Sorption of lead ions from aqueous solution onto

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Sorption of lead ions from aqueous solution onto Enterococcus faecium biomass Meral Yilmaz Cankilic, R. Bengu Karabacak, Turgay Tay and Merih Kivanc

ABSTRACT This study reports kinetics and equilibrium of lead sorption onto the biomass of Enterococcus faecium. E. faecium is a lactic acid bacterium and was isolated from meat. Batch experiments were carried out to analyze the effects of the initial lead concentration, initial pH of the medium, agitation time and temperature on the biosorption. The lead sorption was found to increase with the increase in the solution pH, reaching a plateau value beyond pH 5, and the most favorable pH for removal was determined as 5.0. The highest lead uptake capacity of the biomass was obtained at the initial lead concentration of 300 mg L–1. The Langmuir and Freundlich adsorption models were applied to determine the biosorption isotherm, and the equilibrium data correlated well with the Langmuir

Meral Yilmaz Cankilic Merih Kivanc Faculty of Sciences, Department of Biology, Anadolu University, Eskisehir, Turkey R. Bengu Karabacak Turgay Tay (corresponding author) Faculty of Sciences, Department of Chemistry, Anadolu University, Eskisehir, Turkey E-mail: [email protected]

model. The pseudo-second-order kinetic model was more suitable to fit the experimental data. The results were promising that the biomass of this lactic acid bacterium can be successfully used as a convenient adsorbent for lead removal from aqueous solutions. Key words

| biosorption, Enterococcus faecium, isotherm, kinetics, lead

INTRODUCTION Removal of heavy metals such as cadmium, lead, nickel, chromium and copper from surface and ground water is of high priority because of their high toxicities to living organisms and frequent appearance in wastewaters of many industries, including electroplating, metal finishing, metallurgical, tannery, chemical manufacturing, mining and battery manufacturing industries. Heavy metals in wastewaters can easily enter the food chain after consumption of aquatic animals and plants irrigated using such waters. For this reason, heavy metal pollution has received great attention in recent years (Brinza et al. ; Maximous et al. ; Mousavi et al. ). A number of techniques for the removal of metal ions from aqueous solutions have been developed over the years. The most important ones include precipitation, adsorption, ion exchange and coagulation processes. However, some of these methods can be expensive and not fully effective. Adsorption has received great attention in recent years for removing dissolved metal ions from liquid wastes (Bayat ; Yadanaparthi et al. ), and to lower adsorption costs the use of natural adsorbents abundant in nature has been preferred (Badmus et al. ). The natural adsorbent materials may come from different sources. doi: 10.2166/wst.2013.398

Agricultural by-products (Samantaroy et al. ; Singh et al. ), waste materials (Namasivayam & Yamuna ), rice husk (Wong et al. ), slag (Dimitrova & Mehandgiev ; Cúrkovic´ et al. ), rice bran (Chen et al. ), clays (Harvey & Chantawong ; Sanchez et al. ), cocoa shells (Meunier et al. ), Cucumis melo (Akar et al. ), sargassum (Silva et al. ), tree fern (Ho ), leaves (King et al. ), chitosan, granular red mud (Zhu et al. ), zeolite (Stylianou et al. ), activated carbon (Giraldo & Moreno-Piraján ; Kumar et al. ), sugar beet pulp (Pehlivan et al. ), Pseudomonas sp. (Huang & Liu ), and sawdust (Asadi et al. ) are some of the natural adsorbents employed in adsorption. Lead is considered to be a persistent pollutant and occurs in wastewater which mainly comes from battery manufacturing, printing, painting, dying and other industries. Its high levels cause several health problems such as anemia, kidney and liver diseases, paralysis, brain disorders and at times death, and also low levels result in hyperactivity, learning disabilities in children, night blindness and suppression of the body’s immune system ( Jain et al. ). Some studies have reported lead removal from wastewater to an acceptable level by precipitation, coagulation and

