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Chromium and cobalt sequestration using exopolysaccharides produced by freshwater cyanobacterium Nostoc linckia
Ecological Engineering 82 (2015) 121–125
Contents lists available at ScienceDirect
Ecological Engineering journal homepage: www.elsevier.com/locate/ecoleng
Short communication
Chromium and cobalt sequestration using exopolysaccharides produced by freshwater cyanobacterium Nostoc linckia Sharma Mona a , Anubha Kaushik b, * a b
Amity Institute of Environmental Toxicology, Safety and Management, Amity University Uttar Pradesh, Noida, 201313, India University School of Environment Management, Guru Gobind Singh Indraprastha University, New Delhi, India
A R T I C L E I N F O
A B S T R A C T
Article history: Received 11 September 2014 Received in revised form 24 February 2015 Accepted 5 April 2015 Available online 16 May 2015
This study investigated biosorption of chromium(VI) and cobalt(II) by exopolysaccharides (EPS) of a freshwater cyanobacterium, Nostoc linckia HA-46 from aqueous solution. Experiments were performed in batch mode to determine the adsorption dynamics of the cyanobacterial EPS. The adsorption capacity for Cr(VI) and Co(II) ions by EPS is found to be dependent on pH, contact time and initial metal ion concentration. The uptake kinetics of the metal ions follow pseudo-second order model. The maximum adsorption coefficient of determination (0.993Cr and 0.997Co) for Langmuir model indicates best fitness of this model in explaining the sorption as a multilayer process. The maximum adsorption capacities of the EPS were 14.3 mg Cr g1 (at pH 2.0) and 17.9 mg Co g1 (at pH 4.0) at an initial concentration of 20 mg L1. The EPS of Nostoc linckia shows better biosorption capacity for Co(II) than Cr(IV) metal ion. ã 2015 Elsevier B.V. All rights reserved.
Keywords: Exopolysaccharide Nostoc linckia Chromium Cobalt Biosorption Kinetics Adsorption isotherms
1. Introduction Accumulation of various toxic metals in wastewaters and aquatic bodies due to mining activities, tannery, dye and pigments, chemical fertilizers, pesticide and electroplating industries along with municipal sewage disposal has concerned general public (Das et al., 2008). Most heavy metals are toxic and sometimes carcinogenic, posing a serious threat to aquatic life and the humans (Hanif et al., 2009). Removal of heavy metals from wastewater has recently become the subject of considerable interest (Rzymski et al., 2014) owing to strict legislations. Chromium(VI) used in tannery, textile and electroplating is toxic to living organisms and is carcinogenic in nature (Mona et al., 2011a). Heavy exposure of Cr(VI) causes cancer in the digestive tract and lungs and may cause epigastric pain, nausea, vomiting, severe diarrhea and hemorrhage. Cobalt is used in manufacturing glasses and ceramics and in various metallurgical processes. Being an essential component of vitamin B-12, it is beneficial in trace amount, but at higher concentrations, cobalt becomes hazardous to respiratory and cardiovascular systems, and may cause coma or death (Mayflor, 2009). The ability of biological materials to adsorb rul et al., 2008; Mona et al., 2011b) has metal ions and dyes (Ertug received considerable attention for the development of an
* Corresponding author. Tel.: +91 11 25302362; fax: +91 11 28035243. E-mail address: [email protected] (A. Kaushik). http://dx.doi.org/10.1016/j.ecoleng.2015.04.037 0925-8574/ ã 2015 Elsevier B.V. All rights reserved.
efficient, clean and inexpensive technology for wastewater treatment. Exopolysaccharides (EPS) originating from bacteria, cyanobacteria, algae (Sharma et al., 2008) and fungi are recommended as surface active bioagents for toxic metal sequestration (Parker et al., 2000). A large number of cyanobacteria are characterized by the presence of exocellular polysaccharidic layers possessing mechanical and physicochemical stability with high degree of cross linking among the polysaccharide chains (Hoiczyk and Hansel, 2000). EPS-producing cyanobacteria have been considered very promising as chelating agents for the removal of positively charged metal ions from water solutions, owing to the presence of a large number of negative charges on the external cell layers (De Philippis and Micheletti, 2009). The aim of the present investigation was to quantify EPS produced by a freshwater cyanobacterium, Nostoc linckia in response to moderate concentrations of Cr(VI) and Co(II) in aqueous medium and study the biosorptive potential of the EPS for these metal ions. The species has earlier been reported (Kiran et al., 2004) as a very good biosorbent for removal of Cr(VI) from aqueous solutions. 2. Materials and methods 2.1. Cyanobacterial culture and EPS N. linckia HA-46 was isolated from metal contaminated wastewater collected from within the premises of a textile mill in Haryana, India, various characteristics of which are: pH 8.0,
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electrical conductivity 5.0 dS m1, total dissolved solids 1500 mg L1, total hardness 500 mg L1 (as CaCO3), chloride 1500 mg L1, phosphate 2.0 mg L1, Cr(VI) 5.0 mg L1, Co(II) 2.5 mg L1. Monoculture of the cyanobacterium, shown in Fig. 1A, was obtained using standard culturing and purification techniques as described earlier (Mona et al., 2011c). The cultures were grown for 15 days in BG-11 medium spiked with different concentrations (5, 10, 20, 40 and 80 mg L1) of Cr(VI) and Co(II). The cyanobacterial culture was subjected to centrifugation (800 g) on 14d and after separating the settled biomass, the supernatant (containing EPS) was used as biosorbent for removal of Cr(VI) and Co(II) in batch mode. 2.2. Metal biosorption studies Various metal concentrations were prepared from stock solution of 1000 mg L1 Cr(VI) (AR grade potassium dichromate) and Co(II) (AR grade cobaltous nitrate). Batch studies were performed to determine the sorption equilibrium for Cr(VI) and Co(II) onto the cyanobacterial EPS (estimated by the method of Seifter et al., 1959) serving as biosorbent. Cell-free culture (100 ml) containing EPS was taken in triplicate for the two metal ions (20 mg L1) at varying pH (1–6). The flasks were shaken for 2 h at 100 rpm at 25 C on an orbital shaker (Orbitek LT-IL). After optimizing the pH for maximum removal, which was found 2.0 and 4.0 for Cr(VI) and Co(II), respectively, studies were conducted for determining the optimum contact time. Stock solutions of the two metals (1000 mg L1) potassium dichromate/cobaltous nitrate were prepared and diluted to get desired concentrations (10–100 mg L1) of the metal ions. Equilibrium time required for the maximum metal adsorption (20 and 50 mg L1 initial
