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Abstract

This work aimed to study the potential for bioremediation of lanthanum by microalgae Ankistrodesmus sp. and Golenkinia sp., as free cells and immobilized in calcium alginate pellets. To reach that goal, studies have been conducted in batch and in continuous fixed bed column. Kinetic models of pseudo-first order and -second order and equilibrium isotherms of Langmuir and Freundlich were used to predict the metal accumulation behavior by free and immobilized biomass in a batch system. The data were best fit to kinetic model of second order, with coefficients of determination (R²) greater than 0.98. Free cells were more efficient in the process than alginate pellets and it was not possible to model the results due to the very fast uptake. Equilibrium modelling indicated that both free and immobilized cells, as well as alginate pellets results were best fit to Langmuir equation due to the high R² value and similarity with experimental results. Dynamic column tests conducted with Ankistrodesmus sp. and Golenkinia sp. immobilized cells during 8 hours presented 80% efficiency in the removal of the metal, without reaching saturation. The high and fast ability of the microalgae to adsorb lanthanum corroborates their potential large-scale application.

Keywords

Biosorption dynamic system immobilization kinetic modelling lanthanum microalgae

Introduction

In view of the potential accumulation of rare-earth elements and its relative toxicity to living organisms, there is a need to find a suitable and economical method for treating solutions containing these ions (Vijayaraghavan et al., 2009). Moreover, it is expected that the growing demand for automobiles, electronics, computers and mobile devices increases in the coming decades. Thus, the concern with the rare-earth elements accumulation in soils became a global environmental issue (Diniz and Volesky, 2005). There are several conventional methods for the removal/recovery of rare-earth elements from industrial effluents. For example, ion exchange resins and solvent extraction are the most known and applied methods (Palmieri et al., 2002; Palmieri and Garcia, 2000). However, these techniques end up by generating new waste, especially by the use of chemical products and adsorbent resins requiring a suitable final destination, incorporating costs to the process (Sert et al., 2008).

From all of the concerns around this problem, biosorption is an alternative for the recovery of industrial dilute aqueous solutions for the recovery of radionuclides and lanthanides and also for the control of water pollution (Awwad et al., 2010; Kushwaha and Sudhakar, 2013; Thomas et al., 2014).

The ability to capture heavy metals by various microorganisms and biopolymers has been reported, whereas bacteria, yeasts, fungi, algae and industrial and agricultural wastes appear as good candidates for removal of these metals. Thus, biosorption process has also been exploited for the selective recovery of more valuable metals (Amirnia et al., 2012; Das and Das, 2014; Ou et al., 2011). The process proceeds through interactions between the metal species and the active sites (carboxyl, amino, sulfate) present on the outer surface of the cell wall of biomass.

Green algae have high metal ion adsorption capacity, due to the composition of their outer surface structure. The predominating mechanisms include ionic interactions and formation of complexes between metal ions and functional groups existing in the cell walls of microalgae. In addition to its high capacity of sorption, microalgae have extensive availability in the environment and are easy to be cultivated (González et al., 2011). These reasons contributed for the selection of the green microalgae Ankistrodesmus sp. and Golenkinia sp., as biosorbents for the removal of lanthanum in this work. No information about the use of Ankistrodesmus sp. and Golenkinia sp. for the biosorption of any chemical element was found. This was the main reason why those microalgal species were selected for uptake experiments. This trivalent metal, lanthanum, presents technological importance in the industrial chain of super alloys, catalysts, special ceramics, among others (Awwad et al., 2010).

Biosorption in batch and continuous systems is the most commonly used procedure for removing metals, as reported in literature (Calero et al., 2009; Ghaed et al., 2013; Oliveira et al., 2012; Palmieri et al., 2002; Plazinski and Rudziński, 2011; Vieira et al., 2007). In a dynamic process of fixed bed column using microalgae as sorbent materials, it is necessary to immobilize the biomass. An immobilization method is simple and can be carried out under very mild conditions, without damaging the cells. The immobilization can provide several advantages, for example, ease of separation and regeneration of the biomass extending its use significantly (Xiong et al., 2009).

