Abstract

The biosorption of Pb(II) from aqueous solutions by lactic acid bacterium, Lactobacillus brevis, was studied. The effects of initial pH, contact time, initial Pb(II) concentration, bacterial concentration, rotation speed and temperature of biosorption of Pb(II) from aqueous solutions were investigated. The optimal condition for Pb2+ ions adsorption was observed at pH 6, with the rotational speed of 120 rpm.min−1, bacterial concentration of 3 g.L−1, temperature of 40 °C and contact time of 12 h. The correlation regression coefficients showed that the biosorption process can be well fitted with the Redlich-Peterson, Langmuir, Freundlich and Temkin isotherm models. The equilibrium adsorption capacity reached 53.632 mg.g−1. Binding energy value was 0.264 kJ/mol, which indicated that the adsorption process seemed to involve chemisorption and physisorption. Kinetics of adsorption was found to fit well with the pseudo-second-order and Elovich kinetic equations. Thermodynamic parameters revealed the feasibility, spontaneity and endothermic nature of adsorption.

INTRODUCTION

As industrial activities increase rapidly all over the world, heavy metal pollution and toxicity have been brought into public concern. Lead (Pb), a kind of heavy metal, is one of the most ubiquitous toxic heavy metals, attracting broad attention towards the hazard to human health and environment because of its non-biodegradable and metallic toxicity. Due to being widely used in printing, metallurgy, construction, the military and medical treatment, it can contaminate water through various approaches. Lead cannot be degraded to generate non-toxic products in the natural environment. It can accumulate and get concentrated in soil, plants, and aquatic organisms, resulting in biomagnifying Pb in the food chain (Nwachukwu et al. 2010; Ashraf et al. 2011). The safe permissible level of Pb2+ content in drinking water shall not exceed 0.01 mg/L (Imasuen & Egai 2014).

A long period of exposure to Pb can harmfully affect the nervous system, prevent hemoglobin synthesis, cause kidney damage, and reduce semen quality (Järup 2003). The traditional methods for removing heavy metals from water can be achieved with chemical precipitation, ion exchange, membrane filtration and so on, but these methods are sometimes not cheap, not effective at low metal concentrations, nor suitable for in vivo treatment (Rawat et al. 2014). Chelating agents can remove metals from the body effectively (Ahamed & Siddiqui 2007; Blaurock-Busch 2011; Patrick L 2003), but it has some limitations and side effects (Cappellini et al. 2011; Balooch et al. 2014). Therefore, safe novel treatments need to be studied to deal with it. Biosorption, as an emerging and promising application, has engaged in the research into removing heavy metals in recent years. Compared to traditional methods, biosorption has the advantages of low investment, easy accessibility and no residue (Porova et al. 2014). With the feature of small size, fast breeding and high absorption efficiency, microorganisms have the potential to be the biological absorbent.

Lactic acid bacteria, microorganisms that are used as probiotics, are non-pathogenic and exist in the human gastrointestinal tract and fermented foods. Lactic acid bacteria have the capacity to bind many toxic compounds such as aflatoxins (Ahlberg et al. 2015), microcystin-LR (Nybom et al. 2012), as well as heavy metals from aqueous solution. Many reports show that LAB can selectively and efficiently remove different toxic ions, Cd(II), Pb(II), Cu(II), As(V) and so on, from aqueous solution (Tian et al. 2015; Zhai et al. 2015; Elsanhoty et al. 2016; Yi et al. 2017).

In the present work, the biosorption of Pb(II) ions with a lactic acid bacterium, Lactobacillus brevis, has been studied. What's more, the effect of pH, contact time, initial concentration of Pb(II) ions, temperature, and bacterial concentration have been investigated. Moreover, the adsorption isotherms and kinetics onto Lactobacillus brevis were also studied.

MATERIALS AND METHODS

Bacterial strains and culture

The strain used in this study was Lactobacillus brevis, a lactic acid bacterium obtained from pickles (purchased from a local market, Sichuan, China). Bacteria were cultured in MRS-broth (Sigma-Aldrich, China) for 24 h at 35 °C. Then the cultured biomass was centrifuged (5,000 rpm, 10 min), and washed twice with deionized water before the experiment.

Pb biosorption assay

A weighed amount of cell pellets was resuspended in deionized water containing 100 mg/L Pb as lead nitrate (Sinopharm Chemical Reagent Company, Shanghai, China) to give a final bacterial concentration of 1 g/L. Biomass weight in the suspension was calculated after drying. The effect of temperature (20–40 °C) on the biosorption capacity was evaluated with incubating at initial pH for 16 h, 120 rpm. The pH (2–7), adjusted with dilute NaOH and HNO3 (Sinopharm Chemical Reagent Company, Shanghai, China) and the samples were incubated for 16 h at 35 °C, and 120 rpm. Similarly, the effect of bacterial concentration (1–7 g.L−1), contact time (1–24 h), rotation speed (0–200 rpm.min−1), initial metal concentration (10–200 mg.L−1). All experiments were repeated at least twice.