concentration) was determined by agitating 100 mL of each of the metal solution at its respective optimal pH, in 250-mL Erlenmeyer flasks on an orbital shaker (Orbitek LT-IL) at 25 C for 180 min at 100 rpm. Samples were withdrawn at fixed time intervals from the flasks and analyzed on atomic absorption spectrophotometer (Shimadzu AA6300) for residual concentration of chromium/cobalt in the aqueous solution. Equilibrium studies were performed using different initial metal ion concentrations (10–100 mg L1) at optimal pH and contact time. Amount of metal adsorbed, qewas calculated as: qe(mg/g) = V(Co – Ce)/m, where Co is initial metal concentration (mg L1), Ce the equilibrium concentration (mg L1), V the volume of metal solution (L) and m is the mass of EPS (g). Percent removal was calculated as the ratio of difference in initial and final metal concentration (Co Ce) to initial concentration (Co): R (%) =
C o C e Co
100. Residual concentration of Cr(VI) and
Co(II) ions in the synthetic solution was analyzed using anatomic absorption spectrophotometer (Shimadzu AA6300). To understand the mechanism of biosorption, different isotherms like Langmuir (Langmuir, 1918), Freundlich (Freundlich and Helle, 1939), BET (Brunauer et al., 1938), Temkin (Hosseini et al., 2003), Flory–Huggins (Horsfall and Spiff, 2005), and Dubinin–Radushkevich model (Dubinin, 1960) were applied to the equilibrium data (Table 1), as explained in detail earlier (Kiran and Kaushik, 2008). Surface morphology of the dry adsorbent before and after exposure to Cr(VI) and Co(II) were studied by Scanning electron microscope (Philips PSEM 515). Dry samples were mounted on stubs and coated with gold palladium of thickness 100–1500A and then transferred to the sample chamber of instrument. This was operated at 15 KV and current density of 15 pA.
Fig. 1. Micrograph of Nostoc (A) and scanning electron micrographs of unloaded (B), Cr(VI)-loaded (C) and Co(II)-loaded (D) EPS of Nostoc linckia.
S. Mona, A. Kaushik / Ecological Engineering 82 (2015) 121–125
3. Results N. linckia showed increased production of EPS when exposed to moderate metal ion concentration (40 mg L1), but production of EPS declined when metal concentrations increased to 80 mg L1, particularly, in case of Cr(VI). The cyanobacterium produced about 40% more EPS in the presence of cobalt as compared to that of chromium (Fig. 2), which needs to be investigated further. Removal of metal ions by EPS of N. linckia was found to be pHdependent and for both the ions acidic pH favored more removal. Biosorption was maximum at pH 2.0 and 4.0 for Cr(VI) and Co(II), respectively, while lower pH of 1.0 as well as higher pH of 6.0 were less favorable (data not shown). pH higher than 6 was avoided as hydroxide formation and precipitation are reported to interfere with removal of metal ions (Aksu et al., 2002). 3.1. Biosorption kinetics Biosorption experiments of the two metal ions by EPS of the cyanobacterium as a function of contact time (5– 180 min) for two initial metalconcentrations (20 and 50 mg L1) were performed at the pH optimized for the two metals. At both the concentrations, metal removal increased with increasing contact time till 120 min for Cr and 135 min for Co, and then equilibrium was attained. At equilibrium, Cr and Co adsorption were 15.4, 17.1 mg g1 and 7.8, 43.2 mg g1at 20 and 50 mg L1 initial metal concentrations, respectively. Assuming the biosorption capacity of cyanobacterial EPS for Cr(VI) and Co(II) to be directly proportional to the number of active sites occupied on the sorbent, Lagergren rate equation (Lagergren, 1898) was applied. Rate constants for adsorption of the metal was determined using pseudo first order and pseudo second order equations as shown below: Logðqe qt Þ ¼
dq logqe k1 t and ¼ k2 ðqe qt Þ2 2:303 dt
(1)
where qe,qt are metal ion sorbed (mg g1) at equilibrium at any time (t), k1 is Lagergren rate constant (min1), k2 pseudo second order constant (g mg1 min1), respectively. A linearized form of the equation becomes: t/q = 1/k2qe2 + 1/qet
123
better to pseudo second order model. The values of all the parameters viz., k1, k2 and qe calculated from the slope and intercept of plots are represented in Table 2. The experimental values of qe when compared with theoretical values of qe obtained from the second order kinetic model and the R2 values showed validity of the pseudo second order kinetic model. Values of qe calculated from the first order kinetic model by plotting log (qe qt) versus t was much different from the experimental value of qe, thus diminishing the application of first order model for the present system (Table 2). 3.2. Equilibrium models Six two-parameter models were used to explain the sorption equilibrium data, various parameters of which are depicted in Table 1 and discussed below: 3.2.1. Langmuir isotherm The equilibrium data was fitted to Langmuir isotherm, which is represented as: qe = QobCe/(1 + bCe) where qe is the amount of metal adsorbed (mg g1), Ce is the residual metal (Cr(VI) or Co(II)) concentration (mg L1), Qo (mg g1) and b (L mg1) are Langmuir constants showing the adsorption capacity and energy of adsorption, respectively (Langmuir, 1918). Linear plot obtained from Langmuir isotherm and the values of Langmuir constants (Qo and b) calculated from the intercept and slope of the plot are presented in the Table 2. The EPS showed very high adsorption capacity (Qo = 183.3 and 194.4 mg g1 for Cr(VI) and Co(II), respectively (Table 1). Separation factor (RL), a dimensionless constant was also calculated to examine the favorability of adsorption using the equation RL = 1/(1 + bCo), where Co is the initial metal ion concentration (mg L1). This parameter explains the isotherm as follows: RL > 1 unfavorable, RL = 1 linear, 0
(2)
The linear plot of t/q versus t showed better fitness of data for both the metals at 20 and 50 mg L1 concentrations as compared to the plot log (qe qt) versus t indicating that the sorption data fits
1
Fig. 2. Production of EPS (mg g biomass) in response to varying concentration of Cr(VI) and Co(II) by Nostoc linckia.