In the present work, calcium alginate was chosen as immobilization agent, a biopolymer present mainly in cell wall of brown algae, also able to capture metals. The overall objective of this work was to study the interactions of lanthanum – a representative of the rare-earth elements – with green microalgae of the genera Ankistrodesmus sp. and Golenkinia sp., with the following specific objectives:

To assess the kinetics and equilibrium uptake of lanthanum by microalgal cells of both genera, free and immobilized in calcium alginate, not previously tested for the biosorption of any other chemical element;

To use kinetic and equilibrium models to predict lanthanum uptake behavior, based on the results obtained from both microalgal cells;

To conduct preliminary studies with cells of both genera, immobilized in calcium alginate, under dynamic conditions for the uptake of lanthanum, to evaluate the possibility of scaling-up the process and mainly observe the feasibility of using microalgal cells in continuous systems.

Methodology

Green microalgae

Microalgae Ankistrodesmus sp. (Domain: Eukaryota, Kingdom: Viridiplantae, Phylum: Chlorophyta, Class: Chlorophyceae, Order: Sphaeropleales, Family: Selenastraceae) and Golenkinia sp. (Domain: Eukaryota, Kingdom: Plantae, Division: Chlorophyta, Class: Chlorophyceae, Order: Chlorococcales, Family: Micractiniaceae) were used. Both biomasses were maintained at 23℃ and controlled photoperiod of 12 hours for germination, at pH 7.5. Every 15 days, cells were subcultured in ASM-1 culture medium, which were previously sterilized.

In order to quantify the microalgae Ankistrodesmus sp. and Golenkinia sp. and to define the different stages of growth, a growth curve was obtained by quantification of the cells through direct measurement of the dry mass against time, ensuring that all equilibrium and kinetic experiments were conducted with microbial cells in the same metabolic state. Cells were collected for experiments in the middle of the exponential phase of growth. Growth curves were obtained after 50 days of growth, without a lag phase, due to the continuous subculturing of both cells. The initial Ankistrodesmus inoculum was equal to 0.1 g/L and the exponential phase ranged from the 5th to the 30th day, followed by stabilization of growth at 0.72 g/L. The initial Golenkinia inoculum was equal to 0.1 g/L with the same exponential growth range, followed by stabilization of growth at 0.65 g/L cells. The morphology of both microalgae Ankistrodesmus sp. and Golenkinia sp., as well as the purity of the cultures were confirmed with the help of an optical microscope, at 400 × magnification.

Cells immobilization

Calcium alginate pellets were prepared by dripping an aqueous solution of sodium alginate 4% (w/v) in an aqueous solution of calcium chloride 37% (w/v), in the volumetric ratio of 1:1 under constant stirring (Motta, 2013). The pellets were stored in refrigerator in aqueous solution of 3.7% calcium chloride solution (w/v).

Cultures of Ankistrodesmus sp. and Golenkinia sp. with 18 days of growth were centrifuged and added to the aqueous solution of sodium alginate, thus producing the immobilized cells. The same volume of culture was added to the same amount of sodium alginate solution. Thereafter, the procedure was the same as the production of calcium alginate pellets.

La³⁺ solutions

Standard solutions were prepared with heptahydrated lanthanum chloride (LaCl₃.7H₂O) in distilled water. The pH was adjusted with hydrochloric acid to 4.5 to ensure the ionic configuration of lanthanum (La³⁺). At this pH value, the predominating form of lanthanum in solution is La³⁺. The concentration of lanthanum was determined by ICP-OES (Quimis, Model Q 216-11EX, Brazil), with a 95% confidence level.

Batch studies

For batch experiments, Ankistrodesmus sp. and Golenkinia sp. cultures were used. Free cells and alginate immobilized cells were tested. A blank experiment with cell-free alginate pellets was also conducted. The experiments were performed in triplicate.

Kinetic study

Cultures of Ankistrodesmus sp. and Golenkinia sp. grown for 18 days were used in the kinetic experiments at La³⁺ concentrations of 10 mg/L (0.072 mmol/L) and 100 mg/L (0.72 mmol/L). La³⁺ uptake was studied at 1, 2, 5, 10, 15 and 30 minutes. For the experiments, pellets of alginate and the alginate immobilized cells were established having 10 pellets per flask.

Equilibrium study

Initially a 1000 mg/L (7.2 mmol/L La³⁺) solution was prepared as a stock solution. From this solution, dilutions were made for concentrations of 10 mg/L (0.072 mmol/L La³⁺) to 500 mg/L (3.6 mmol/L La³⁺). Solutions thus prepared were used in equilibrium experiments, under the previously stated conditions during 90 minutes of contact.

