Sorption of copper(II) ions in the biomass of alga Spirogyra sp.

Bioelectrochemistry 87 (2012) 65–70

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Sorption of copper(II) ions in the biomass of alga Spirogyra sp. Małgorzata Rajfur ⁎, Andrzej Kłos 1, Maria Wacławek 1 Chair of Biotechnology and Molecular Biology, Opole University, ul. kard. B. Kominka 4, 45–032 Opole, Poland

a r t i c l e

i n f o

Article history: Received 16 September 2011 Received in revised form 16 December 2011 Accepted 17 December 2011 Available online 30 December 2011 Keywords: Heavy metals The alga Spirogyra sp. Sorption kinetics Equilibrium parameters

a b s t r a c t Sorption of copper ions by the alga Spirogyra sp. was investigated to determine the influence of experimental conditions and the methods of sample preparation on the process. The experiments were carried out both under the static and the dynamic conditions. Kinetics and equilibrium parameters of the sorption were evaluated. In addition, the influence was studied of the algae preparation methods on the conductivity of demineralized water in which the algae samples were immersed. The static experiments showed that the sorption of Cu 2+ ions reached equilibrium in about 30 min, with approximately 90% of the ions adsorbed in the initial 15 min. The sorption capacity determined from the Langmuir isotherms appeared highly uncertain (SD = ± 0.027 mg/g dry mass or ± 11%, for the live algae). Under static conditions, the slopes of the Langmuir isotherms depended on the ratio of the alga mass to the volume of solution. The conductometric measurements were proven to be a simple and fast way to evaluate the quality of algae used for the experiments. © 2011 Elsevier B.V. All rights reserved.

1. Introduction The ability to live under diverse conditions and to effectively resist the physicochemical factors makes algae the pioneers in colonizing new environments. The resistance of live algae to heavy-metal ions present in the environment can result from effective excretion of the ions, prevention of the ionic absorption, or tolerance towards the ions in the body cells. The main mechanism algae used to avoid the absorption of heavy-metal ions into their cells is binding the ions to the cell walls. Other strategies include the extracellular secretion of substances that complex the metals to reduce their diffusion across cell membranes into the cells, the intracellular transformation of heavy metals into the less-toxic forms, and reducing the affinity of membrane permeases to facilitate the removal of ions or their organic complexes from the cells [1]. Many studies indicated that the main mechanism of metal sorption in Thallophyta, such as lichens and algae, is the ion exchange in the extracellular structures of the thalli. A secondary mechanism involves the incorporation of metal ions into the intracellular structures. The extracellular ion exchange is faster and reaches equilibrium in a dozen or several dozens of minutes [2-5]. On the contrary, a perturbed homeostasis between the extra- and intracellular fluids returns to equilibrium in several hours. Sorption of heavy metals by dried or live algae has been studied for years. The results show that algae can be successfully used in the

phytoremediation of waters [6-10], in wastewater treatment [25,11-13], and in the biomonitoring of surface waters [6-8,14-27]. Different groups and species of algae exhibit different sorption properties, which depend on the physiological and morphological structures of thalli, on the habitat from which the biomass is taken, and on the way algae are prepared for the analysis [28]. Most frequently, the researchers aim to describe the kinetics of the sorption process, as well as to determine the sorption capacity of algae and the parameters of sorption equilibria [7]. The sorption capacities of algae differ largely. For instance, the algae Cladophora glomerata and Spirogyra sp. displayed the sorption capacity for copper ions equal to 15.0 [29] and 133.3 mg/g dry mass (d.m.) [7], respectively. Probably, such differences result not only from the species diversity, but also from the general methodology of research and the methods of algae preparation. The aims of the presented research were to compare and to optimize the parameters of the sorption of copper ions by the alga Spirogyra sp., both in the static systems (decreasing concentration of copper ions in solution) and in the dynamic systems (constant concentration of copper ions in solutions). The attention was paid to the methods of the alga preparation before the analyses. A proper identification of factors which influence the sorption equilibria is essential for effective application of algae biomass in the phytoremediation of waters and in wastewater treatment, as well as in biomonitoring. For instance, the presented results can be used in the development of a simple biosensor for measuring the contamination of surface waters with heavy metals. 2. Materials and methods