Table 1 Isotherm constants of two parameter models for Cr(VI) and Co(II) biosorption on EPS of N. linckia. Isotherm
Parameters
Langmuir
Qo (mg g1) b (L mg1) R2
183.3 0.198 0.9934
194.4 0.231 0.9965
Freundlich
Kf (mg g1) n R2
50.1 3.12 0.7436
53.4 4.32 0.8121
Temkin
a (L g1) b (kJ mol1) R2
3.13 0.089 0.9432
3.87 0.094 0.9767
Flory–Huggins
KFH nFH DG0 (kJ mol1) R2
1112.4 4.87 19.6 0.9549
120.7 5.21 20.1 0.9656
Dubinin–Radushkevich
qD (mg g1) BD (mol2 kJ2) E (kJ2 mol2) R2
191.3 0.51 1.16 0.9611
193.3 0.61 1.32 0.9767
BET
qmax (mg g1) B (L mg1) R2
181.5 2.9 104 0.9888
191.84 3.2 104 0.9898
Cr(VI)
Co(II)
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Table 2 Kinetic model parameters for metal adsorption on EPS at 20 and 50 mg/L initial metal concentration. Initial metal concentration (mg L1)
Experimental qe(mg g1)
First order model
Second order model
Theoretical qe (mg g1)
K1 (min1)
R2
Theoretical qe (mg g1)
K2 (mg g1 min1)
R2
Cr(VI) 20 50
15.4 37.8
6.19 30.21
0.0451 0.0521
0.8989 0.9112
17.32 44.3
2.113 13.21
0.9986 0.9998
Co(II) 20 50
17.12 43.23
9.65 27.67
0.0531 0.0711
0.6988 0.764
16.87 39.87
2.321 5.121
0.9787 0.9989
3.2.2. Freundlich isotherm This isotherm assuming a heterogeneous surface of the adsorbent, was applied to equilibrium data in the form of the equation Log qe = Log Kf + 1/n (Log Ce), where qe is metal adsorbed (mg g1), Ce is residual metal ion concentration (mg L1), Kf is Freundlich constant indicating adsorbent capacity (mg g1 dry weight) and n is Freundlich exponent (Table 1) known as adsorbent intensity (Freundlich and Helle, 1939). A linear plot of Log qe versus Log Ce explained the applicability of this isotherm for the biosorbent, indicated by high values of Kf (50.1 and 53.4 for Cr and Co, respectively). 3.2.3. Temkin isotherm Temkin isotherm is based on the assumption that fall in the heat of sorption is more linear rather than logarithmic, as provided in Freundlich equation (Aharoni and Ungarish, 1977). It was suggested that due to sorbent and sorbate interactions, the heat of sorption of all the molecules in the layer would reduce linearly with coverage (Hosseini et al., 2003) in the form of equation ln (aCe), where b is the Temkin constant related to the heat of qe = RT b sorption (kJ mol1), R is the gas constant (0.0083 kJ (mol K)1), a is the Temkin isotherm constant (L g1), and T the absolute temperature (K), qe is the amount of metal adsorbed (mg g1), Ce is the residual metal ion concentration (mg L1). From the curve plotted between qe and lnCe, constants a and b were calculated and shown in Table 1. 3.2.4. Flory–Huggins isotherm This model was applied to assess the degree of surface coverage of the sorbate on the sorbent. The linearized form of the model u = LogK + n Log (1 u )where (Horsfall and Spiff, 2005) is: Log Ce FH FH Ce is the residual metal concentration (mg L1), KFH is Flory– Huggins model equilibrium constant, nFH is the Flory–Huggins model exponent and u = (1 Ce/Co) is degree of surface coverage. Values of KFH and nFH calculated from the slope and intercept of the linear plot and shown in Table 1. High R2 values shows the excellent applicability of the model. The Gibbs free energy of spontaneity (G0) was calculated as DG0 = RT lnKFH. The negative value of G0 (19.6 for Cr and 20.1 for Co) obtained for the biosorption of Cr (VI) and Co(II)) onto the cyanobacterial EPS (Table 1) shows feasibility and spontaneous nature of the process. 3.2.5. Dubinin–Radushkevich isotherm According to this model, the sorption curve depends on the porous structure of the sorbent and linear form of the isotherm is: 1 ), where qD (mg g1) and BD qe = qD exp(BDED2); ED = RT ln(1 + Ce 2 2 (mol KJ ) are the Dubinin–Radushkevich model constants and ED is the Polanyi potential. p The mean energy of sorption was calculated as: E = 1/ 2BD. The 2 values of both the constants along with R (Table 1) are high for the adsorbent showing good fitness of the isotherm. The energy value
for biosorbent is very low (1.16 and 1.32 kJ2 mol2 for Cr(VI) and Co (II), respectively) indicating weak interaction of the metal with the present sorbent. 3.2.6. Brunauer, Emmer & Teller (BET) model This model assumes that first layer of sorbate molecules adsorbs on the surface with energy comparable to the heat of adsorption for monolayer sorption and the subsequent layers have equal energies (Brunauer et al., 1938) explained as: qe = Bqmax C e , where Cs is saturation concentration of solute C ðCe C s Þ½1þðB1Þ
e Cs
(mg L1) and B is a constant related to energy of adsorption. Values of qmax and B calculated from the plot are shown in Table 1. High R2 shows applicability of the model to our data. Though all the applied models explained the sorption data well, the Langmuir model is best fitted. The scanning electron micrographs of EPS of the cyanobacterium (Fig. 1B–D) reveal its porous nature along with depressions and grooves on the surface (Fig. 1B), indicating availability of abundant binding sites for the biosorption of Cr(VI) and Co(II)). Binding of the metal ions on the surface of EPS is clearly visible as white encrustations over the pores in the SEM for both the metals (Fig. 1 C and D). 