Dynamic studies

Based on the results obtained in batch studies, continuous experiments were carried out with the alginate pellets and cells Ankistrodesmus sp. and Golenkinia sp. immobilized in calcium alginate. Dynamic tests were done in a fixed bed reactor 40 cm in height and 4.5 cm internal diameter, containing side ports for sample collection. The tests were performed using the side exit of the reactor to collect the samples, located 20 cm from the base of the column. Twelve liters of a standard solution in a concentration of 150 mg/L (1.08 mmol/L) La³⁺ was fed to the bottom of the column at 25 mL/min, for a period of 8 hours.

Kinetic and equilibrium modeling

Batch system. The amount of lanthanum recovered per unit of free or immobilized biomass (La³⁺ mmol/g biosorbent) was calculated by equation (1).

q_{t} = \frac{(C_{0} - C) V}{1000 w}

(1)

where q_t is the lanthanum sorption capacity at time t (mmol La³⁺/g biosorbent), C₀ and C_t (mmol/L) are the initial and residual concentrations of lanthanum in the solution at times t₀ and t, respectively; V is the volume of lanthanum solution (mL) and w is the mass of the biosorbent (g).

Kinetic models

In order to check the fit of experimental data obtained and to investigate the mechanism involved in the uptake of lanthanum, the kinetic models of pseudo-first order and -second order were used. The model of pseudo-first order or model of Lagergren, in its linear form, is given by equation (2).

\log (q_{e} - q_{t}) = \log q_{e} - \frac{k_{1}}{2.303} t

(2)

where q (mmol/g) is the lanthanum sorption capacity at equilibrium and k₁ (min⁻¹) is the equilibrium constant of the reaction rate of the pseudo-first-order model. The linearized second-order model is expressed according to equation (3).

\frac{t}{q_{t}} = \frac{1}{k_{2} q^{2}} + \frac{1}{q_{e}} t

(3)

where k₂ (g/mmol⁻¹min⁻¹) is the equilibrium constant of the reaction rate of the second-order model.

Equilibrium models

Quantitative evaluation of biosorption of lanthanum was performed by the adsorption isotherms based on the models of Langmuir and Freundlich. The linear mathematical description of the Langmuir isotherm is given by equation (4).

\frac{1}{q_{e}} = \frac{1}{q_{max}} + \frac{1}{q_{max} k_{L}} \frac{1}{C_{e}}

(4)

where q_max (mmol/g) is the maximum sorption capacity, k_L (L/mmol) is the Langmuir constant which indicates the affinity of the biosorbent of the metal and the residual metal concentration in the solution at equilibrium (mmol/L). The linear form of Freundlich equation is given by equation (5).

\log q_{e} = \log k_{F} + \frac{1}{n} \log C_{e}

(5)

where k_F is the Freundlich constant that indicates the adsorption capacity metal and n is a constant related to the strength of adsorption.

Dynamic process

For the evaluation of the continuous process, the normalized concentration (C_e/C₀) versus volume (V) and the uptake efficiency (E_f) versus time (t) were used. The efficiency was calculated as percent recovery against time, as given by equation (6).

E_{f} = \frac{C_{0} - C_{t}}{C_{0}} 100

(6)

C₀ and C_t are the initial concentrations of lanthanum and the equilibrium concentration of lanthanum against time, respectively. It is thus possible to estimate the saturation point of the process (Silva et al., 2010). Only one dynamic condition was tested for both cells and alginate, just to check the viability of using the immobilized cells under continuous operation.

Results and discussion

Biomass growth

Ankistrodesmus sp. reached a maximum growth concentration of 0.72 g/L, while Golenkinia sp. reached a maximum concentration of 0.65 g/L in the same period of 30 days. It could be observed that the absence of a lag phase is probably due to successive subculturing of the original culture.

It was also observed that exponential growth phase occurred between 5 and 30 days for both cultures, with the cells on the same metabolic state, indicating that this is the best range for the cultivation and use of cells in the experiments (Figure 1).

Figure 1.

Growth curves of Ankistrodesmus sp. and Golenkinia sp. cells.

Comparing the environmental physico-chemical conditions used for the growth of cells, such as light intensity, temperature, pH and composition of the culture medium and the work of Converti et al. (2009) and Pérez et al. (2008), it can be seen that the pH and optimum temperature for the growth of microalgae (7.8 and 20–23℃, respectively) were very close to the ones selected in this study. Also, light is the primary factor for the growth of these microalgae, confirming the importance of maintaining the cultures under light controlled periods.