⁎ Corresponding author. Tel.: + 48 77 401 60 42; fax: + 48 77 401 60 50. E-mail addresses: [email protected] (M. Rajfur), [email protected] (A. Kłos), [email protected] (M. Wacławek). 1 Tel.: + 48 77 401 60 42; fax: + 48 77 401 60 50. 1567-5394/$ – see front matter © 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.bioelechem.2011.12.007

Samples of the alga Spirogyra sp. were collected from a weakly contaminated water reservoir in a former gravel quarry located in the Opole city, Poland. The samples were cleaned from plant

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M. Rajfur et al. / Bioelectrochemistry 87 (2012) 65–70

impurities and aquatic organisms, then flushed with demineralized water. Clean samples were either used for the research, or subjected to further preparation. The experiments were carried out using either the live or dried algae. The live algae were used immediately after cleansing. Dehydration of algae was done by lyophilization at 223 K for 20 h, or by evaporation of water either at 323 K for 24 h or at 353 K for 12 h. Solutions of copper sulfate were acidified with nitric acid down to pH 5.00 (± 0.02), in order to avoid precipitation of undissociated hydroxides [7].

Instrument Detection Limit (IDL) and the Instrument Quantification Limit (IQL) for copper were 0.0045 mg/dm 3 and 0.041 mg/dm 3, respectively. The concentration of copper in the most concentrated calibration standard available from ANALTYIKA Ltd., Czech Republic, namely 5 mg/dm 3, was assumed to be the upper limit of the linear relation between the concentration of the analyte and the instrument signal. The conductivity measurements were carried out using a CC551 conductometer from Elmetron, Poland. All chemicals used were purchased from MERCK.

2.1. Determination of kinetic and equilibrium parameters of sorption in static systems (without the solution flow)

2.5. Quality control

In static kinetic experiments, a sample of algae weighing about 0.600 (± 0.001) g d.m. (dry mass or mass after drying) was placed in a perforated container of 15 cm 3 volume and immersed into 200 cm 3 of aqueous solution of copper sulfate. Dried algae were always soaked in demineralized water for 30 min before the experiments. The solutions were intensively agitated with a magnetic stirrer. Each experiment lasted 40 min, with samples of solutions sipped periodically for the AAS analysis of copper. The static equilibrium experiments were carried out almost in the same way as the kinetic ones. The difference was that the mass of algae and the initial concentration of copper sulfate were varied. Moreover, samples of solutions for the analyses of copper were taken only at the beginning and at the end of each 40 min long experiment. 2.2. Determination of equilibrium parameters in dynamic systems (with the solution flow) In dynamic experiments, a sample of algae was placed in a container through which a solution of copper sulfate was flown continuously at 200 cm 3/min. The concentration of dissolved copper ions in the container was found constant throughout each experiment. The runs lasted 40 min each. The concentration of copper in algae was determined before and after each experiment. For this purpose, the algae were mineralized with aqua regia in a microwave mineralizer CEM MARS X. The values determined were corrected for the concentration of copper naturally present in the algae: cCu(a,0) = 0.0078 ± 0.0008 mg/g dry matter. 2.3. Conductometric quality analysis of prepared algae A sample of analyzed algae weighing about 0.040 (± 0.001) g was placed in a perforated container and immersed in 200 cm 3 of demineralized water which had the conductivity of 0.7(±0.1 μS/cm. Then, the conductivity changes were recorded for 3 h. A similar method was applied to evaluate the destruction of cellular membranes in lichens caused by the atmospheric aerosol pollution [30]. 2.4. Analytical instruments and chemicals Copper was determined with an atomic absorption spectrometer SOLAAR 969 from UNICAM/Thermo Electron Corporation, USA. The

The quality control of measurements was assured by test analyses of the BCR 414 plankton and BCR-482 lichen reference materials from the Institute for Reference Materials and Measurements in Belgium. The results obtained are summarized in Table 1. 2.6. The Langmuir isotherm model The Langmuir isotherm model, which is valid for the monolayer adsorption onto a surface containing a finite number of identical sorption sites, can be written in the following form [31]:    −1 cða;1Þ ¼ cða;maxÞ  K  cðs;1Þ  1 þ K  cðs;1Þ

