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Ecotoxicology

, Volume 23, Issue 4, pp 742–748 | Cite as

Cr(III) removal by a microalgal isolate, Chlorella miniata: effects of nitrate, chloride and sulfate

  • Xu Han
  • Yu-Feng Gong
  • Yuk-Shan Wong
  • Nora Fung Yee Tam
Article

Abstract

In the present study, nitrate, chloride and sulfate anion systems were used to investigate the presence of anions on the removal of Cr(III) by Chlorella miniata. Kinetic studies suggested that the equilibrium time of Cr(III) biosorption was not affected by the presence of different sodium salts, even at the concentration of 1.0 M, and all reached equilibrium after 24 h. Equilibrium experiments showed that the effects of different anions on Cr(III) biosorption varied, and the inhibitory order was SO4 2− > Cl > NO3 . Langmuir isotherm indicated that the maximum sorption capacity of C. miniata increased with the increase of pH under different anion systems. The strongest inhibition effect of the sulfate system was attributed to the formation of Cr(OH)SO4 aq. and the decrease of Cr(OH)2+ and Cr3+ in solution, while the difference of inhibitory effect in the other two anion systems could be accounted by the formation of the inner-sphere surface complex in the nitrate system and the outer-sphere surface complex in the chloride system. The present study suggested that the presence of anions greatly affected the removal of Cr(III) on C. miniata and thereby their transport in the environment.

Keywords

Microalgae Biosorption Chromium Langmuir Anion Speciation 

Introduction

Trivalent chromium, Cr(III), is a pollutant commonly found in wastewater produced from leather tanning, dye, wood preservation and electroplating industries. Cr(III) is thought to be an essential nutrient required for sugar and fat metabolism in organisms (Anderson 1997), however, long time exposure also causes skin allergies and cancer (Yun et al. 2001). In addition, Cr(III) can be oxidized to the more carcinogenic and mutagenic Cr(VI) by MnO2 in the environment or by some bacteria in soil under proper conditions (Sethunathan et al. 2005). Therefore, Cr(III) should be removed from wastewater prior to discharge.

In the recent years, biosorption has been widely studied for the removal of metal ions, especially at the concentrations ranging from 1 to 100 mg L−1, due to its lower cost and higher effectiveness than the conventional methods such as chemical precipitation and ion exchange (Kapoor and Viraraghavan 1995). Biosorption of target metal ions might be hindered under the presence of different anions (Pulsawat et al. 2003). However, the effect of anion species on biosorption has always been neglected. The inhibition among different anions such as nitrate, chloride and sulfate varied, depending on different metal cations used in the experiments (Ahuja et al. 1999a, b; Diniz and Volesky 2005; Kuyucak and Volesky 1989; Pulsawat et al. 2003). Metal speciation and chemical complexation with anions in solution seemed to be a possible reason for the decreases of metal cation biosorption in the presence of various anions (Diniz and Volesky 2005; Herrero et al. 2005; Trevors et al. 1986; Tsezos et al. 1996). Kapoor and Viraraghavan (1995) assumed that if the stability constants of metal-anion complexes were greater than that of metal-biosorption sites on the cell-wall surface, the biosorption could be expected to be reduced considerably. On the contrary, Das et al. (2002) found that the presence of anion species, including Cl, C2O4 2−, CH3COO, NO3 and SO4 2− (up to 0.5 M of their individual concentration) in the aqueous solutions had no effect on the sorption of the Pu(IV) (plutonate) by the immobilized Saccharomyces cerevisiae. Texier et al. (1999) also found that the presence of Cl, NO3 and SO4 2− did not affect La(III) biosorption by Pseudomonas aeruginosa.

Cr(III) is a cation and its biosorption performance under the presence of different anions is still unknown so far. Chlorella miniata was a green microalgal species (spherical cells with a diameter of 2–3 μm) isolated from a municipal sewage treatment plant in Hong Kong SAR by the present research team. This isolate had been reported for its high biosorption capacity to Ni(II), Zn(II), Cr(III) and Cr(VI) ions (Chong et al. 2000; Han et al. 2006, 2007; Tam et al. 2001; Wong et al. 2000). The present study therefore aims to (1) evaluate and compare the performance of C. miniata in the removal of Cr(III) in the presence of different anion systems, including Cl, NO3 and SO4 2− (in the form of sodium salts), which are commonly found in industrial wastewater and whose concentrations are very high in some chromium-contained wastewater (Fahim et al. 2006; Suteerapataranon et al. 2006); (2) explore the effect of anion species and its concentration on Cr(III) removal on the basis of metal speciation and removal mechanisms.