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Sorption of Pb ions from aqueous solution onto Enterococcus faecium biomass

adsorption processes (Day et al. ; Lee et al. ; Chu ; Matlock et al. ; Chiron et al. ; Zhang et al. ). The lactic acid bacteria (LAB) are Gram-positive bacteria and well-known for their large number of different polar and ionic groups like carboxyl, hydroxyl, and phosphate on their cell surfaces (Landersjö et al. ). These groups give the bacteria capability of binding cations like lead and cadmium ions. In the present study, the Enterococcus faecium strain, belonging to LAB, was investigated as a suitable biosorbent for removing lead from aqueous solution under different experimental conditions.

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determined by flame atomic absorption spectrometry with an air-acetylene flame at 283.3 nm wavelength in the concentration range 0–10 ppm with a Perkin Elmer Analyst 800 spectrophotometer for lead. Amounts of adsorbentbound lead was calculated from the difference between the initial and final concentrations of heavy metal ion in solution. The equilibrium sorption capacity of the E. faecium biomass at the equilibrium conditions was determined using the mass balance equation: qe ¼

(C0 Ce )V m

where qe is the amount of Pb2þ ions adsorbed onto the biomass (mg g1), C0 and Ce are the initial and final Pb2þ concentrations in solution (mg L1), respectively, V is the volume of the medium (L) and m is the amount of the biomass used in the adsorption process (g).

MATERIAL AND METHODS Preparation of biomass The Enterococcus faecium strain was isolated from meat and identified using the RiboPrinter® Microbial Characterization System (DuPont). The isolate was inoculated into MRS broth (Lactobacillus broth according to de Man, Rogosa and Sharpe) for 48 h at 37 C. Then the biomass was centrifuged (8,000 × g, 15 min), washed twice with ultra-pure water (Milli-Q), lyophilized and stored at –20 C. W

W

Preparation of lead solutions A stock solution of Pb2þ ions (500 mg L1) was prepared in deionized water with Pb(NO3)2. All working solutions of varying concentrations from 25 to 500 mg L1 were obtained by diluting the stock solution with distilled water. The pH of working solutions was adjusted to desired values with 0.1 M HCl or 0.1 M NaOH at the beginning of the experiments and was not controlled further.

RESULTS AND DISCUSSION Figure 1 shows the time course of the Pb2þ uptake by the E. faecium biomass. A rapid sorption rate was observed within the first 6 h of the process and then the uptake capacity of the biomass remained nearly constant with a value of approximately 140 mg Pb2þ per g biomass. Such initial uptakes of heavy metals by different biosorbents have also been reported in the literature (Puranik & Paknikar ; Yin et al. ; Yilmaz et al. ).

Biosorption experiments Batch biosorption experiments were carried out in 250 mL bottles, containing 50 mg of the biomass and 100 mL of Pb2þ solution at the desired concentration, pH and temperature. Experiments were done in duplicate and averaged. The bottle contents were shaken using an orbital shaker at 150 rpm. After the contact time, the mixtures were centrifuged at 5,000 rpm for 5 min and the concentration of non-adsorbed Pb2þ ions in the supernatant was determined by using a flame atomic absorption spectrophotometer. Concentrations of residual heavy metal in filtrate were

Figure 1

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Time course of Pb2þ uptake by the E. faecium biomass. Biosorption conditions: C0 ¼ 300 mg L1; m ¼ 50 mg; pH ¼ 5.0; V ¼ 100 mL; T ¼ 30 C; agitation rate W

150 rpm.