ð1Þ

where: c(a,1)—equilibrium concentration of a given metal in algae (mg/kg), c(s,1)—equilibrium concentration of the corresponding metal ions in solution (mg/dm 3), c(a,max)—sorption capacity of algae (mg/kg d.m.), K—constant. Eq. (1) can be rearranged to the linear form, which is easy to plot and suitable for determination of the Langmuir constants:  −1  −1  −1 cða;1Þ ¼ cða;maxÞ  K  cðs;1Þ þ cða;maxÞ

ð2Þ

3. Results The research was divided into three stages. The first stage included the static kinetic experiments which involved both the live and the prepared algae. In the second stage, static experiments were used to evaluate the uncertainty of measurements and to unveil the influence of the methods of algae preparation on the sorption properties. The third stage, which comprised both the static and the dynamic experiments, was aimed at determination of the equilibrium parameters of the Langmuir isotherm model of sorption. The experimental methods were described in Section 2. 3.1. Kinetics of sorption The static kinetic experiments were carried out to evaluate how fast the sorption equilibria were reached between the algae and the solutions they immersed in Fig. 1 shows how the concentration of copper changed in time in solutions containing the live algae and the algae prepared by various methods. The experimental parameters

Table 1 Measured and certified values of Cu concentration in the BCR 414 plankton and the BCR 482 lichen reference material. BCR 414 plankton Certified value

BCR 482 lichen ± Uncertainty

AAS Mean

D ± SD

(mg/kg d.m.) 29.5 a

1.3

27.8

a

1.9

Certified value

(%)

(mg/kg d.m.)

− 5.8

7.03

Deviation—a difference between a measured value and a certified value, divided by the certified value.

±Uncertainty

AAS

D

Mean

± SD

6.54

0.18

a

(%) 0.19

− 7.0

M. Rajfur et al. / Bioelectrochemistry 87 (2012) 65–70

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Fig. 1. Changes in time of copper concentration in solutions of copper sulphate after immersion of: (a) live algae; (b) lyophilised algae; (c) algae dried at 323 K; (d) algae dried at 353 K.

Fig. 3. Influence of time of alga conditioning in demineralized water on the sorption properties: (a) algae dried at 323 K; (b) lyophilized algae; (c) algae dried at 353 K. The lines show: (1) σ, (2) σ + SD, (3) σ − SD.

were: the initial concentration of copper in solutions— cCu,0 = 17.0 × 10 − 6 (± 1.0 × 10 − 6) mol/dm 3; wet mass of live algae —8.0 g, equivalent to 0.58 g after drying; dry mass of prepared algae —0.58 (± 0.02) g. The results showed that initially, for about 15 min, the live algae and the prepared algae adsorbed copper ions with different intensity. After about 30 min, each sorption process attained a dynamic equilibrium state at which the sorption properties of the algae were comparable. Each algae sample accumulated about 63% of copper ions initially present in the solutions. The experiment was repeated after 30 days, during which the dried algae samples were stored in tightly closed plastic containers. The sorption properties of the dried algae changed—each sample, irrespective of the way the algae had been dried, accumulated only about 50% of the initial amount of copper ions.

Similar uncertainties determined for 0.6 g samples of the lyophilized algae and the algae dried either at 323 K or 353 K were respectively 4.1%, 5.3% and 6.2%. Most probably, the increased uncertainty observed for the live algae resulted from large differences in dry masses of the samples. For instance, when 8 g samples of wet algae were dried, the dry masses obtained were scattered within ± 8.7% around the mean value of σ = 0.604 g. Fig. 3 shows how the sorption properties of the dried, the lyophilized and the live algae changed with time during conditioning in demineralized water The results indicate that the lyophilized algae and the algae dried at 323 K should be immersed in demineralized water for at least 15 min to reach the proper sorption properties. The algae dried at 353 K generally had slightly worse sorption properties. Interesting confirmation of decreased sorption properties of dry algae, as compared to the live algae (Fig. 3), came from the measurements of conductivity of water used for conditioning the algae. Fig. 4 shows the time changes of the mean conductivity of solutions in which the live algae or the dried algae (either fresh or stored for 30 days) were immersed. The samples of prepared algae weighed 0.04 g—the value equal to the mass of live alga dried after the experiment. As already mentioned in Materials and methods, a similar approach has been used to evaluate the destruction of cell membranes in lichens [30]. The presented results proved that the preparation of algae changed their thalli. Cellular structures were damaged so that the ionic substances leaked out and increased the conductivity of solutions.