Materials and methods

Mass culture of microalgae and preparation of biosorbent

Chlorella miniata was cultivated in a transparent acrylic column, and the culture was illuminated by cool fluorescent light with an average light intensity 4.2 klux in 16/8 h light/dark cycle at room temperature 25 ± 1 °C. The algae were harvested at the stationary phase and centrifuged at 5,000 rpm for 15 min, washed with deionized water twice to remove any residues adsorbed on the cell walls. The washed cells were then freeze dried prior to use.

Cr(III) biosorption experiments

Cr(NO3)3·9H2O was selected as the Cr(III) salt in Cr(III) biosorption experiments. In kinetic studies, the freeze dried algal biomass (5.0 g L−1) was mixed with 100 mg L−1 Cr(III) in different anion systems (nitrate, chloride and sulfate), and the initial concentration for each ion was 1.0 M (in sodium salt). The flask without any sodium salt added was employed as the control. In previous study, pH 4.5 was proven to an ideal value for Cr(III) biosorption under the Cr(III) concentration of 100 mg L−1, and chemical precipitation of Cr(OH)3 could be avoided [Ksp(Cr(OH)3 = 6.3 × 10−31] under such conditions (Han et al. 2006). In kinetic experiments, pH was maintained at 4.5, and adjusted with the addition of 0.01 M NaOH or the respective acid, which means HNO3, HCl and H2SO4 for nitrate, chloride and sulfate systems, respectively. The working volume was 100 mL in a 250 mL conical flask, and liquid solution samples (1 mL from each flask) were collected at regular time intervals and analyzed for residual concentrations of Cr(III).

In the equilibrium experiments, in order to investigate the anion concentration on Cr(III) removal, the freeze dried algal biomass 5.0 g L−1 was mixed with 20 mL Cr(III) at the concentration of 100 mg L−1 in different anion systems, and concentrations of nitrate, chloride and sulfate (in sodium salts) varied from 0 to 1.0 M. pH was maintained at 4.5, and adjusted with the addition of 0.01 M NaOH or the respective acid. A control that did not have any sodium salt at the beginning of the experiment was also prepared.

The biosorption capacity of C. miniata to Cr(III) was determined through mixing the freeze-dried cells of 5.0 g L−1 with 20 mL solution containing Cr(III) at concentrations ranging from 20 to 400 mg L−1 under the anion concentration of 0.2 M. Our previous results suggested that at pH <3.0, the biosorption of Cr(III) on the biomass was pretty low, while at pH >4.5, Cr(OH)3 precipitation would form in solution (Han et al. 2006), therefore, the fixed pH 3.0, 4.0 and 4.5 were used and adjusted with the respective acid during the experiments. In all experiments, samples were agitated on a shaker at 160 rpm at room temperature (25 ± 1 °C). Cr(III) in solution was determined by atomic absorption spectroscopy (AAS) (Shimadzu, AA-6501).

Statistical analyses

In Cr(III) kinetic experiments, a parametric two-way analysis of variance (ANOVA) was used to test any difference in Cr(III) removal percentages among anion species and reaction time. In the equilibrium experiments of anion concentration on Cr(III) removal, a parametric two-way ANOVA was used to test any difference in Cr(III) removal percentages among anion species and concentrations. A parametric one-way ANOVA was also used to determine any significant difference among different anion species under fixed concentrations. A multiple comparison test of Tukey was employed when the ANOVA result showed a significant difference among treatments at P ≤ 0.05. All statistical tests were carried out by software SPSS Version 11 from SPSS Inc. (USA).