Sipaúba-Tavares et al. (2009) studied the behavior of Ankistrodemsus gracilis in relation to its growth in a distinct culture medium. Authors found that the exponential growth phase of these cells was between 5 and 11 days, followed by a marked decrease in growth. This distinct growth obtained from the literature may be due to the different culture media and culture conditions. In the study of Cometti and Neto (2011), the microalgae Golenkinia radiata was grown in ASM-1 medium for 28 days, not enough for maximum growth. The results obtained in this study with respect to cell growth, were quite satisfactory, partially in accordance to the ones observed in the literature.

Optical microscopy

The micrographs of Ankistrodesmus sp. and Golenkinia sp. cells are shown in Figure 2. It can be seen that the microalgae Ankistrodesmus sp. shows a good distribution of individual cells, disposed crosswise and radial. According to the work of Rodrigues et al. (2010), the morphology of the cells is fusiform, elongated and straight. Golenkinia sp. cells are spherical, isolated and free-floating as described by Schubert (2003).

Figure 2.

Micrographs of Ankistrodesmus sp. (a) and Golenkinia sp. (b). 400× magnification.

The results of the microscopic observation confirmed the purity of both cultures not contaminated by other species, corroborating the study of Blanken et al. (2013) reporting that closed bioreactors provide a good control on the process parameters, such as increased productivity in cells and also highly protecting against invasive species.

Batch studies

Kinetic study

The results of the kinetic study of the biosorption of lanthanum by biomass of free Ankistrodesmus sp. and Golenkinia sp. cells, using solutions at concentrations of 10 and 100 mg/L, respectively, indicated that equilibrium was reached in short periods, both for free Ankistrodesmus sp. free and Golenkinia sp. cells. The extremely rapid stabilization of lanthanum sorption capacity at equilibrium (q), suggested that the application of kinetic models for the theoretical determination of q was not be required. Thus, only q experimental values were presented in Table 1.

Table 1.

Kinetic results of La³⁺ biosorption by Ankistrodesmus sp. and Golenkinia sp. cells.

Biomass	La³⁺ (mg/L)	Exp. q_e (mmol/g)	First order model		Second order model
Biomass	La³⁺ (mg/L)	Exp. q_e (mmol/g)	Calc. q_e (mmol/g)	R²	Calc. q_e (mmol/g)	R²
Ankistrodesmus sp. free cells	10	4.63 ± 0.11	Models did not apply. Fast biosorption observed
Ankistrodesmus sp. free cells	100	6.55 ± 0.21
Golenkinia sp. free cells	10	5.08 ± 0.13
Golenkinia sp. free cells	100	8.73 ± 0.49
Calcium alginate	10	0.19 ± 0.01
Calcium alginate	100	0.66 ± 0.08
Ankistrodesmus sp. immobilized cells	10	0.10 ± 0.00
Ankistrodesmus sp. immobilized cells	100	0.84 ± 0.10	0.79 ± 0.04	0.81	0.82 ± 0.03	0.99
Golenkinia sp. immobilized cells	10	0.14 ± 0.09	0.05 ± 0.00	0.89	0.11 ± 0.00	0.98
Golenkinia sp. immobilized cells	100	0.44 ± 0.02

La³⁺: lanthanum.

The physiological state of biomass (active or inactivated), types of biomaterials, the speciation of the metal ion in the solution and environmental conditions highly affect the biosorption mechanism of rare-earth elements (Das and Das, 2013).

In the present work, a possible explanation for the rapid adsorption of the metal on the biomass is that this phenomenon is due to purely physico-chemical interactions between the surface of the biomass and the solution metal. The process of biosorption by living cells occurs in two stages: at the first stage, the metal ions are rapidly adsorbed on the cell surface through interaction between the metal and the existing functional groups on the outer layer of the cell wall (adsorption). In the second stage, the metal ions gain access to the cell membrane and the cytoplasm of the cell (bioaccumulation). However, Evans (1983) states in his work, that due to the dense nature of the lanthanides, they are able to bind to cell membranes of live cells but not to penetrate it, while easily connecting to the cytoplasm of dead cells. Contributing to this reason, Kratochvil and Volesky (1998) said that this first stage is responsible for about 90% of metal immobilization in the biosorption process using algal cells as biosorbents. It must be pointed out that the advantage of this rapid uptake can be applied in practical applications, i.e. smaller reactors can be used in large-scale biosorption operations.