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It is well established that the pH of the solution has tremendous effect on the heavy metal sorption capacities of biosorbents due to the fact that the charge of the groups on the surface of biomasses and metal chemistry in the process are pH dependent. Some research on the biosorption of heavy metals onto different kinds of microbial biomass have found that maximum biosorption occurs around neutral pH (Xue et al. ; Feng & Aldrich ; Calero et al. ). In order to determine the optimal pH for sufficient biosorption of Pb2þ onto the E. faecium biomass, biosorption experiments at different initial pH values varying from 1.0 to 6.0 were performed (Figure 2). As expected, the biosorption process was strongly pH dependent and the highest uptake values were obtained at pH 5 and 6. The uptake capacity of the biomass dropped sharply at pH 3 and below, and was approximately 1/20 of those at pH 5 and 6. These results are similar to the results of various biosorption processes reported in the literature (Puranik & Paknikar ; Singh et al. ; Maximous et al. ). Biosorption of Pb2þ at pH values higher than 6 was not investigated because of occurrence of precipitation of Pb2þ ions from the solution. The Pb2þ biosorption capacity of the E. faecium biomass was also investigated as a function of the initial Pb2þ concentration (C0) (Figure 3). As the initial concentrations of Pb2þ increased from 25 to 500 mg L1, a steady increase in the biosorption capacity of the biomass was observed. Higher than C0 ¼ 300 mg L1, the biosorption capacity nearly leveled off. On the other hand, % Pb2þ uptake of the biomass decreased from approximately 80% to about 20% as the initial concentration of Pb2þ increased. Even

Figure 3

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Effect of pH on Pb2þ biosorption capacity of E. faecium. Biosorption conditions: C0 ¼ 300 mg L1; m ¼ 50 mg; V ¼ 100 mL; T ¼ 30 C; contact time 25 h; agitaW

tion rate 150 rpm.

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W

agitation rate 150 rpm; contact time 25 h.

the lowest initial Pb2þ concentration, 25 mg L1, tested in this study is a very high Pb2þconcentration compared to the ones observed in wastewaters; our 50 mg biomass was able to remove approximately 80% of 2.5 mg Pb2þ in that concentration. This percentage indicates an efficient removal of Pb2þ by the biomass. The findings about biosorption capacity and %Pb2þ uptake are reasonable because, at low Pb2þ concentration, plenty of binding sites for the ions are available on the biomass. At high Pb2þ concentrations, the binding sites on the biosorbent were apparently occupied or saturated by the Pb2þ ions. Thus the biosorption capacity of the biomass remained nearly constant at the concentration of 300 mg Pb2þ per liter and higher. Based on this finding, further biosorption experiments were carried out at 300 mg L1 initial Pb2þ concentration. The temperature of the adsorption medium may be a factor for energy-dependent mechanisms in metal adsorption by microbial cells. In this study equilibrium Pb2þ uptakes onto the E. faecium biomass were not altered significantly at temperatures 20, 30 and 40 C, indicating the adsorption process is not temperature dependent. Nearly constant values of qe, approximately 140 mg Pb2þper gram of the biomass, were obtained at the temperatures applied. Thus 30 C was chosen as the temperature of further experiments. Adsorption isotherms are important to reveal the mechanism of the adsorption process, and Langmuir and Freundlich isotherms are commonly used to analyze adsorption data (Freundlich ; Langmuir ). The Langmuir isotherm model is valid for monolayer adsorption onto a surface containing a given number of identical sorption W

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Effect of initial Pb2þ concentration on the biosorption capacity of E. faecium. Biosorption conditions: m ¼ 50 mg; V ¼ 100 mL; temperature 30 C; pH 5.0;

W

Figure 2

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sites. The Langmuir equation is commonly expressed as: Ce 1 Ce ¼ þ qe qmax KL qmax where the slope and intercept of the linear plot of Ce/qe versus Ce gave the values of 1/qmax and 1/qmaxKL, respectively. qmax is the amount of metal ion removed and maximum uptake capacity of the adsorbent (mg g1), Ce is the equilibrium concentration of the metal ion in the solution (mg L1), and KL is the Langmuir constant (L mg1). The Freundlich equation assumes the adsorption occurs on a heterogeneous surface, and is described by the following equation:

Figure 4

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Comparison of experimental equilibrium data with the theoretical equilibrium data obtained from the non-linearized equations of Langmuir and Freundlich isotherms.

