, and results are pre-sented in Table 3.

Both BET analysis and Langmuir analysis results in Table 3. show that the surface area, the pore volume and the pore diameter of the biosorbent increase after the sorp-tion experiments. Increase in the surface area supports the idea that adsorption occurs onto the biosorbent surface. Furthermore, increases in the pore volume and pore diam-eter also indicate the sorption of Cd+2 _{ions. According to}

these results, it can be inferred that some portion of the Cd+2 ions undergo physical adsorption onto the biomass surface. Carbon, hydrogen, nitrogen and volatile solids values given in Table 3 also decrease after the biosorption experiments. As it is seen, from the FTIR results (Fig 4.), this may be due to the binding of Cd+2 _{chemically to the adsorbate.}

Scanning electron microscopy, SEM, micrographs of the biosorbent before and after the sorption are shown in Fig. 5. As it is seen from Fig.5, before the sorption, the bi-osorbent surface appears to be rough and sponge-like which indicates a typical biomass texture. After the adsorp-tion experiment, its surface experiences a slight change in

(A) (B)

FIGURE 5 - The SEM micrographs of biosorbent before (A) and after (B) the biosorption.

(a)

(b)

FIGURE 6 – The EDX spectra of biosorbent before (A) and after (B) the biosorption.

morphology. Energy dispersive X-ray (EDX) analysis was also conducted to evaluate the adsorption of Cd2+ _{on the} biosorbent (Fig.6).

The EDX spectrum for the raw biosorbent seen in Fig.6(a) indicates the presence of sodium (Na), potassium

(K), calcium (Ca), magnesium (Mg), phosphorus (P), chlo-ride (Cl), carbon (C), and oxygen (O), but does not show the characteristic signal of Cd2+ _{ions on the surface of the} biosorbent. After the biosorption experiment, a significant amount of K+_{, Na}+ _{and Ca}2+ _{releases from the biosorbent.} As it is expected, Cd2+ _{ions detected after the biosorption}

process suggest a possible ion exchange occurrence be-tween these ions and Cd2+ _{ions. According to these} obser-vations, it can be concluded that the ion exchange mecha-nism plays an important role in cadmium uptake.

4. CONCLUSION

Based on all results, it can be concluded that dried ac-tivated sludge can be evaluated as an alternative biosorbent for treatment of Cd+2 _{containing wastewater, since it is} low-cost biomass and has a considerably high biosorption capacity. Initial pH, biosorbent concentration and removal time can be taken into account as important process param-eters. The physical and chemical sorption forces are effec-tive at the excessive Cd+2 _{accumulations on the biosorbent.} The Langmuir isotherm fits better than the Freundlich iso-therm indicating the applicability of monolayer coverage of Cd+2 _{on biosorbent surface. The pseudo-second-order} kinetic model describes the adsorption kinetics more accu-rately.

ACKNOWLEDGEMENT

This research was financially supported by the Re-search Fund of Bulent Ecevit University (Project code: 2010-45-10-01).

The authors have declared no conflict of interest.

REFERENCES

[1] Igwe, J., Abia, A. (2006) A bioseparation process for remov-ing heavy metals from waste water usremov-ing biosorbents. Afri-can Journal of Biotechnology, 5(11).

[2] Baysal, Z., Çinar, E., Bulut, Y., Alkan, H., Dogru, M. (2009) Equilibrium and thermodynamic studies on biosorption of Pb(II) onto Candida albicans biomass. Journal of Hazardous Materials, 161(1), 62-67.

[3] Wang, X., Chen, L., Xia, S., Zhao, J., Chovelon, J.-M., Re-nault, N.J. (2006) Biosorption of Cu(II) and Pb(II) from aque-ous solutions by dried activated sludge. Minerals Engineering, 19(9), 968-971.

[4] Xu, H., Liu, Y. (2008) Mechanisms of Cd2+_{, Cu}2+ _{and Ni}2+ bi-osorption by aerobic granules. Separation and Purification Technology, 58(3), 400-411.

[5] Li, X., Xu, Q., Han, G., Zhu, W., Chen, Z., He, X., Tian, X. (2009) Equilibrium and kinetic studies of copper(II) removal by three species of dead fungal biomasses. Journal of Hazard-ous Materials, 165(1–3), 469-474.

[6] Özer A., Tümen F. (2003) Cd(II) Adsorption from aqueous so-lution by actived carbon from sugar beet pulp imprenated with phosphoric acid, Fresenius Environmental Bulletin, 12(9), 1050-1058.

[7] Hammaini, A., González, F., Ballester, A., Blázquez, M.L., Muñoz, J.A. (2007) Biosorption of heavy metals by activated sludge and their desorption characteristics. Journal of Environ-mental Management, 84(4), 419-426.