Measurement of lead

After the contact time, the solutions were centrifuged at 5,000 rpm for 10 min and the supernatants were used to determine the concentration of Pb2+ ions by flame atomic absorption spectrophotometry (TAS-990; Puxi General Instrument Co., Ltd, Beijing). The instrument response was periodically checked with a standard Pb2+ ion solution.

The equilibrium sorption capacity of the Lactobacillus brevis biomass at the corresponding equilibrium conditions was determined according to the following mass balance equation:  
formula
(1)
where qe is the amount of Pb2+ ions adsorbed on the biomass (mg g−1), C0 is the initial Pb2+ ion concentration in solution (mg.L−1), Ce is the final metal ion concentration in solution (mg.L−1), V is the volume of the medium (L) and m is the amount of the biomass used in the adsorption process.
The metal ions; removal efficiency Q (%) was calculated by Equation (2)  
formula
(2)

RESULTS AND DISCUSSION

Effect of contact time

Figure 1 shows the effect of contact time on the biosorption of Pb2+ ions by Lactobacillus brevis. With the increase of treatment time, the amount of adsorption of lead ions increased, and the amount of adsorption at 12 h was almost the largest, reaching 44.23 mg/g by per gram of Lactobacillus brevis. This adsorption phenomenon was similar to the previous reports on the biosorption of heavy metals by different biosorbents (Fiol et al. 2006; Wang et al. 2010); however, the time of adsorption equilibrium was different. The different results may be due to the different amount of bacteria added, different kinds of bacteria, different experimental conditions and so on. Therefore, chose 12 hours as the adsorption time of other experiments. The relationship between the amount of adsorption and time can be further applied to dynamic fitting.

Figure 1

Effect of contact time on the biosorption of Pb2+ ions. Biosorption conditions: Co = 100 mg.L−1; 1 g.L−1; T = 35 °C; ratate speed 120 rpm.

Figure 1

Effect of contact time on the biosorption of Pb2+ ions. Biosorption conditions: Co = 100 mg.L−1; 1 g.L−1; T = 35 °C; ratate speed 120 rpm.

This has been extensively reported in the literature (El-Sayed 2013; Kinoshita et al. 2013). The process can be divided into two stages. The first stage is rapid increase. It is the phenomenon of physical adsorption or ion exchange on the surface of bacteria, which is called passive adsorption, and this adsorption takes up the main part. In this stage, there is a considerable number of available vacant binding sites on the biosorbent and Pb(II) ions, so the lead ions can be combined with the binding site at will, the opportunity of binding is very large, so the adsorption is faster. The second stage is a slow process of achieving equilibrium, which is called active adsorption. With the increase of contact time, the adsorption becomes slower because the binding sites are gradually occupied by lead ions, which reduces the concentration of lead ions in the solution and the number of binding sites, and there are repulsive forces from Pb(II) ions adsorbed on the adsorbent's surface; all of these factors make the adsorption slower.

Effect of temperature

Much literature has reported the effects of temperature on the biosorption. From these studies, it can be concluded that the temperature of the adsorption medium might have an important effect on metal ions' adsorption by bacteria. These results suggested that there are two different biosorption mechanisms because of different metals and different kinds of adsorbents. One is that the temperature has a great influence on the adsorption, the adsorption process needs to consume energy, the other is that it has no effect. Figure 2 shows the effects of temperature (20–40 °C) on the biosorption of Pb2+ ions by Lactobacillus brevis. The results showed that the temperature significantly affected the biosorption of Pb2+ ions. The biosorption capacity increased as temperature increased, and at the temperature of 40 °C, the biosorption was highest, reaching 42.35 mg.g−1.

Figure 2

Effect of temperature on the biosorption of Pb2+ ions. Biosorption conditions: Co = 100 mg L−1; 1 g.L−1; rotational speed 120 rpm; contact time 16 h.

Figure 2

Effect of temperature on the biosorption of Pb2+ ions. Biosorption conditions: Co = 100 mg L−1; 1 g.L−1; rotational speed 120 rpm; contact time 16 h.