1 log qe ¼ log KF þ log Ce n Table 2

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1

where KF (in L g ) and n are Freundlich constants. The Langmuir and Freundlich isotherm parameters of the biosorption determined from the slopes and intercepts of the corresponding plots are given in Table 1. The regression coefficient value of the Langmuir equation (0.976) was better than that of the Freundlich equation (0.950). It appears that the Langmuir isotherm gives a better fit than the Freundlich isotherm. Figure 4 shows the plots of non-linearized Langmuir and Freundlich isotherm equations and experimentally obtained data. In order to elucidate the kinetics of the biosorption of Pb2þ onto the biomass, the pseudo-first-order and pseudosecond-order kinetic models were applied to the experimental data. The pseudo-first-order kinetic model equation (Lagergren ) is expressed as: log (q1 qt ) ¼ log q1

Parameters of the pseudo-first-order and the pseudo-second-order kinetic model for the biosorption of Pb2þ onto the E. faecium biomass

Pseudo-first-order 1

k1 (min ) q1 (mg g1) r21

Pseudo-second-order 3

2.764 × 10 55.2 0.936

k2 (g mg1 min1) q2 (mg g1) 2 r2

2.16 × 104 140.8 0.999

q1 were calculated from the slope and y-intercept of the plot of log (q1–qt) against t (Table 2). The pseudo-second-order kinetic model equation (Ho & McKay ; Calero et al. ) is given as: t 1 1 ¼ þ t qt k2 q22 q2

k1 t 2:303

where q1 and qt are the amounts of Pb2þ biosorbed at equilibrium and at time t (mg g1), respectively, and k1 is the pseudo-first-order rate constant (min1). Values of k1 and

Table 1

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Langmuir and Freundlich isotherm parameters for the biosorption of Pb2þ ions onto E. faecium biomass

Langmuir

Freundlich 1

qmax (mg g ) 1

KL (L mg ) r2L

175.44

2.80

n 1

0.0154

KF (L g )

0.976

r2F

18.54 0.950

Figure 5

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Pseudo-second-order kinetic plot for the biosorption of Pb2þ onto E. faecium biomass. Biosorption conditions: C0 ¼ 300 mg L1; m ¼ 50 mg; V ¼ 100 mL; T ¼ 303 K; agitation rate ¼ 150 rpm.

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where q2 is the maximum adsorption capacity of the biomass (mg g1) for the pseudo-second-order adsorption, k2 is the equilibrium rate constant for the pseudo-secondorder adsorption (g mg1 min1). Values of k2 and q2 were calculated from the slope and y-intercept of the plot of t/qtagainst t (Table 2, Figure 5). The experimental obtained data were better fitted to the pseudo-second order kinetic model than the pseudo first-order kinetic model.

CONCLUSION In this work, the biomass of E. faecium was used as a biosorbent in removal of Pb2þ from aqueous solutions. The biosorption process was affected by initial metal concentrations, pH, and contact time. The biomass was found to sorb a maximum of 175.44 mg Pb2þ per gram under conditions of pH 5.0, contact time of 25 h, biosorbent mass of 50 mg and initial metal ion concentration of 300 mg L1. The amount of Pb2þ taken up by the biomass increased rapidly during the first 6 h and then increased slightly with time. The Pb2þ adsorption capacity of the biomass increased with increasing pH value and initial lead ion concentration. Langmuir and Freundlich isotherms were used as adsorption models to describe the effects of lead ion concentration after equilibrium. The Langmuir isotherm model gave a better fit than the Freundlich isotherm. The kinetic study showed that the equilibrium was reached at 400 min. The kinetics of the biosorption of Pb2þ onto E. faecium followed a pseudo-second-order adsorption kinetics. As a result, in this work, the bacterial biomass, E. faecium, was found to be an effective biosorbent for removal of lead ion from aqueous solutions and it could be used as an inexpensive and quite efficient biosorption material.

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First received 28 December 2012; accepted in revised form 29 May 2013