Results

Kinetics of Cr(III) biosorption

Kinetics of Cr(III) biosorption were studied in order to determine the equilibrium time. As shown in Fig. 1, kinetic performance of Cr(III) biosorption was similar under different anion systems. The equilibrium time was not affected by the presence of different anions (in sodium salts) even at the concentration of 1.0 M, and all reached equilibrium after 24 h. However, the inhibitory effect of anion species on Cr(III) removal varied. Only 44.5 and 15.8 % of the Cr(III) were effectively removed in chloride and sulfate systems, respectively, which were far less than that of the control (70.7 %). Cr(III) in the nitrate system did not show any inhibitory effect even at 1.0 M nitrate concentration and the Cr(III) removal percentage was comparable with that of the control (P > 0.05). It is obvious that the inhibitory effect of anions on Cr(III) removal decreased in the order of SO4 2− > Cl > NO3 .
Fig. 1

Kinetic of Cr(III) biosorption under different anion systems, each at an initial anion concentration (in sodium salt) of 1.0 M. Mean and standard deviation values of three replicates are shown

Equilibrium experiments in Cr(III) biosorption

In equilibrium experiments, the effect of anion concentration on the performance of Cr(III) biosorption varied, depending on the anion systems (Fig. 2). For the nitrate system, Cr(III) removal at equilibrium was not affected by nitrate concentrations (NaNO3) ranging from 0 to 1.0 M (P > 0.05). In the chloride system, Cr(III) removal decreased steadily with the increase of chloride concentration (NaCl). In the sulfate system, there was a rapid decrease (38.2 %) of Cr(III) removal from 0 to 0.1 M (Na2SO4), but further increase of sulfate to 1.0 M had less inhibition, with an additional 14.4 % reduction in Cr(III) removal.
Fig. 2

Equilibrium study of Cr(III) biosorption under different initial anion concentrations after 24 h (the initial anion concentration of 0.0 M was the control). Mean and standard deviation values of three replicates are shown

In this experiment, the anions came from two different sources. The first source was from the salts added at the beginning of the experiment, and the second was from the respective acid used for pH adjustment. Throughout the experiment, based on the amount of acid used to maintain pH at 4.5, total amounts of anions that came from the acid were approximately 1–10 mM in nitrate and chloride systems, and about 0.5–10 mM in sulfate system. It is obvious that only small amounts of anions came from acids in the control (without any salt addition). In the control, Cr(III) removal percentage remained at about 70.0 %, and different acids had no significant effect on Cr(III) removal (P > 0.05), indicating that the anion effect of the additional acid for pH adjustment could be neglected, and any of the three acids could be used for pH adjustment in Cr(III) biosorption.

The results in Fig. 3 showed that anion effects on Cr(III) biosorption capacity were different and followed the inhibitory order of SO4 2− > Cl > NO3 under different pH values. Cr(III) biosorption capacity increased with the increase of pH, and the maximum biosorption capacity of C. miniata to Cr(III) was evaluated by the Langmuir model, defined as follows:
$$ {\text{q}} = \frac{{{\text{Q}}_{\hbox{max} } {\text{bC}}_{\text{e}} }}{{1 + {\text{bC}}_{\text{e}} }} $$
(1)
where q (mg g−1 biomass) represents the biosorption capacity, Ce (mg L−1) is the equilibrium concentration of Cr(III), Qmax (mg g−1 biomass) is the maximum sorption capacity and b (L mg−1) is the sorption constant.
Fig. 3

Cr(III) biosorption capacity in different anion systems under different pH (anion concentration 0.2 M). a pH 3.0; b pH 4.0; c pH 4.5. The symbols are experimental data and the solid lines are prediction based on Langmuir isotherm (Eq. 1)

Results in Table 1 showed that the maximum sorption capacity increased with the increase of pH in three anion systems, and the high R2 indicated the well description of the sorption isotherm, except the equilibrium data at pH 3.0 in sulfate system, which could be due to the little sorption under the experimental condition.
Table 1

Regression results of Langmuir parameters in the conditions of different pH and anion systems (anion concentration of 0.2 M)

pH

Qmax (mg g−1 biomass)

b (L mg−1)

R2

Controla

NO3

Cl

SO4 2−

Controla

NO3

Cl

SO4 2−

Controla

NO3

Cl

SO4 2−

pH 3.0

14.7

13.7

15.2

b

0.018

0.014

0.005

b

0.962

0.958

0.957

b

pH 4.0

28.7

29.9

30.8

8.8

0.015

0.011

0.005

0.006

0.944

0.984

0.994

0.943

pH 4.5

41.2

42.8

35.3

11.9

0.025

0.014

0.015

0.005

0.951

0.993

0.979

0.974

aControl was the Cr(III) biosorption experiments conducted without sodium salt added, and the data was obtained from our previous results (Han et al. 2006)

bData not available

Speciation of Cr(III)