[8] Kuyucak, N., Volesky, B. (1988) Biosorbents for recovery of metals from industrial solutions. Biotechnology letters, 10(2), 137-142

[9] Mohan, D., Singh, K.P. (2002) Single- and multi-component adsorption of cadmium and zinc using activated carbon de-rived from bagasse—an agricultural waste. Water Research, 36(9), 2304-2318

[10] Al-Qodah, Z. (2006) Biosorption of heavy metal ions from aqueous solutions by activated sludge. Desalination, 196(1–3), 164-176.

[11] Dilek, F.B., Gokcay, C.F., Yetis, U. (1998) Combined effects of Ni(II) and Cr(VI) on activated sludge. Water Research, 32(2), 303-312.

[12] Yan, G., Viraraghavan, T. (2000) Effect of pretreatment on the bioadsorption of heavy metals on Mucor rouxii. Water sa-pre-toria-, 26(1), 119-124

[13] Moffat, A.S. (1995) Plants Proving Their Worth in Toxic Metal Cleanup. Science, 269 (5222), 302-303

[14] Aksu, Z., Akpınar, D. (2000) Modelling of simultaneous bio-sorption of phenol and nickel(II) onto dried aerobic activated sludge. Separation and Purification Technology, 21(1–2), 87-99

[15] Arican, B., Gokcay, C.F., Yetis, U. (2002) Mechanistics of nickel sorption by activated sludge. Process Biochemistry, 37(11), 1307-1315

[16] Sağ, Y., Tatar, B., Kutsal, T. (2003) Biosorption of Pb(II) and Cu(II) by activated sludge in batch and continuous-flow stirred reactors. Bioresource Technology, 87(1), 27-33

[17] Tsezos, M., Volesky, B. (1982) The mechanism of uranium biosorption by Rhizopus arrhizus. Biotechnology and Bioen-gineering, 24(2), 385-401.

[18] Brown, M.J., Lester, J.N. (1982) Role of bacterial extracellular polymers in metal uptake in pure bacterial culture and acti-vated sludge—II Effects of mean cell retention time. Water Research, 16(11), 1549-1560.

[19] Rudd, T., Sterritt, R., Lester, J. (1984) Formation and condi-tional stability constants of complexes formed between heavy metals and bacterial extracellular polymers. Water Research, 18(3), 379-384

[20] Ledin, M., Pedersen, K., Allard, B. (1997) Effects of pH and ionic strength on the adsorption of Cs, Sr, Eu, Zn, Cd and Hg byPseudomonas putida. Water, Air, & Soil Pollution, 93(1), 367-381.

[21] Chang, D., Fukushi, K., Ghosh, S. (1995) Stimulation of acti-vated sludge cultures for enhanced heavy metal removal. Wa-ter environment research, 67(5), 822-827.

[22] Lawson, P.S., Sterritt, R.M., Lester, J.N. (1984) Adsorption and complexation mechanisms of heavy metal uptake in acti-vated sludge. Journal of Chemical Technology and Biotech-nology. Biotechnology, 34(4), 253-262.

[23] Ho, Y.S., McKay, G. (1999) Pseudo-second order model for sorption processes. Process Biochemistry, 34(5), 451-465. [24] Ho, Y., McKay, G. (1998) A comparison of chemisorption

ki-netic models applied to pollutant removal on various sorbents. Process safety and environmental protection: transactions of the Institution of Chemical Engineers, part B, 76(4), 332-340. [25] Fu, Y., Viraraghavan, T. (2000) Removal of a dye from an aqueous solution by the fungus Aspergillus niger. Water Qual-ity Research Journal of Canada, 35(1), 95-111

[26] Lesmana, S.O., Febriana, N., Soetaredjo, F.E., Sunarso, J., Ismadji, S. (2009) Studies on potential applications of biomass for the separation of heavy metals from water and wastewater. Biochemical Engineering Journal, 44(1), 19-41.

[27] Srivastava, P., Hasan, S.H. (2011) Biomass of Mucor heimalis for the biosorption of cadmium from aqueous solutions: equi-librium and kinetic studies. BioResources, 6(4), 3656-3675. [28] El-Sayed, M.T. (2012) The use of Saccharomyces cerevisiae

for removing cadmium (II) from aqueous waste solutions. Af-rican Journal of Microbiology Research, 6(41), 6900-6910. [29] Aksu, Z. (2001) Biosorption of reactive dyes by dried

acti-vated sludge: equilibrium and kinetic modelling. Biochemical Engineering Journal, 7(1), 79-84.

[30] Özer, A., Özer, D., Dursun, G., Bulak, S. (1999) Cadmium(II) adsorption on Cladophora crispata in batch stirred reactors in series. Waste Management, 19(3), 233-240.

Received: April 03, 2014 Accepted: July 30, 2014

CORRESPONDING AUTHOR Sureyya Altin

Bülent Ecevit University

Department of Environmental Engineering Zonguldak, 67100

TURKEY

Phone: +90-372-257-4010/1565 E-mail: saltin@karaelmas.edu.tr