3.2. Influence of the algae preparation method on the sorption process The uncertainty of measuring the sorption of copper ions by the live algae was estimated be repeating 10 times a selected static kinetic experiment. The initial wet mass of algae was 8 g, while the initial concentration of copper ions in solutions was 17.0 × 10 − 6 (±1.0 × 10 − 6) mol/dm 3. The results are shown in Fig. 2. The uncertainty of copper concentration determined in the live algae after 40 min of sorption was SD = ± 0.027 mg/g d.m. (± 11%).

3.3. Equilibrium parameters

Fig. 2. Sorption of copper ions by the live alga Spirogyra sp. - uncertainty of measurements expressed as the standard deviation SD of the mean σ. The lines show: (1) σ; (2) σ + SD; (3) σ − SD.

The sorption equilibria were studied both for the live and the prepared algae, in the static and dynamic systems. The results were analyzed using the Langmuir isotherm model (Eq. (2)). Fig. 5 shows the Langmuir isotherms obtained for samples of the alga Spirogyra sp. that were immersed in 200 cm 3 of copper sulfate solutions during the static experiments. The mass of each sample was 0.8 g, whether of dry prepared algae or of live algae dried after the experiments. Table 2 contains the parameters of the Langmuir isotherms determined, and their statistical description. Fig. 6 compares the Langmuir isotherms determined for the live algae samples of various dry masses in the static and dynamic systems. The parameters of the isotherms are displayed in Table 3. The statistical description of the Langmuir parameters in Tables 2 and 3 indicates high uncertainty of the sorption capacity measured, as the standard deviation of the b coefficient is higher by an order of magnitude than the mean value of the coefficient itself.

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Fig. 4. Influence of the algae preparation method on the conductivity of demineralized water the algae were immersed in: (a) live algae, (b) lyophilized algae, (c) algae dried at 323 K, (d) algae dried at 353 K, (e) algae dried and stored for 30 days.

Fig. 5. The Langmuir isotherms determined in static experiments for: (a) live algae; (b) lyophilised algae; (c) algae dried at 323 K; (d) algae dried at 353 K.

4. Discussion The results of this work disagree in some points with the literature views. However, the authors generally agree that ion exchange is the main mechanism of heavy-metal sorption by algae, and that in a dozen or few dozens of minutes the sorption is completed in 90% [23-26,32]. The latter conclusion was confirmed by the results presented in Fig. 1. The kinetics of sorption has been described with several models, such as that of Weber and Morris [4,5]. Still, the elementary approach to the heterogeneous ion exchange is better based on a model of a second order reaction [33], even though the approach is difficult to apply because of lacking data on the quality of ions desorbed from algae, and high uncertainty of the algal sorption

Fig. 6. The Langmuir isotherms determined for samples of live algae of various dry masses σ in dynamic experiments (a) σ = 0.39 g d.m., SD = ±0.12 g d.m.; and in static experiments (b–d): (b) σ = 1.42 g d.m./dm3, SD = ±0.10 g d.m./dm3; (c) σ = 2.81 g d.m./dm3, SD = ± 0.18 g d.m./dm3; (d) σ = 4.01 g d.m./dm3, SD = ±0.29 g d.m./dm3.