4. Discussion Most cyanobacterial exopolysaccharides are characterized by the presence of various functional groups that help in chelating ions (De Philippis et al., 2001). A wide variety of cyanobacterial genera have been documented for EPS synthesis and metal adsorption properties (Sharma et al., 2008; Chakraborthy et al., 2011; Gupta and Rastogi, 2008; Ozturk et al., 2009). Interaction between metallic cations and negative charge of acidic functional groups of EPS are favored at low pH. Decreased solubility of metal complexes in solution with increasing pH (Vijayaraghavan and Palanivelu Velan, 2006) could also result in low biosorption at high pH. Decrease in adsorption capacity of EPS at pH higher than 2 for Cr is explained by the fact that due to the exposure of more negatively charged functional groups, negatively charged chromate ions (HCrO4, CrO7, Cr4O132 and Cr3O102) present in solution are repelled (Aksu et al., 2002; Gardea-Torresdey et al., 2000). A net positive charge at pH 2, due to protonation of functional groups and presence of hydronium ions around the surface, further facilitates the adsorption of negatively charged hexavalent chromate ions (Kiran and Kaushik, 2008; Matheickal et al., 1991; Fourest et al., 1994). Sorption of the metal was relatively more rapid suggesting the involvement of a passive process like physical adsorption or ion exchange on the surface of the cyanobacterial EPS during the initial period. This was followed by a steady and slow stage that is likely to be associated with some active energy mediated process. The metal removal process seems to involve physisorption. Typical bonding energy range for ion-
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exchange mechanism is reported to be in the range of 8–16 kJ mol1 while physisorption processes are reported to have adsorption energies less than 40 kJ mol1 (Zafar et al., 2007). 5. Conclusion Production of EPS by N. linckia is stimulated by Co(II) and Cr(VI) and it has excellent biosorption potential for both the metals, but more so for cobalt as indicated by SEM images and the qmax values obtained from adsorption isotherms. Acknowledgements This work was financially supported by a grant of UGC-SAP (DRS-II) and Senior Research Fellowship to the author from CSIR, New Delhi. References Aharoni, C., Ungarish, M., 1977. Kinetics of activated chemisorption. Part 2 theoretical models. J. Chem. Soc. Faraday Trans. 73, 456–464. Aksu, Z., Acikel, U., Kabasakal, E., Tezer, S., 2002. Equilibrium modeling of individual and simultaneous biosorption of chromium(VI) and nickel(II) onto dried activated sludge. Water Res. 36, 3063–3073. Brunauer, S., Emmer, P.H., Teller, E., 1938. Adsorption of gases in multimolecular layers. J. Am. Chem. Soc. 60, 309–319. Chakraborthy, N., Banerjee, A., Pal, R., 2011. Accumulation of lead by free and immobilized cyanobacteria with special reference to accumulation factor and recovery. Bioresour. Technol. 102, 4191–4195. Das, N., Karthika, P., Vimala, R., Vinodhini, V., 2008. Use of natural products as biosorbent of heavy metals an overview. Nat. Prod. Radiance 7 (2), 133–138. De Philippis, R., Micheletti, E., 2009. Heavy metal removal with exopolysaccharidesproducing cyanobacteria. In: Shammas, N.K., Hung, Y.T., Chen, J.P., Wang, L.K. (Eds.), Heavy Metals in the Environment. CRC Press, Boca Raton, pp. 89–122. De Philippis, R., Sili, C., Paperi, R., Vincenzini, M., 2001. Exopolysaccharideproducing cyanobacteria and their possible exploitation. J. Appl. Phycol. 13 (4), 293–299. Dubinin, M.M., 1960. The potential theory of adsorption of gases and vapors for adsorbents with energetically non-uniform surface. Chem. Rev. 60, 235–266. rul, S., Bakır, M., Donmez, G., 2008. Treatment of dye-rich wastewater by an Ertug immobilized thermophilic cyanobacterial strain: Phormidium sp. Ecol. Eng. 32 (3), 244–248. Fourest, E., Canal, C., Roux, J.C., 1994. Improvement of heavy metal biosorption by mycelial dead biomass (Rhizopusarrhizus, Mucormieheiand Penicillumchrysogenum): pH control and cationic activation. FEMS Microb. Rev. 14, 325–332. Freundlich, H., Helle, W.J., 1939. Ubber die adsorption in Lusungen. J. Am. Chem. Soc. 61, 2–28. Gardea-Torresdey, J.L., Tiemann, K.J., Armendariz, V., Bess-Oberto, L., Chianelli, R.R., Rios, J., Parsons, J.G., Gamez, G., 2000. Characterization of Cr(VI) binding and
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Contents lists available at ScienceDirect
Ecological Engineering journal homepage: www.elsevier.com/locate/ecoleng
Short communication
Chromium and cobalt sequestration using exopolysaccharides produced by freshwater cyanobacterium Nostoc linckia Sharma Mona a , Anubha Kaushik b, * a b
Amity Institute of Environmental Toxicology, Safety and Management, Amity University Uttar Pradesh, Noida, 201313, India University School of Environment Management, Guru Gobind Singh Indraprastha University, New Delhi, India
A R T I C L E I N F O
A B S T R A C T
Article history: Received 11 September 2014 Received in revised form 24 February 2015 Accepted 5 April 2015 Available online 16 May 2015
This study investigated biosorption of chromium(VI) and cobalt(II) by exopolysaccharides (EPS) of a freshwater cyanobacterium, Nostoc linckia HA-46 from aqueous solution. Experiments were performed in batch mode to determine the adsorption dynamics of the cyanobacterial EPS. The adsorption capacity for Cr(VI) and Co(II) ions by EPS is found to be dependent on pH, contact time and initial metal ion concentration. The uptake kinetics of the metal ions follow pseudo-second order model. The maximum adsorption coefficient of determination (0.993Cr and 0.997Co) for Langmuir model indicates best fitness of this model in explaining the sorption as a multilayer process. The maximum adsorption capacities of the EPS were 14.3 mg Cr g1 (at pH 2.0) and 17.9 mg Co g1 (at pH 4.0) at an initial concentration of 20 mg L1. The EPS of Nostoc linckia shows better biosorption capacity for Co(II) than Cr(IV) metal ion. ã 2015 Elsevier B.V. All rights reserved.
