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Effects of bloom-forming cyanobacterial extracellular polymeric substances on the adsorption of cadmium onto kaolinite: behaviors and possible mechanisms
© Kuang et al. 2016
Received: 14 October 2015
Accepted: 20 April 2016
Published: 27 April 2016
Cyanobacterial blooms result in high level of cyanobacterial extracellular polymeric substances (EPS) in water. The effects of bloom-forming cyanobacterial EPS on the distribution of Cd(II) in the interface between sediment and water is unknown. Clay is a main component in sediment. The effects of EPS, originated from a typical bloom-forming cyanobacterium Microcystis aeruginosa, on the adsorption and desorption characteristics of Cd(II) by kaolinite were investigated in this study. Results of XRD analysis indicated that cyanobacterial EPS bound on the surface of kaolinite. The composite of kaolinite + EPS showed higher adsorption capacity toward Cd(II) than pure kaolinite, and hydroxyl groups were involved in the adsorption processes. The data for the adsorption of Cd(II) by kaolinite are well fitted by both Langmuir model and Freundlich model, whereas only Freundlich model well describes the adsorption data of Cd(II) by the composite of kaolinite + EPS. The adsorption of Cd(II) onto kaolinite was an exothermic process, but it became an endothermic process after EPS incorporation. Results of desorption showed that EPS incorporation increased the adsorption of kaolinite toward Cd(II) through physical adsorption, ion exchange and complexation.
Heavy metal ions are toxic, non-biodegradable and can accumulate through food chain. Heavy metal pollution has caused serious ecological problems and posed a great health risk to human. Cadmium is a most hazardous heavy metal due to its high toxicity and carcinogenic effects (Son et al. 2012). In recent decades, industrial effluent and agricultural run-off caused widespread cadmium contamination in aquatic environments (Öztürk et al. 2009; Florian et al. 2011).
Another world wide water problem is the eutrophication and harmful algal blooms. Microcystis is a typical bloom-forming cyanobacterium. It frequently dominates in eutrophic fresh waters. Take China as an example, two large lakes, Lake Taihu and Lake Dianchi, were all received severe Microcystis based water blooms (Ye et al. 2009; Wu et al. 2014). Microcystis could maintain very high cell density in water during bloom formation stage. Ye et al. (2009) reported that the total cyanobacterial density (mainly as Microcystis) reached as high as 2.93 × 1011 cells/mL in Lake Taihu, China. Microcystis can excrete EPS into water. High cell density of Microcystis frequently results in high concentration of EPS in water column. Xu et al. (2013) reported that the EPS in cultures of Microcystis aeruginosa researched 130 μg per 107 cells. The main component of EPS in Microcystis culture is polysaccharides, and then followed by proteins (Xu et al. 2013). EPS enrich hydroxyl groups, carboxylic groups, acetylated amino, and also contain some noncarbohydrate constituents, e.g. phosphate and sulfate (De Philippis et al. 2011). These chemical groups in EPS can effectively bind with heavy metal ions through ions exchange or complexation (Gong et al. 2005; Fang et al. 2011).
Clay is a main component in sediment (Hou et al. 2013). Previous studies indicated that bacterial EPS could be absorbed by clays and sediments through hydrogen bonding and some other chemical bondings (Pierre et al. 2014; Cao et al. 2011; Fang et al. 2012). EPS addition changed the adsorption characteristics of heavy metal ions by clays, which in turn changed the concentration of heavy metal ions in water (Fang et al. 2010). The major part of heavy metal ions in aquatic environment is deposited in sediment through precipitation, sorption and complexation. The deposition of heavy metal ions from water column to sediment would decrease their concentration in water, and then decrease their bio-toxicity, and vice versa. Thus, studying on the transfer of heavy metal ions between water–sediment systems is crucial in evaluation of the ecological effect and the health risk of heavy metal contamination in aquatic environment.