The speciation of Cr(III) was calculated using the software Mineql+, which was developed by Schecher and McAvoy (1992). The relative abundance of different species of Cr(III) under different anion systems was shown in Fig. 4. Similar speciation was observed in both nitrate and chloride systems (Fig. 4a, b), and Cr3+ and Cr(OH)2+ were the two dominant species. With the increase of initial anion concentration, Cr3+ increased while Cr(OH)2+ decreased and both began to level off when initial anion concentration (as NaNO3 or NaCl) was larger than 0.2 M. The total amounts of other species such as Cr(OH) 2 + , Cr(NO3)2+ and CrCl2+ were <5 % in both systems. The speciation of Cr(III) in the sulfate system was totally different from the above two systems (Fig. 4c). With the increase of initial anion concentration (as Na2SO4), both Cr3+ and Cr(OH)2+ decreased, dropped to 2.9 and 3.8 %, respectively at 1.0 M sulfate concentration, while a new species, Cr(OH)SO4 aq., increased rapidly from 4.8 to 49.5 % when the anion concentration increased from 0 to 0.1 M, and reached 83.4 % at 1.0 M anion concentration. As for the other species, since their percentage was far less than these three species (total amount <5 %), their changes in the experiment were negligible.
Fig. 4

Cr(III) speciation in different anion systems (initial sodium salt concentration 0–1.0 M) in the experiment with 100 mg L−1 Cr(III) and pH kept at 4.5 with the respective acid. a Nitrate system; b chloride system; c sulfate system. In a, b, species Cr(OH)+ was not shown in the figure because its amount was smaller than 5 %, and in c, species such as Cr(OH)+, CrSO4 +, Cr(OH)2SO4 2+, Cr(OH)SO4 aq. and Cr(OH)2(SO4)2 were not shown because their total amounts were smaller than 5 %. Percentages of each species were calculated using the software Mineql+

Discussion

The presence of anions could affect metal cation biosorption, and their inhibition differed among the biomass employed and the metals needing to be removed. Kuyucak and Volesky (1989) found that nitrate significantly inhibited Co2+ biosorption by dead marine brown algae (Ascophylum nodosum), while phosphate and sulfate had no effect. Pulsawat et al. (2003) reported that the inhibitory effect of anions on Mn(II) biosorption by extracellular polymeric substance (EPS) from Rhizobium etli followed the order of Cl > NO3  > SO4 2−. However, the inhibitory order of anion on Zn2+ biosorption by Oscillatoria anguistissima was SO4 2− > Cl > NO3 (Ahuja et al. 1999b). In all these studies, the differences caused by the presence of different anions were not explained and metal speciation was not taken into consideration. Diniz and Volesky (2005) suggested that the formation of the monovalent LaSO4 + was the reason explaining the high inhibitory effect of SO4 2−, followed by Cl and NO3 on La3+ biosorption by seaweed Sargassum polycystum. Herrero et al. (2005) further confirmed that metal speciation was important in Hg(II) biosorption by algal biomass and the binding constants of three mercury species, HgCl2, HgOHCl and Hg(OH)2 formed in the chloride environment were different. In the present study, the inhibitory order for Cr(III) biosorption by C. miniata was SO4 2− > Cl > NO3 , which was the same as the study on Zn(II) biosorpion by Ahuja et al. (1999b).

It is generally believed that the addition of salts in solution can increase the ionic strength of the solution, which has a negative effect on target metal removal (Niu and Volesky 1999, 2003; Schiewer and Wong 2000). However, the rapid decrease of Cr(III) biosorption in the range of 0–0.1 M in the sulfate system could not be totally attributed to the increase of the ionic strength (the ionic strength of 0.1 M Na2SO4 in sulfate system was 0.3 M), since Cr(III) removal percentage at 0.5 M of NaCl or NaNO3 (ionic strength was 0.5 M) was even larger than that at 0.1 M Na2SO4 in sulfate system as shown in Fig. 2. Mowever, it could be found that such a decrease coincided well with the formation of the new species Cr(OH)SO4 aq. (Fig. 4c). Compared to Cr3+, Cr(OH)SO4 aq. was a neutral-charged compound and could not easily adsorb on the negative-charged biomass. Our previous study also showed that Cr3+ and Cr(OH)2+ were the main Cr(III) species adsorbed on the biomass (Han et al. 2006). The decrease of Cr(III) biosorption in the sulfate system could therefore be explained by the sharp decrease of Cr3+ and Cr(OH)2+, and the formation of Cr(OH)SO4 aq. when sulfate was added even at an initial concentration of 0.1 M. In the nitrate and chloride systems, the amounts of Cr(NO3)2+ and CrCl2+ were small (Fig. 4a, b), negating the need of explaining the effects of these two systems.