Effect of initial pH

As shown in Figure 3, the biosorption amount of Pb2+ ions was a strongly pH-dependent process, and the amount of adsorption by strains was a quite different under different pH. The biosorption was very low at pH ≤ 3, and only about 3.6 mg.g−1 at pH 2. As pH increased, the biosorption increased and the highest binding of lead, 44.4 mg.g−1, was achieved at pH 6, when pH values were higher than 6 the biosorption amount decreased with increasing pH. Our results were similar to some literature (Nadeem et al. 2008; Lalhruaitluanga et al. 2010).

Figure 3

Effect of pH on the biosorption of Pb2+ ions. Biosorption conditions: Co = 100 mg L−1; 1 g.L−1; T = 35 °C; rotational speed 120 rpm; contact time 12 h.

Figure 3

Effect of pH on the biosorption of Pb2+ ions. Biosorption conditions: Co = 100 mg L−1; 1 g.L−1; T = 35 °C; rotational speed 120 rpm; contact time 12 h.

According to the relevant literature, studies have shown that pH has a significant influence on the biosorption processes. Because it influences not only the solubility of metal ions but also the ionization states of bacterial surface groups in the processes (Vásquez et al. 2007; Gao et al. 2011). When pH was low, the cation was the main advantage. On one hand, it was easy to protonate the anionic groups on the surface of the bacteria. At the same time, anionic groups also competed with the metal cation which leaded to its low adsorption efficiency. When the pH value reached 6, the carboxyl group, hydroxyl group, phosphate radical and amino are gradually exposed and combined with metal cations, which increase the lead ion removal rate. But pH continued to increase, it would cause the precipitation effect of metal hydroxide. Based on these results, pH values of 6 was used in further lead biosorption experiments.

Effect of initial Pb2+ ion concentration

The initial concentration of Pb(II) had a strong influence on the adsorption capacity of Lactobacillus brevis. The concentration of lead ranged from 10 to 200 mg.L−1. As can be seen from Figure 4, the biosorption capacity increased as initial Pb(II) concentration increased, the adsorption increased rapidly at beginning, and subsequently slowed. When the initial concentration of lead ions increased from 10 mg/L to 200 mg/L, the adsorption amount increased from 8.06 mg/L to 51.43 mg/L. Nevertheless, it may not reach the highest biosorption capacity. In other words, it meant that Pb(II) adsorption could be higher because of the increasing number of free Pb(II) ions competing for the available binding sites at higher Pb(II) concentrations.

Figure 4

Effect of initial Pb2+ ion concentration on the biosorption of Pb2+ ions. Biosorption conditions: Co = 100 mg.L−1 pH 6; contact time 12 h; 1 g.L−1; T = 35 °C.

Figure 4

Effect of initial Pb2+ ion concentration on the biosorption of Pb2+ ions. Biosorption conditions: Co = 100 mg.L−1 pH 6; contact time 12 h; 1 g.L−1; T = 35 °C.

However, as was observed, the percentage adsorption of Pb(II) was decreased with the increase in initial Pb(II) concentration. The highest percentage adsorption of Pb(II) was at the lowest concentration of 10 mg/L, for there were a larger number of binding sites available on the biosorbent for Pb(II) at low concentration. When the concentration of lead ions was higher, the number of binding sites in the bacteria were finite, which led to the amount of lead ions being far greater than the number of binding sites, the ratio of the number of sites reduced, and more lead ions could not be combined in the solution, thus the adsorption rate of lead ions was reduced.

Effect of rotation speed

The effect of rotation speed on the lead adsorption capacity is shown in Figure 5. The results indicated that as the rotation speed increased from 0 to 120 rpm.min−1, the adsorption of Pb(II) increased from 37.47 to 50.01 mg/g, and the maximum biosorption was found at a rotation speed of 120 rpm.min−1. However, adsorption capacity decreased when the rotation speed further increased from 120 to 200 rpm.min−1. This moderate rotation speed gave a better homogeneity to the mixture solution of biomass granulates, and the lead ions had a greater opportunity to bind with the binding sites. At a high rotation speed, vortex phenomena occurred. Lead ions experienced binding instability and the suspension was no longer homogenous, finally resulting in the decrease of adsorption of lead ions. The results are similar to Selatnia et al. (2004).

Figure 5

Effect of rotational speed on the biosorption of Pb2+ ions. Biosorption conditions: Co = 100 mg L−1; 1 g.L−1; pH 6; contact time 12 h, T = 35 °C.

Figure 5

Effect of rotational speed on the biosorption of Pb2+ ions. Biosorption conditions: Co = 100 mg L−1; 1 g.L−1; pH 6; contact time 12 h, T = 35 °C.