Keywords: Exopolysaccharide Nostoc linckia Chromium Cobalt Biosorption Kinetics Adsorption isotherms
1. Introduction Accumulation of various toxic metals in wastewaters and aquatic bodies due to mining activities, tannery, dye and pigments, chemical fertilizers, pesticide and electroplating industries along with municipal sewage disposal has concerned general public (Das et al., 2008). Most heavy metals are toxic and sometimes carcinogenic, posing a serious threat to aquatic life and the humans (Hanif et al., 2009). Removal of heavy metals from wastewater has recently become the subject of considerable interest (Rzymski et al., 2014) owing to strict legislations. Chromium(VI) used in tannery, textile and electroplating is toxic to living organisms and is carcinogenic in nature (Mona et al., 2011a). Heavy exposure of Cr(VI) causes cancer in the digestive tract and lungs and may cause epigastric pain, nausea, vomiting, severe diarrhea and hemorrhage. Cobalt is used in manufacturing glasses and ceramics and in various metallurgical processes. Being an essential component of vitamin B-12, it is beneficial in trace amount, but at higher concentrations, cobalt becomes hazardous to respiratory and cardiovascular systems, and may cause coma or death (Mayflor, 2009). The ability of biological materials to adsorb rul et al., 2008; Mona et al., 2011b) has metal ions and dyes (Ertug received considerable attention for the development of an
* Corresponding author. Tel.: +91 11 25302362; fax: +91 11 28035243. E-mail address: [email protected] (A. Kaushik). http://dx.doi.org/10.1016/j.ecoleng.2015.04.037 0925-8574/ ã 2015 Elsevier B.V. All rights reserved.
efficient, clean and inexpensive technology for wastewater treatment. Exopolysaccharides (EPS) originating from bacteria, cyanobacteria, algae (Sharma et al., 2008) and fungi are recommended as surface active bioagents for toxic metal sequestration (Parker et al., 2000). A large number of cyanobacteria are characterized by the presence of exocellular polysaccharidic layers possessing mechanical and physicochemical stability with high degree of cross linking among the polysaccharide chains (Hoiczyk and Hansel, 2000). EPS-producing cyanobacteria have been considered very promising as chelating agents for the removal of positively charged metal ions from water solutions, owing to the presence of a large number of negative charges on the external cell layers (De Philippis and Micheletti, 2009). The aim of the present investigation was to quantify EPS produced by a freshwater cyanobacterium, Nostoc linckia in response to moderate concentrations of Cr(VI) and Co(II) in aqueous medium and study the biosorptive potential of the EPS for these metal ions. The species has earlier been reported (Kiran et al., 2004) as a very good biosorbent for removal of Cr(VI) from aqueous solutions. 2. Materials and methods 2.1. Cyanobacterial culture and EPS N. linckia HA-46 was isolated from metal contaminated wastewater collected from within the premises of a textile mill in Haryana, India, various characteristics of which are: pH 8.0,
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electrical conductivity 5.0 dS m1, total dissolved solids 1500 mg L1, total hardness 500 mg L1 (as CaCO3), chloride 1500 mg L1, phosphate 2.0 mg L1, Cr(VI) 5.0 mg L1, Co(II) 2.5 mg L1. Monoculture of the cyanobacterium, shown in Fig. 1A, was obtained using standard culturing and purification techniques as described earlier (Mona et al., 2011c). The cultures were grown for 15 days in BG-11 medium spiked with different concentrations (5, 10, 20, 40 and 80 mg L1) of Cr(VI) and Co(II). The cyanobacterial culture was subjected to centrifugation (800 g) on 14d and after separating the settled biomass, the supernatant (containing EPS) was used as biosorbent for removal of Cr(VI) and Co(II) in batch mode. 2.2. Metal biosorption studies Various metal concentrations were prepared from stock solution of 1000 mg L1 Cr(VI) (AR grade potassium dichromate) and Co(II) (AR grade cobaltous nitrate). Batch studies were performed to determine the sorption equilibrium for Cr(VI) and Co(II) onto the cyanobacterial EPS (estimated by the method of Seifter et al., 1959) serving as biosorbent. Cell-free culture (100 ml) containing EPS was taken in triplicate for the two metal ions (20 mg L1) at varying pH (1–6). The flasks were shaken for 2 h at 100 rpm at 25 C on an orbital shaker (Orbitek LT-IL). After optimizing the pH for maximum removal, which was found 2.0 and 4.0 for Cr(VI) and Co(II), respectively, studies were conducted for determining the optimum contact time. Stock solutions of the two metals (1000 mg L1) potassium dichromate/cobaltous nitrate were prepared and diluted to get desired concentrations (10–100 mg L1) of the metal ions. Equilibrium time required for the maximum metal adsorption (20 and 50 mg L1 initial
concentration) was determined by agitating 100 mL of each of the metal solution at its respective optimal pH, in 250-mL Erlenmeyer flasks on an orbital shaker (Orbitek LT-IL) at 25 C for 180 min at 100 rpm. Samples were withdrawn at fixed time intervals from the flasks and analyzed on atomic absorption spectrophotometer (Shimadzu AA6300) for residual concentration of chromium/cobalt in the aqueous solution. Equilibrium studies were performed using different initial metal ion concentrations (10–100 mg L1) at optimal pH and contact time. Amount of metal adsorbed, qewas calculated as: qe(mg/g) = V(Co – Ce)/m, where Co is initial metal concentration (mg L1), Ce the equilibrium concentration (mg L1), V the volume of metal solution (L) and m is the mass of EPS (g). Percent removal was calculated as the ratio of difference in initial and final metal concentration (Co Ce) to initial concentration (Co): R (%) =