With the addition of salts, such as Na2SO4, not only could the presence of anions (e.g. SO4 2−) in the solution affect biosorption performance, but the presence of metal cations (e.g. Na+) could also affect the biosorption performance of target metals. It is generally considered that Na+, a cation, could compete with the target metal cation for the adsorption sites by binding on the biomass in electrostatic, but not covalent format, thus inhibiting target metal biosorption (Schiewer and Wong 2000; Chen et al. 1997). Therefore, Cr(III) biosorption in all three systems examined in the present study should decrease as the concentration of Na+ increased. However, the insignificant difference in Cr(III) removal at anion concentrations (as NaNO3) ranging from 0 to 1.0 M (Fig. 2) indicated that the presence of nitrate might enhance the Cr(III) biosorption and counteract the inhibitory effect of Na+, while such a counteraction could not be determined in the other two systems (NaCl and Na2SO4). When studying metal adsorption on oxide and hydroxide surfaces, it was also found that the adsorption of many metal ions exhibited little or no dependence on NaNO3 concentrations, but metal adsorption decreased with increases of NaCl concentrations (Criscenti and Sverjensky 1999). Herrero et al. (2005) even showed that an increase of nitrate salt could slightly enhance mercury uptake by a marine microalga.

The decrease of adsorption with the increase of ionic strength has been interpreted as outer-sphere surface complexation, while insensitivity to ionic strength has been taken as an indicator for inner-sphere surface complexation, which means that metal ions bind directly to the surface with no intervening water molecules, and have a high affinity for surface sites (Hayes and Leckie 1987; Hayes et al. 1988). Our previous study confirmed that surface complexation was the dominant mechanism involved in Cr(III) biosorption by C. miniata and the carboxyl group was proved to be the dominant site for biosorption (Han et al. 2006). The significant change of Cr(III) biosorption in the chloride system, compared with that in the nitrate system (Fig. 2), indicated that Cr(III) more easily formed an inner-sphere complex with the carboxyl group in the nitrate system, but formed an outer-sphere complex in the chloride system. Andrade et al. (2005) also suggested that Ni(II), Pb(II) and Zn(II) formed a more stable surface complex on a green freshwater alga in the nitrate system than in the chloride system. In the sulfate system, since different species of Cr(III) also contributed to its removal, it was not possible to determine what kind of surface complex might be formed based on the present results.

Conclusions

The present study showed that anions had inhibitory effects on the Cr(III) biosorption by the biomass of C. miniata and followed the order of SO4 2− > Cl > NO3 . The formation of Cr(OH)SO4 aq., and the decrease of Cr(OH)2+ and Cr3+ in the sulfate system explained why SO4 2−, even at a low concentration, had the strongest inhibitory effect on Cr(III) biosorption. The inhibitory difference in the other two anion systems could be accounted by the formation of inner-sphere and outer-sphere surface complex in nitrate and chloride system, respectively.

Notes

Acknowledgments

The research work was supported by the Areas of Excellence Scheme established under the University Grants Committee of the HKSAR (Project No. AoE/P-04/2004). The financial support from the National Natural Science Foundation of China (XH, Nos. 41003040 and 41373114), and from Open Funding Project of the Key Laboratory of Systems Bioengineering, Ministry of Education were also acknowledged.

Conflict of interest

The authors declare that they have no conflict of interest.

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Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Xu Han
    • 1
    • 2
    • 3
  • Yu-Feng Gong
    • 2
  • Yuk-Shan Wong
    • 4
  • Nora Fung Yee Tam
    • 5
  1. 1.State Key Laboratory of Hollow Fiber Membrane Materials and ProcessesTianjin Polytechnic UniversityTianjinPeople’s Republic of China
  2. 2.School of Environmental and Chemical EngineeringTianjin Polytechnic UniversityTianjinPeople’s Republic of China
  3. 3.Key Laboratory of Systems Bioengineering, Ministry of EducationTianjin UniversityTianjinPeople’s Republic of China
  4. 4.Department of BiologyHong Kong University of Science and TechnologyKowloonHong Kong, China
  5. 5.Department of Biology and ChemistryCity University of Hong KongKowloonHong Kong, China

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