For the kinetic study with calcium alginate pellets, using La³⁺ solution at concentrations of 10 and 100 mg/L, the results showed that the immobilized biomass showed the same behavior as the free cells, with equilibrium being reached in the first minutes of the process in both concentrations. The rapid stabilization of q, confirmed that it was not possible to model experimental data with kinetic models. Thus, only experimental q values are shown in Table 1. Free cells and calcium alginate beads reached saturation very fast, preventing suitable modeling by both first and second-order models. The same behavior was observed by Ankistrodesmus sp. immobilized cells, when a 10 mg/L solution was used and by Golenkinia sp. immobilized cells, when a 100 mg/L solution was tested. This is probably related to the very small size of Golenkinia sp. cells, which largely contributes to a fast uptake due to the increased surface area, in comparison to Ankistrodesmus sp. cells.

Alginate molecules have very similar binding compounds, than on the surface of microalgae, since this biosorbent material is a constituent of the brown seaweeds wall. Thus, calcium alginate pellets contain high concentrations of carboxyl groups, which represent approximately 70% of active sites available for uptake of metal ions, explaining their equivalent performance in comparison to free cells (Bai et al., 2013).

The results of the kinetic study with Ankistrodesmus sp. and Golenkinia sp. immobilized cells, with La³⁺ solutions at concentrations of 10 and 100 mg/L showed different behavior. The kinetic study of the biosorption of La³⁺ by Ankistrodesmus sp. immobilized cells from a 10 mg/L solution, indicated that equilibrium has been reached in the early minutes of the process, followed by stabilization of q, corroborating that the use of kinetic models is not required (Table 1). In opposition, it was observed that the results from a 100 mg/L of La³⁺ solution, required longer periods of time to reach equilibrium, followed by stabilization of q. The time required to reach equilibrium was equal to 30 minutes (Figure 3).

Figure 3.

Kinetic results of a La³⁺ biosorption by Ankistrodesmus sp. immobilized in calcium alginate (left – 100 mg/L solution) and Golenkinia sp. immobilized in calcium alginate (right – 10 mg/L solution).

In this case, it was possible to check the models against the experimental data, being observed that the equation that best fit the experimental results was the second-order model, based on the higher value of the determination coefficient (R²). Also, a comparison between the experimental q_e and calculated q is presented in Table 2.

Table 2.

Equilibrium results of La³⁺ biosorption based on Langmuir and Freundlich models.

Biomass	Exp. q_max (mmol/g)	Langmuir model		Freundlich model
Biomass	Exp. q_max (mmol/g)	Exp. q_max (mmol/g)	R²	R²
Ankistrodesmus sp. free cells	9.05 ± 0.79	10.43 ± 2.96	0.95	0.81
Golenkinia sp. free cells	5.21 ± 0.38	5.05 ± 0.91	0.94	0.89
Calcium alginate	0.96 ± 0.14	1.23 ± 0.24	0.96	0.77
Ankistrodesmus sp. immobilized cells	1.94 ± 0.27	2.08 ± 0.41	0.97	0.85
Golenkinia sp. immobilized cells	1.09 ± 0.06	1.26 ± 0.07	0.99	0.90

La³⁺: lanthanum.

On the other hand, the kinetic study with immobilized Golenkinia sp. cells presented opposite results: in the experiment with this biomass using the concentration of 10 mg/L of La³⁺, the results indicated that the time required to reach equilibrium increased until the stabilization of q, the time required to reach equilibrium was equal to 15 minutes (Figure 3).

In this case, it was possible to fit experimental data to kinetic models, and it was observed that the equation that best fitted the experimental results was also the second-order model. A comparison between predicted and experimental results can also be found in Table 2. In contrast, the results using 100 mg/L of La³⁺ showed that equilibrium has been reached in the early moments of contact, and it observed stabilization of q, indicating it is not necessary to use kinetic models to explain or predict the behavior of the process.