capacity measured. Table 4 collects the published data on the sorption capacity of various algae species towards specified metals. For comparison, the sorption capacities towards copper of natural sorbents diatomite, bentonite, kaolin, compost, sewage sludge, slag, red mud, apple waste and tea waste were 5.54, 7.59, 4.47, 12.77, 19.3, 30.0, 19.73, 10.8 and 48.0 mg/g, respectively [40,41]. Natural sorbents were also used to clean aqueous solutions from several other analytes such as Pb, Cr, Zn, Cd and polychlorinated insecticides (endosulfan and methoxychlor) [42-46]. Data in Table 4 indicate the algae species significantly differ in their sorption capacities. For instance, the sorption capacity towards copper was 133.3 mg/g d.m. for Spirogyra sp. [7] but only 15.0 mg/ g d.m. for Cladophora glomerata [29]. Unfortunately, the quoted authors had not specified the uncertainties of their measurements. The results collected in Tables 2 and 3 show that the uncertainty of the Langmuir coefficient b = (c(a,max)) − 1, which is used to determine the sorption capacity of algae, is higher by an order of magnitude than the coefficient itself. The most uncertain results were obtained for live algae in the static systems (Fig. 2). The possible explanation is that samples of live alga differed much in dry masses which could be determined only after the experiments. The dynamic method avoided such errors, as proved by high correlation coefficients estimated for the experiments with algae samples significantly differing in mass—σ ±30% (Table 3 and Fig. 6). Another factor that influenced the parameters of the sorption process was the way the algae were prepared for the experiments. Fig. 1 showed only slight differences in the kinetics of copper sorption by the live and the freshly dried algae. It was important that before the experiments, the dried algae had been conditioned by immersing in demineralized water (Fig. 3). The sorption properties of dried algae decreased by about 20% after 30 days of storage, irrespective of the way they had been dried. This conclusion disagrees with published results showing that the dead biomass of the algae Chlorella sp. and Scenedesmus had better sorption properties than the living biomass [28].

Table 2 Parameters of Langmuir isotherms of Fig. 5 (static experiments) and their statistics (standard deviations SDa and SDb, relative standard deviations RSDa and RSDb, and correlation coefficients R2), and the maximal sorption capacity of the algae, c(a,max). Algae Live Lyophilized Dried at 323 K Dried at 353 K

a = (c(a,max) K)− 1 1.87 5.82 5.32 6.30

±SDa 0.30 0.19 0.20 0.54

RSDa (%) 16 3.3 3.8 8.6

b = (c(a,max))− 1 0.007 0.035 0.029 0.051

±SDb 0.97 0.34 0.37 0.84

RSDb (%) 4

1.4 × 10 9.7 × 102 1.3 × 103 1.6 × 103

R2

c(a,max)/(mg/g d.m.)

0.908 0.996 0.994 0.972

137 29 34 20

M. Rajfur et al. / Bioelectrochemistry 87 (2012) 65–70

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Table 3 Parameters of Langmuir isotherms of Fig. 6 and their statistics (standard deviations SDa and SDb, relative standard deviations RSDa and RSDb, and correlation coefficients R2) for the live algae samples of various dry masses σ, and the maximal sorption capacity of the algae, c(a,max). ± SDa

RSDa (%)

b = (c(a,max))− 1

± SDb

RSDb (%)

R2

c(a,max)/(mg/g d.m.)

Static experiments 4.01 1.87 2.81 0.83 1.42 0.227

0.30 0.10 0.023

16 12 10

0.007 0.039 0.067

0.97 0.35 0.17

1.4 × 104 8.9 × 102 2.5 × 102

0.908 0.942 0.959

137 26 15

Dynamic experiments 0.39 0.2035

0.0069

3.4

0.039

0.15

3.8 × 102

0.993

26

σ/g

a = (c(a,max) K)− 1

The sorption properties of the algae (Fig. 1) correlated with the conductivity changes of the demineralized water in which the algae were immersed (Fig. 4). Probably, both the lyophilization and thermal drying of algae caused irreversible changes in the structure of the algae cellular membranes. When soaked with water, the damaged cells more easily released the ionic substances into solutions while their sorption properties declined. Thus, the conductometric measurements constitute a promising and fast method of evaluating the quality of algae used for sorption. The slopes of the Langmuir isotherms in Figs. 5 and 6—a = (c(a,max) K)− 1, where K = k'/ k'' (k' and k'' are the rate constants of a product formation and decomposition)—required some interpretation. Following the example of sorption of heavy metals by lichen, the heterogeneous ion exchange can be treated as a second order reaction, the rate constant of which depends on the initial concentrations of substrates [33], whereas the equilibrium constant K depends on the concentration and type of all cations taking part in the reaction [47]. Cations naturally present in algae, mainly H+, Na +, K +, Ca2+ and Mg2+, also participate in the ion exchange process in copper solution but have different affinities to the active centers. Any change of the algae mass in a static system alters the number of active centers and, consequently, the number of cations which participate in the exchange reaction. Experiments with alga samples of different masses in solutions of equal initial concentrations of copper ions always result in different equilibrium concentrations of dissolved copper and different proportions of desorbed cations. Thus, in the case of Langmuir isotherms determined from static experiments, the slope a should change monotonically with the mass of algae used in experiments, provided the sorption capacity c(a,max) (mg/g d.m. of the sorbent) was constant. Fig. 6 shows that in solutions of equal volumes, the slope a decreased with decreasing mass of algae down to the value determined in the dynamic system. This is an expected result, since in dynamic systems the concentration of copper ions in solutions is constant and does not depend on the