C o C e Co
100. Residual concentration of Cr(VI) and
Co(II) ions in the synthetic solution was analyzed using anatomic absorption spectrophotometer (Shimadzu AA6300). To understand the mechanism of biosorption, different isotherms like Langmuir (Langmuir, 1918), Freundlich (Freundlich and Helle, 1939), BET (Brunauer et al., 1938), Temkin (Hosseini et al., 2003), Flory–Huggins (Horsfall and Spiff, 2005), and Dubinin–Radushkevich model (Dubinin, 1960) were applied to the equilibrium data (Table 1), as explained in detail earlier (Kiran and Kaushik, 2008). Surface morphology of the dry adsorbent before and after exposure to Cr(VI) and Co(II) were studied by Scanning electron microscope (Philips PSEM 515). Dry samples were mounted on stubs and coated with gold palladium of thickness 100–1500A and then transferred to the sample chamber of instrument. This was operated at 15 KV and current density of 15 pA.
Fig. 1. Micrograph of Nostoc (A) and scanning electron micrographs of unloaded (B), Cr(VI)-loaded (C) and Co(II)-loaded (D) EPS of Nostoc linckia.
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3. Results N. linckia showed increased production of EPS when exposed to moderate metal ion concentration (40 mg L1), but production of EPS declined when metal concentrations increased to 80 mg L1, particularly, in case of Cr(VI). The cyanobacterium produced about 40% more EPS in the presence of cobalt as compared to that of chromium (Fig. 2), which needs to be investigated further. Removal of metal ions by EPS of N. linckia was found to be pHdependent and for both the ions acidic pH favored more removal. Biosorption was maximum at pH 2.0 and 4.0 for Cr(VI) and Co(II), respectively, while lower pH of 1.0 as well as higher pH of 6.0 were less favorable (data not shown). pH higher than 6 was avoided as hydroxide formation and precipitation are reported to interfere with removal of metal ions (Aksu et al., 2002). 3.1. Biosorption kinetics Biosorption experiments of the two metal ions by EPS of the cyanobacterium as a function of contact time (5– 180 min) for two initial metalconcentrations (20 and 50 mg L1) were performed at the pH optimized for the two metals. At both the concentrations, metal removal increased with increasing contact time till 120 min for Cr and 135 min for Co, and then equilibrium was attained. At equilibrium, Cr and Co adsorption were 15.4, 17.1 mg g1 and 7.8, 43.2 mg g1at 20 and 50 mg L1 initial metal concentrations, respectively. Assuming the biosorption capacity of cyanobacterial EPS for Cr(VI) and Co(II) to be directly proportional to the number of active sites occupied on the sorbent, Lagergren rate equation (Lagergren, 1898) was applied. Rate constants for adsorption of the metal was determined using pseudo first order and pseudo second order equations as shown below: Logðqe qt Þ ¼
dq logqe k1 t and ¼ k2 ðqe qt Þ2 2:303 dt
(1)
where qe,qt are metal ion sorbed (mg g1) at equilibrium at any time (t), k1 is Lagergren rate constant (min1), k2 pseudo second order constant (g mg1 min1), respectively. A linearized form of the equation becomes: t/q = 1/k2qe2 + 1/qet
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better to pseudo second order model. The values of all the parameters viz., k1, k2 and qe calculated from the slope and intercept of plots are represented in Table 2. The experimental values of qe when compared with theoretical values of qe obtained from the second order kinetic model and the R2 values showed validity of the pseudo second order kinetic model. Values of qe calculated from the first order kinetic model by plotting log (qe qt) versus t was much different from the experimental value of qe, thus diminishing the application of first order model for the present system (Table 2). 3.2. Equilibrium models Six two-parameter models were used to explain the sorption equilibrium data, various parameters of which are depicted in Table 1 and discussed below: 3.2.1. Langmuir isotherm The equilibrium data was fitted to Langmuir isotherm, which is represented as: qe = QobCe/(1 + bCe) where qe is the amount of metal adsorbed (mg g1), Ce is the residual metal (Cr(VI) or Co(II)) concentration (mg L1), Qo (mg g1) and b (L mg1) are Langmuir constants showing the adsorption capacity and energy of adsorption, respectively (Langmuir, 1918). Linear plot obtained from Langmuir isotherm and the values of Langmuir constants (Qo and b) calculated from the intercept and slope of the plot are presented in the Table 2. The EPS showed very high adsorption capacity (Qo = 183.3 and 194.4 mg g1 for Cr(VI) and Co(II), respectively (Table 1). Separation factor (RL), a dimensionless constant was also calculated to examine the favorability of adsorption using the equation RL = 1/(1 + bCo), where Co is the initial metal ion concentration (mg L1). This parameter explains the isotherm as follows: RL > 1 unfavorable, RL = 1 linear, 0
(2)
The linear plot of t/q versus t showed better fitness of data for both the metals at 20 and 50 mg L1 concentrations as compared to the plot log (qe qt) versus t indicating that the sorption data fits
1
Fig. 2. Production of EPS (mg g biomass) in response to varying concentration of Cr(VI) and Co(II) by Nostoc linckia.