Effect of bacterial concentration

Figure 6 shows the influence of bacterial concentration on the lead adsorption capacity. The results show that as the concentration of the bacteria increased from 1 to 5 g.L−1, the percentage adsorption of Pb(II) increased from 46.56% to 95.04%. This may be due to the number of mycelium increasing, thereby increasing the number of corresponding binding sites. Nevertheless, as the concentration of the bacteria further increased from 5 to 7 g.L−1 the percentage adsorption capacity decreased, by 5 percentage points. This may be because the available binding sites increased with bacterial concentration at lower bacterial concentration. However, at higher concentrations of Lactobacillus brevis, the adsorption capacity decreased. This may be because lots of the available binding sites were overlapped or aggregated, which led to the available binding sites of total bacterial surface area decreasing. When the concentration of bacteria was 3 mg/L, the adsorption capacity was almost the largest; as a result, the best amount of bacteria added to the strain was 3 g.L−1. These results were in good agreement with the findings of Pal et al. (2006).

Figure 6

Effect of bacterial concentration on the biosorption of Pb2+ ions. Biosorption conditions: Co = 100 mg.L−1; T = 35 °C; pH6; contact time 12 h, rotation speed 120 rpm.

Figure 6

Effect of bacterial concentration on the biosorption of Pb2+ ions. Biosorption conditions: Co = 100 mg.L−1; T = 35 °C; pH6; contact time 12 h, rotation speed 120 rpm.

The sorption isotherms and kinetics

Four isotherm equations, namely the Langmuir, Freundlich,Redlich-Peterson and Temkin equations, were used to analyze the biosorption data. The equations are represented in Table 1.

Table 1

Isotherm model equations

Adsorption isotherm model Equations 
Langmuir  
Freundlich  
Temkin  
Redlich-Peterson  
Adsorption isotherm model Equations 
Langmuir  
Freundlich  
Temkin  
Redlich-Peterson  

Where qe is the amount of metal ions removed and qmax is the maximum adsorption capacity, ce is the equilibrium concentration (mg.L−1), KL is the Langmuir constant, kf and n are Freundlich constants, kRP, aRP and b are the Redlich-Peterson constants, A and B are the Temkin constants, B = RT/a, and a is binding energy. R is the gas constant (8.314 × 10−3 kJ.mol−1.K−1), T is the absolute temperature (K).

The plot of the observed equilibrium adsorption and the Langmuir, Freundlich, Redlich-Peterson and Temkin isotherms are given in Figure 7. The parameters of Langmuir, Freundlich Temkin and Redlich-Peterson isotherms were calculated and are given in Table 2. It appeared that the adsorption data were well fitted with the four isotherms, but best with Redlich-Peterson equation. The regression coefficient value of the Redlich-Peterson equation is 0.995. It can be known from these models that the bacteria had monolayer adsorption in the adsorption process, and may also have had physical adsorption. The value of n > 2 indicated that the lead ions can be bound easily. The equilibrium adsorption capacity reached 53.632 mg.g−1. Binding energy a = 0.264 k J/mol, which indicates that the adsorption process seems to involve chemisorption and physisorption.

Table 2

Langmuir, Freundlich, Temkin and Redlich-Peterson isotherm model parameters

Model qmax KL  R2 
Langmuir 53.632 0.070  0.989 
Freundlich kf  R2 
2.674 8.138  0.966 
Redlich-Peterson KRP aRP R2 
9.867 0.562 0.791 0.995 
Temkin  R2 
3.559 9.691  0.967 
Model qmax KL  R2 
Langmuir 53.632 0.070  0.989 
Freundlich kf  R2 
2.674 8.138  0.966 
Redlich-Peterson KRP aRP R2 
9.867 0.562 0.791 0.995 
Temkin  R2 
3.559 9.691  0.967 
Figure 7

Fitting with Langmuir, Freundlich, Redlich-Peterson and Temkin adsorption isotherms for Pb(II) adsorption.

Figure 7

Fitting with Langmuir, Freundlich, Redlich-Peterson and Temkin adsorption isotherms for Pb(II) adsorption.

The kinetics of Pb2+ ion adsorption was further investigated. The three kinetic models; namely, the Elovich kinetic model, pseudo-first-order kinetic model and pseudo-second-order kinetic model were used to analyze the biosorption data, respectively. They are given in Figure 8. The equations are represented in Table 3, where qt represents the adsorption capacities of Pb2+ at equilibrium at time t (min) and q is the adsorption capacity at equilibrium, a and b are parameters of the Elovich equation, and k1 (min−1) is the rate constant for pseudo-first-order adsorption. k2 (g.mg−1. min−1) is the rate constant for the pseudo-second-order adsorption.