Table 4 Sorption capacity of various algae and the parameters of their preparation for the analyses (temperature of drying—T; time of drying—ts; time of conditioning—tk). Alga type or species

Cladophora glomerata Cladophora glomerata Oedogonium Nostoc sp. Oedogonium Spirogyra sp. Spirogyra sp. Spirogyra sp. Ecklonia maxima Ecklonia maxima Ecklonia maxima Ulothrix zonata Spirogyra neglecta Spirogyra neglecta

Sorption capacity: metal (mg/g d.m.)

Parameters of algae preparation T/K

ts/h

tk/h

Cu; 15.0 Pb; 22.5 Pb; 145 Pb; 93.5 Cd; 31.0 Cr; 14.7 Pb; 140 Cu; 133.3 Cu; 85–94 Pb; 227–243 Cd; 83.5 Cu; 176.2 Cu; 115.3 Pb; 116.1

323 323 343 343 343 – 343 – 373 373 373 373 353 353

24 24 24 24 24 6 24 6–8 24 24 24 5–6 –

– – – – – – – – 3 3 3 0.75 –

References

[29] [29] [34] [34] [35] [36] [32] [7] [37] [37] [37] [38] [39] [39]

mass of algae participating in the sorption. Similar variation of a in static systems has been observed by other authors [48].

5. Conclusions The presented results indicate that the parameters of copper sorption by the alga Spirogyra sp. depend on the experimental conditions and on the way the alga samples are prepared for the experiment. In static systems, the sorption parameters depend on the ratio of the alga mass to the volume of solutions. Such dependence does not occur in dynamic systems. Storing of freshly prepared algae for future use spoils their sorption properties. The quality of prepared algae can be assessed simply by immersing a sample of algae in demineralized water and measuring the conductivity of solution. Thorough identification of factors which affect the sorption and equilibrium processes is extremely important for the research aiming at the application of algae as biosensors of quality of surface waters.

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Małgorzata Rajfur is a science worker (doctor, assistant professor) in Opole University (Poland). She is a graduate of the Mathematics, Physics and Chemistry Faculty of Opole University. Her Ph.D. in environmental engineering was completed at Technical University in Łódź. Her field of research focuses on the use of biota for assessment of pollution of various ecosystems by heavy metals. She has been Member of Organisation Committee of Central European Conferences ECOpole. She has cooperated with Joint Institute for Nuclear Research, Dubna, Russia and University in Hradec Králové, Czech Republic. Andrzej Kłos is a science worker (doctor, assistant professor) in Opole University (Poland). He is a graduate of the Mathematics, Physics and Chemistry Faculty of High School of Pedagogics in Opole. Doctor in chemical science (Military University of Technology in Warszawa). Ph.D. in technical science (Faculty of Process Engineering and Environment Protection, Technical University in Łódź). Secretary of Chemistry and Ecological Engineering Society. Member of Organisation Committee of Central European Conferences ECOpole. Scientific interests: biomonitoring and monitoring of environment, environmental chemistry, environment protection, membrane processes. International cooperation: Joint Institute for Nuclear Research, Dubna, Russia, University in Hradec Králové, Czech Republic. Maria Wacławek is full Professor of technical sciences at the Opole University (Poland). She is Editor-in-Chief of 2 scientific journals. She is an EU expert in the field of renewable energy sources. She has been a supervisor of 4 doctoral theses. She is the author and co-author of 190 scientific papers (mainly in indexed journals) and six scientific monographs. She has been the coordinator of many international and national research projects. She serves as a Deputy Dean of Faculty of Natural and Technical Sciences at the Opole University. She is an organiser of Central European Conferences ECOpole.