Table 1 Isotherm constants of two parameter models for Cr(VI) and Co(II) biosorption on EPS of N. linckia. Isotherm
Parameters
Langmuir
Qo (mg g1) b (L mg1) R2
183.3 0.198 0.9934
194.4 0.231 0.9965
Freundlich
Kf (mg g1) n R2
50.1 3.12 0.7436
53.4 4.32 0.8121
Temkin
a (L g1) b (kJ mol1) R2
3.13 0.089 0.9432
3.87 0.094 0.9767
Flory–Huggins
KFH nFH DG0 (kJ mol1) R2
1112.4 4.87 19.6 0.9549
120.7 5.21 20.1 0.9656
Dubinin–Radushkevich
qD (mg g1) BD (mol2 kJ2) E (kJ2 mol2) R2
191.3 0.51 1.16 0.9611
193.3 0.61 1.32 0.9767
BET
qmax (mg g1) B (L mg1) R2
181.5 2.9 104 0.9888
191.84 3.2 104 0.9898
Cr(VI)
Co(II)
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Table 2 Kinetic model parameters for metal adsorption on EPS at 20 and 50 mg/L initial metal concentration. Initial metal concentration (mg L1)
Experimental qe(mg g1)
First order model
Second order model
Theoretical qe (mg g1)
K1 (min1)
R2
Theoretical qe (mg g1)
K2 (mg g1 min1)
R2
Cr(VI) 20 50
15.4 37.8
6.19 30.21
0.0451 0.0521
0.8989 0.9112
17.32 44.3
2.113 13.21
0.9986 0.9998
Co(II) 20 50
17.12 43.23
9.65 27.67
0.0531 0.0711
0.6988 0.764
16.87 39.87
2.321 5.121
0.9787 0.9989
3.2.2. Freundlich isotherm This isotherm assuming a heterogeneous surface of the adsorbent, was applied to equilibrium data in the form of the equation Log qe = Log Kf + 1/n (Log Ce), where qe is metal adsorbed (mg g1), Ce is residual metal ion concentration (mg L1), Kf is Freundlich constant indicating adsorbent capacity (mg g1 dry weight) and n is Freundlich exponent (Table 1) known as adsorbent intensity (Freundlich and Helle, 1939). A linear plot of Log qe versus Log Ce explained the applicability of this isotherm for the biosorbent, indicated by high values of Kf (50.1 and 53.4 for Cr and Co, respectively). 3.2.3. Temkin isotherm Temkin isotherm is based on the assumption that fall in the heat of sorption is more linear rather than logarithmic, as provided in Freundlich equation (Aharoni and Ungarish, 1977). It was suggested that due to sorbent and sorbate interactions, the heat of sorption of all the molecules in the layer would reduce linearly with coverage (Hosseini et al., 2003) in the form of equation ln (aCe), where b is the Temkin constant related to the heat of qe = RT b sorption (kJ mol1), R is the gas constant (0.0083 kJ (mol K)1), a is the Temkin isotherm constant (L g1), and T the absolute temperature (K), qe is the amount of metal adsorbed (mg g1), Ce is the residual metal ion concentration (mg L1). From the curve plotted between qe and lnCe, constants a and b were calculated and shown in Table 1. 3.2.4. Flory–Huggins isotherm This model was applied to assess the degree of surface coverage of the sorbate on the sorbent. The linearized form of the model u = LogK + n Log (1 u )where (Horsfall and Spiff, 2005) is: Log Ce FH FH Ce is the residual metal concentration (mg L1), KFH is Flory– Huggins model equilibrium constant, nFH is the Flory–Huggins model exponent and u = (1 Ce/Co) is degree of surface coverage. Values of KFH and nFH calculated from the slope and intercept of the linear plot and shown in Table 1. High R2 values shows the excellent applicability of the model. The Gibbs free energy of spontaneity (G0) was calculated as DG0 = RT lnKFH. The negative value of G0 (19.6 for Cr and 20.1 for Co) obtained for the biosorption of Cr (VI) and Co(II)) onto the cyanobacterial EPS (Table 1) shows feasibility and spontaneous nature of the process. 3.2.5. Dubinin–Radushkevich isotherm According to this model, the sorption curve depends on the porous structure of the sorbent and linear form of the isotherm is: 1 ), where qD (mg g1) and BD qe = qD exp(BDED2); ED = RT ln(1 + Ce 2 2 (mol KJ ) are the Dubinin–Radushkevich model constants and ED is the Polanyi potential. p The mean energy of sorption was calculated as: E = 1/ 2BD. The 2 values of both the constants along with R (Table 1) are high for the adsorbent showing good fitness of the isotherm. The energy value
for biosorbent is very low (1.16 and 1.32 kJ2 mol2 for Cr(VI) and Co (II), respectively) indicating weak interaction of the metal with the present sorbent. 3.2.6. Brunauer, Emmer & Teller (BET) model This model assumes that first layer of sorbate molecules adsorbs on the surface with energy comparable to the heat of adsorption for monolayer sorption and the subsequent layers have equal energies (Brunauer et al., 1938) explained as: qe = Bqmax C e , where Cs is saturation concentration of solute C ðCe C s Þ½1þðB1Þ
e Cs