There are several parameters which determine the rate of adsorption, such as stirring speed of the aqueous phase and structural properties of the support of the biosorbent. Thus, the slow speed behavior of adsorption of La³⁺ by Ankistrodesmus sp. and Golenkinia sp. immobilized cells can be attributed to the resistance found by the solute to diffuse through the membrane to reach functional groups on the surface of the encapsulated biomass. Another author tried to explain the complex interactions between microbial cells and metal elements, using the surface complexation method, concluding that carboxyl, phosphate and hydroxyl groups from the surface of microbial cells readily interact with metal elements in solution (Liu et al., 2013).

The published literature does not present many papers on the use of biomasses for the biosorption of rare-earth elements. Similar tests were performed with other types of biomasses, such as prawn carapace and corn style for the biosorption of cerium (Das and Das, 2014). In these studies, authors performed biosorption experiments at contact times of 2–6 hours, observing a better applicability of the pseudo-first-order model, typical of physisorption.

Equilibrium studies

Results with free and immobilized biomasses of Ankistrodesmus sp. and Golenkinia sp. revealed that, in all cases, the maximum sorption capacity (q_max) could be established. The amounts of adsorbed La³⁺ increased until 100 mg/L (0.72 mmol/L) and 150 mg/L (1.08 mmol/L) concentrations, for free and immobilized Ankistrodesmus sp., respectively; 100 mg/L (0.72 mmol/L) and 50 mg/L (0.36 mmol/L) for free and immobilized Golenkinia sp., respectively; and 100 mg/L (0.72 mmol/L) for calcium alginate pellets. From these values, there was no significant increase in the amount of La³⁺ adsorbed per unit mass of dry adsorbent (q), with equilibrium being reached. Langmuir and Freundlich isotherms were used to predict the theoretical equilibrium values, and it was observed that in all tests, the model that best described equilibrium is the Langmuir equation. q_max values, both experimental and predicted values are shown in Table 2. Nd³⁺, another rare-earth element, was studied by Palmieri and Garcia (2000), with similar results.

They observed that Ankistrodesmus gracilis is very efficient for removing this metal in aqueous solutions; equilibrium experiments performed with the microalgae Monoraphidium sp., indicated a q_max value of 10.48 mmol/g after 2 hours. This value was very close to that observed in the present work with the biomass of free Ankistrodesmus sp. cells, which was 10.43 mmol/g (Figure 4). A comparison of the uptake efficiency with activated charcoal (0.44 mmol/g) concluded that microalgal cells produced best results, mainly due to the chemical and physical characteristics of the cell wall.

Figure 4.

La³⁺ equilibrium sorption by free Ankistrodesmus sp. cells.

Metal adsorption differences can be explained by the properties of each biosorbent, mainly functional groups and surface area. The microalgae, in addition to a high surface area, present amine, carboxyl, phosphate and sulfate groups (Palmieri and Garcia, 2000). The uptake efficiency also depends on some factors such as the diffusivity coefficient and metal speciation in solution, the latter directly related to pH.

In Table 2, it can be seen that both pure alginate pellets and the immobilized microalgae had a maximum uptake capacity smaller than free microalgae. Similarly, it can be seen that free Ankistrodesmus sp. is more efficient than free Golenkinia sp. to capture La³⁺. It is also observed that q_max values for pure alginate pellets and immobilized Golenkinia sp. are very close, indicating that there is no advantage in immobilizing these cells, since the sorption efficiency is almost the same. Adsorption, in this case, can be attributed to alginate.

According to Wu et al. (2010), the adsorption efficiency increases at higher adsorbent amounts. This can be attributed to the fact that higher doses of the adsorbent in the solution result in greater availability of active sites due to the increased surface area of the biosorbent. On the other hand, our results indicated that a greater mass of alginate in the pellets may have led to a reduction in specific adsorption of lanthanum. An increase in alginate pellets dose reduced the amount of metal recovered per unit mass of dry biosorbent. Bai et al. (2013) studied the effect of the amount of the biosorbent biosorption capacity of the metal ion and the biomass by increasing the dose of 10–80 mg of adsorbent; results indicated that q value reduced from 20 to 4.8 mg/g, corroborating that higher metal sorption capacity decreased with the amount of adsorbent. Xu et al. (2011) reached the same conclusion when working with La³⁺ and Ce³⁺ biosorption by Agrobacterium sp. HN1.