Figure 8

Fitting with Elovich, pseudo-first-order and pseudo-second-order kinetics for Pb(II) adsorption.

Figure 8

Fitting with Elovich, pseudo-first-order and pseudo-second-order kinetics for Pb(II) adsorption.

Table 3

Kinetic model equations

Kinetic model Equation 
Elovich  
Lagergren pseudo-first-order  
Lagergren pseudo-second-order  
Kinetic model Equation 
Elovich  
Lagergren pseudo-first-order  
Lagergren pseudo-second-order  

The pseudo-first-order, Elovich and pseudo-second-order kinetic parameters are shown in Table 4. The pseudo-first-order kinetics could not describe the adsorption process correctly because of having the lowest correlation coefficients. In most cases, the pseudo-first-order equation can only be used to describe a period of initial adsorption, but cannot be used to describe the whole adsorption process. On the contrary, the pseudo-second-order model provided excellent correlation coefficients (R2 > 0.99). Therefore, it could be inferred that the adsorption fitted with the pseudo-second-order kinetic model perfectly. Thus the adsorption of lead ions by bacteria has a heterogeneous diffusion process.

Table 4

Elovich, pseudo-first-order and pseudo-second-order kinetic parameters

Elovich Pseudo-first-order Pseudo-second-order 
R2 k1 R2 k2 R2 
−40.433 12.218 0.972 46.55 0.003 0.934 55.249 6.935e-5 0.992 
Elovich Pseudo-first-order Pseudo-second-order 
R2 k1 R2 k2 R2 
−40.433 12.218 0.972 46.55 0.003 0.934 55.249 6.935e-5 0.992 

Thermodynamic studies

The thermodynamics of the adsorption process were studied. The experimental data obtained at different temperatures were used in calculating the thermodynamic parameters such as the Gibbs free energy change (ΔG), enthalpy change (ΔH) and entropy change (ΔS). The ΔG, ΔH and ΔS were calculated by the following equations  
formula
(3)
 
formula
(4)
where kc is the equilibrium constant, which can be replaced by the Langmuir constant KL at different temperature, R is the gas constant (8.314 × 10−3 kJ.mol−1.K−1), and T is the absolute temperature (K). ΔH and ΔS were obtained from the slope and intercept of the plot of T−1 against lnkc. The parameters are shown in Table 5.
Table 5

Thermodynamic parameters

T (K) ΔG (KJ/mol) ΔH (KJ/mol) ΔS (KJ/mol.K) 
293.15 −22.713   
303.15 −23.823 9.827 0.111 
308.15 −24.378   
313.15 −24.933   
T (K) ΔG (KJ/mol) ΔH (KJ/mol) ΔS (KJ/mol.K) 
293.15 −22.713   
303.15 −23.823 9.827 0.111 
308.15 −24.378   
313.15 −24.933   

As can be seen from Table 5, the values of ΔG < 0 indicate that the adsorption was spontaneous. The ΔH and ΔS were 9.827 kJ mol−1 and 0.111 KJmol−1 K−1, respectively, with a correlation coefficient of 0.958. The value of ΔH was negative, which indicates that the adsorption reaction is endothermic. The value of ΔS > 0 suggested that the randomness increased during the adsorption process.

CONCLUSION

In summary, in this study the biosorption of Pb(II) ions onto Lactobacillus brevis was studied with respect to the initial pH, temperature, initial metal ion concentration, contact time, bacterial concentration and rotation speed. The optimal condition for Pb2+ ion adsorption was found to be pH 6, contact time of 12 h, rotation speed of 120 rpm.min−1, bacterial concentration of 3 g.L−1 and initial Pb2+ ion concentration of 200 mg.L−1. Moreover, the results showed that the adsorption equilibrium data were well fitted with the four models. It can be known from these that the bacteria had monolayer adsorption in the adsorption process, and the lead ions can be bound easily. The equilibrium adsorption capacity reached 53.632 mg.g−1. Binding energy a = 0.264 kJ/mol indicated that the adsorption process seems to involve both chemisorption and physisorption.

Fitting with three kinetic models, the correlation regression coefficients showed that the biosorption process could be fitted well with the pseudo-second-order and Elovich models. This indicated that a heterogeneous diffusion process happened in the adsorption process. In addition, the adsorption process was endothermic, and increased temperature can promote the adsorption.

It can be concluded that the lactic acid bacterium can be used as a potential biosorbent material for the removal of Pb2+ ions from aqueous solution. Further investigation is required to evaluate the effects of this lactobacillus against Pb2+ toxicity in vivo, application of the microorganisms in dietary strategies for people at risk of Pb2+ exposure, and the mechanisms of Pb2+ ion removal.

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