(mg L1) and B is a constant related to energy of adsorption. Values of qmax and B calculated from the plot are shown in Table 1. High R2 shows applicability of the model to our data. Though all the applied models explained the sorption data well, the Langmuir model is best fitted. The scanning electron micrographs of EPS of the cyanobacterium (Fig. 1B–D) reveal its porous nature along with depressions and grooves on the surface (Fig. 1B), indicating availability of abundant binding sites for the biosorption of Cr(VI) and Co(II)). Binding of the metal ions on the surface of EPS is clearly visible as white encrustations over the pores in the SEM for both the metals (Fig. 1 C and D). 4. Discussion Most cyanobacterial exopolysaccharides are characterized by the presence of various functional groups that help in chelating ions (De Philippis et al., 2001). A wide variety of cyanobacterial genera have been documented for EPS synthesis and metal adsorption properties (Sharma et al., 2008; Chakraborthy et al., 2011; Gupta and Rastogi, 2008; Ozturk et al., 2009). Interaction between metallic cations and negative charge of acidic functional groups of EPS are favored at low pH. Decreased solubility of metal complexes in solution with increasing pH (Vijayaraghavan and Palanivelu Velan, 2006) could also result in low biosorption at high pH. Decrease in adsorption capacity of EPS at pH higher than 2 for Cr is explained by the fact that due to the exposure of more negatively charged functional groups, negatively charged chromate ions (HCrO4, CrO7, Cr4O132 and Cr3O102) present in solution are repelled (Aksu et al., 2002; Gardea-Torresdey et al., 2000). A net positive charge at pH 2, due to protonation of functional groups and presence of hydronium ions around the surface, further facilitates the adsorption of negatively charged hexavalent chromate ions (Kiran and Kaushik, 2008; Matheickal et al., 1991; Fourest et al., 1994). Sorption of the metal was relatively more rapid suggesting the involvement of a passive process like physical adsorption or ion exchange on the surface of the cyanobacterial EPS during the initial period. This was followed by a steady and slow stage that is likely to be associated with some active energy mediated process. The metal removal process seems to involve physisorption. Typical bonding energy range for ion-
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exchange mechanism is reported to be in the range of 8–16 kJ mol1 while physisorption processes are reported to have adsorption energies less than 40 kJ mol1 (Zafar et al., 2007). 5. Conclusion Production of EPS by N. linckia is stimulated by Co(II) and Cr(VI) and it has excellent biosorption potential for both the metals, but more so for cobalt as indicated by SEM images and the qmax values obtained from adsorption isotherms. Acknowledgements This work was financially supported by a grant of UGC-SAP (DRS-II) and Senior Research Fellowship to the author from CSIR, New Delhi. References Aharoni, C., Ungarish, M., 1977. Kinetics of activated chemisorption. Part 2 theoretical models. J. Chem. Soc. Faraday Trans. 73, 456–464. Aksu, Z., Acikel, U., Kabasakal, E., Tezer, S., 2002. Equilibrium modeling of individual and simultaneous biosorption of chromium(VI) and nickel(II) onto dried activated sludge. Water Res. 36, 3063–3073. Brunauer, S., Emmer, P.H., Teller, E., 1938. Adsorption of gases in multimolecular layers. J. Am. Chem. Soc. 60, 309–319. Chakraborthy, N., Banerjee, A., Pal, R., 2011. Accumulation of lead by free and immobilized cyanobacteria with special reference to accumulation factor and recovery. Bioresour. Technol. 102, 4191–4195. Das, N., Karthika, P., Vimala, R., Vinodhini, V., 2008. Use of natural products as biosorbent of heavy metals an overview. Nat. Prod. Radiance 7 (2), 133–138. De Philippis, R., Micheletti, E., 2009. Heavy metal removal with exopolysaccharidesproducing cyanobacteria. In: Shammas, N.K., Hung, Y.T., Chen, J.P., Wang, L.K. (Eds.), Heavy Metals in the Environment. CRC Press, Boca Raton, pp. 89–122. De Philippis, R., Sili, C., Paperi, R., Vincenzini, M., 2001. Exopolysaccharideproducing cyanobacteria and their possible exploitation. J. Appl. Phycol. 13 (4), 293–299. Dubinin, M.M., 1960. The potential theory of adsorption of gases and vapors for adsorbents with energetically non-uniform surface. Chem. Rev. 60, 235–266. rul, S., Bakır, M., Donmez, G., 2008. Treatment of dye-rich wastewater by an Ertug immobilized thermophilic cyanobacterial strain: Phormidium sp. Ecol. Eng. 32 (3), 244–248. Fourest, E., Canal, C., Roux, J.C., 1994. Improvement of heavy metal biosorption by mycelial dead biomass (Rhizopusarrhizus, Mucormieheiand Penicillumchrysogenum): pH control and cationic activation. FEMS Microb. Rev. 14, 325–332. Freundlich, H., Helle, W.J., 1939. Ubber die adsorption in Lusungen. J. Am. Chem. Soc. 61, 2–28. Gardea-Torresdey, J.L., Tiemann, K.J., Armendariz, V., Bess-Oberto, L., Chianelli, R.R., Rios, J., Parsons, J.G., Gamez, G., 2000. Characterization of Cr(VI) binding and
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