The immobilization of the biomass proved to be valid because it is an important step to expand the use of bioremediation process on an industrial scale. Unlike the biomass in its native state, immobilization provides biosorbent particles with appropriate size, density and mechanical strength needed for continuous systems. Das and Das (2014) obtained maximum uptakes of 218.3 mg Ce/g prawn carapace and 180.2 mg Ce/g corn style with the results fitting well to Freundlich model, when prawn carapace was used, suggesting a heterogeneous mode of biosorption, whereas Langmuir model showed the best fit for corn style, suggesting a homogeneous layer of Ce biosorption. In another study, Gao et al. (2015) investigated the sorption of La doped with polyvinyl alcohol with poly-γ-glutamic acid, a PSP gel immobilized particle was produced, reaching an uptake efficiency of 97%. Kinetics followed the second-order model and Langmuir fit experimental data model. Qing (2010) also studied La sorption using bamboo charcoal, in a batch system, reaching a maximum uptake capacity of 120 mg La/g charcoal. The system fitted well to both Langmuir and Freundlich models.

An extensive screening of microbial cells was performed by Tsuruta (2007) to study the biosorption of rare-earth elements. In his work, the author tested 76 strains of 69 species of bacteria, actinomycetes, fungi and yeasts. The author performed batch experiments and concluded that the accumulation of the different elements, in single metal solutions, was equivalent, irrespective of the element and the type of microbial cells. The author reports that Sm accumulation by bacterial cells was around 0.31 mmol/g dry cells. It is important to mention that the author did not work with microalgal cells, as reported in the present paper.

Dynamic study

From the results of the continuous study with calcium alginate pellets and Ankistrodesmus sp. and Golenkinia sp. immobilized biomass, it was observed that after feeding 12 liters of solution La³⁺ in the fixed-bed column, the amount of metal recovered was considerably high: La³⁺ residual concentration was around 0.15 for alginate pellets, 0.20 for immobilized Ankistrodesmus sp. and 0.25 when immobilized Golenkinia sp. was used (Figure 5). It can be seen that, in all cases, saturation of the adsorbing bed was not reached, as represented by the very low C_e/C₀.

Figure 5.

Dynamic biosorption of La³⁺ by calcium alginate pellets, immobilized Ankistrodesmus sp. and immobilized Golenkinia sp. cells.

The performance of the column is related to the length and width of the sorption zone, which extends between the section that is saturated with the metal containing biosorbent and the free zone (Vieira et al., 2007). However, it is expected to state that many other interdependent factors contribute to the efficiency of the process, such as flow speed, metal concentration, the type of biomass, etc.

Oliveira et al. (2012) operated a laboratory continuous system during 14 and 18 days, respectively, to reach saturation with La³⁺ and Nd³⁺. Wu et al. (2010) studied the La³⁺ biosorption by calcium alginate pellets magnetized with iron oxide in a dynamic system. They observed that at low flow rates, the breakthrough curve becomes less steep, positively affecting the interactions of the process such as, for example, the metal ion diffusion through the pores of the support.

From Figure 6, it is observed that calcium alginate pellets and the biomass of Ankistrodesmus sp. and Golenkinia sp. immobilized in calcium alginate were still capable of adsorbing about 86% (0.93 mmol/L), 81% (0.87 mmol/L) and 75% (0.81 mmol/L) La³⁺ present in the aqueous medium, respectively. This means that the saturation of the column was still far from being reached. Therefore, it was not possible to model the system to predict saturation, because equilibrium was rapidly reached (Calero et al., 2009).

Figure 6.

Percent efficiency of La³⁺ biosorption by calcium alginate pellets, immobilized Ankistrodesmus sp. and immobilized Golenkinia sp. cells.

This high efficiency of uptake after 8 hours of test shows that this continuous mode of operation presents several advantages since, in addition to supporting a wide processing time, it diminishes the need for change or regenerate the biomass.

It must be emphasized that the breakthrough time of the reactor is reached when the metal concentration in the effluent reaches the maximum value for disposal, according to the local legislation, thus, giving the total volume of effluent treated by the system.

The breakthrough curve is usually expressed in terms of a normalized concentration defined as the ratio of metal concentrations in the liquid outlet and the column inlet (C_e/C₀) versus time or volume of the effluent to a bed of fixed depth (Calero et al., 2009).

A high efficiency of biosorption, both from alginate pellets, as well as with microalgae immobilized pellets can be observed. A simple calculation leads to the conclusion that high concentration factors were obtained. Before feeding La³⁺ to the continuous system, 12 liters of solution containing the element were to be treated, and after the continuous biosorption, it can be seen that practically the entire La³⁺ was captured by the system, a fact that can be confirmed by the very low ratio C_e/C₀.

Thus, two alternatives are presented: (a) proceed to the desorption of La³⁺ with a mineral acid solution to desorb the element from the adsorbing bed. There is, in this case, an expectation for a high concentration factor allowing the recovery of the lanthanum, after desorption solution by traditional techniques (precipitation, electrolysis, etc.) or (b) proceed with the calcination of alginate and immobilized cells. If it is known that alginate melting point is around 300℃ and La³⁺ is 920℃, a controlled combustion, allowing the complete destruction of alginate only, with Lanthanum remaining mixed with the ashes after combustion of the alginate can be achieved.

The option for desorption or combustion is dependent on the efficiency obtained in biosorption, the cost of preparation of biomass, and the final destination for lanthanum. A careful assessment must be made for the best alternative definition, since the present experiments proved that the continuous system is still far from saturation.

Conclusions

Microalgae Ankistrodesmus sp. and Golenkinia sp., free and immobilized in alginate, presented a high potential for La³⁺ biosorption from aqueous diluted solutions. The short time needed to grow the microalgae confirms the effectiveness of bioremediation processes using this type of biomass.

The biosorbents and La³⁺ reached equilibrium in the batch process within minutes and the kinetic equations used to check the results showed that the second-order model was best fit for all those results that could be modeled, showing very similar results between q_calc and q_exp.

The equilibrium and the coefficient of determination (>0.94) showed that the Langmuir isotherm is best suited to explain the experimental results, presenting q_max values very close to what was observed experimentally.

The free microalgae showed greater potential to capture La³⁺. However, the study showed that the immobilization of such biomaterials does not reduce the sorptive capacity nor the rapid contact between the adsorbent and the solute in the biosorption lanthanum. Thus, in addition to working on continuous system, it is possible to use the immobilized cells in batch mode, without significant losses in biosorption efficiency.

The microalgae Ankistrodesmus sp. showed higher q_max values compared with Golenkinia sp., and, therefore, a higher efficiency in the biosorption of La³⁺ is achieved.

Pellets of pure alginate and Golenkinia sp. immobilized cells showed very similar q_max values, indicating that it is not interesting to immobilize this particular microalga for uptake purposes.

The results of the dynamic study in fixed bed column indicated an excellent performance of microalgae immobilized pellets in capturing La³⁺, as well as when pure alginate pellets were tested. At 8 hours of continuous process, 12 liters of solution containing 150 mmol/L of La³⁺ went through the column and the three biosorbents used still kept 80% of its capture efficiency, indicating a high concentration factor should be obtained. It is important to emphasize that the present results are unique in the published literature, bringing new information about the biosorption of rare-earth elements, and opening the possibility for further application of these biomaterials.

Finally, the information obtained from this study can be useful for the project of biosorption reactors, concluding that if microalgae Ankistrodesmus sp. and Golenkinia sp. were used as biosorbent materials immobilized in alginate, there is no need to design large reactors on an industrial scale, due to the high uptake capacity of the biomaterials.

Footnotes

Acknowledgements

Authors would like to thank CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior) for the scholarship to Fernanda do Nascimento Corrêa and UERJ (Universidade do Estado do Rio de Janeiro) and CNPq (Conselho Nacional do Desenvolvimento Científico e Tecnológico) for the scholarship to Aderval Severino Luna.

Declaration of Conflicting Interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This work was funded by CNPq (Conselho Nacional do Desenvolvimento Científico e Tecnológico) through the Produtividade em Pesquisa – PQ 2015 Program, Grant 302907/2015-7.

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Kinetics and equilibrium of lanthanum biosorption by free and immobilized microalgal cells

Abstract

Keywords

Introduction

Methodology

Green microalgae

Cells immobilization

La3+ solutions

Batch studies

Kinetic study

Equilibrium study

Dynamic studies

Kinetic and equilibrium modeling

Kinetic models

Equilibrium models

Dynamic process

Results and discussion

Biomass growth

Optical microscopy

Batch studies

Kinetic study

Equilibrium studies

Dynamic study

Conclusions

Footnotes

Acknowledgements

Declaration of Conflicting Interests

Funding

References

La³⁺ solutions