The structures of EPS originated from different bacteria are different (Pereira et al. 2009). Though the effects of some bacterial EPS, e.g. originated from Pseudomonas putida, Bacillus subtilis, on the adsorption characteristics of heavy metal ions onto clays were studied (Fang et al. 2010; Mikutta et al. 2012), the effects of the EPS, originated from bloom-forming cyanobacteria, on the adsorption characteristics of heavy metal ions by clays remain unknown. In order to elucidate the transfer characteristics of Cd(II) in eutrophic water received cyanobacterial blooms, the effects of EPS originated from Microcystis on the adsorption and desorption characteristics of Cd(II) by kaolinite and their possible mechanisms were investigated in this study.
Cyanobacterial strain, culture conditions, EPS extraction, and reagents
Bloom-forming cyanobacterial strain M. aeruginosa NIES-843 was originated from the National Institute of Environmental Science, Japan, and was kindly provided by Professor Renhui Li (Chinese Academy of Sciences). M. aeruginosa NIES-843 was grown axenically in CT medium (Ichimura 1979) at 25 ± 1 °C under a photoperiod cycle of 12:12 light/dark. The light intensity was set as 30 μmol photons/(s m2). The cell free cultures of M. aeruginosa NIES-843 were collected at stationary phase by centrifuge at 10,000×g for 10 min. The EPS in the cultures was purified in deionised water (18 MΩ cm) using dialysis bags (1000-Da cutoff). The purified EPS solutions were dried using vacuum freezer, and then stored at −20 °C. CdCl2·2.5H2O and other reagents used in this study were purchased from Sinopharm Group Chemical Reagent Ltd. (Shanghai, China), and were of analytical grade.
Preparation of kaolinite
Kaolinite was purchased from Shanghai 54 Chemical Reagent Ltd (Shanghai, China), and it was further purified by washing with ethanol for 3 times, and then followed by washing with deionised water (18 MΩ cm) for 3 times. The fractions of kaolinite, less than 2 μm, were prepared according to the method described by Cai et al. (2006).
Adsorption experiments and adsorption isotherm
X-ray diffraction and Fourier transform infrared spectroscopy analysis
The crystal structures of kaolinite and the composite of kaolinite + EPS were recorded using a XRD-6000 instrument (Shimadzu Seisakusho Ltd., Japan) employing graphite monochromatized Cu Kα radiation, with scanning rate of 4°/min and ranging from 5° to 75°. Fourier transform infrared (FT-IR) spectra of kaolinite and the composite of kaolinite + EPS were obtained on a spectrometer (PerkinElmer Spectrum 65, Perkin-Elmer Co., Norwalk, CT, USA).
Desorption of Cd(II)
Desorption of Cd(II) from the kaolinite and the composite of kaolinite + EPS was performed using deionised water or NH4NO3 or EDTA as desorbent according to the methods previously described by Fang et al. (2011).
Statistical analysis was done by one-way ANOVA using SPSS (version 13.0, SPSS Inc., Chicago, IL, USA). Difference was considered to be significant at P < 0.05 (LSD).
Effects of EPS on the adsorption of Cd(II) by kaolinite
Characteristics of Fourier transform infrared spectroscopy
Characteristics of X-ray diffraction
Effect of pH on the adsorption characteristics
Different initial Cd(II) concentration and adsorption isotherm
Parameters of Langmuir model and Freundlich model for the adsorption of Cd(II) onto kaolinite and the composite of kaolinite + EPS
q max (mg/g)
Kaolinite + EPS
Effect of temperature on adsorption characteristics
The interlayer spacing of kaolinite is 0.716 nm. Only small high polar molecules can enter into the interlayer of kaolinite (Tang et al. 2015). The EPS are large bio-molecules. The size of EPS is far larger than the interlayer spacing of kaolinite. Results of XRD determination showed that cyanobacterial EPS addition and Cd(II) adsorption did not affect the diffraction patterns of kaolinite, indicating that the EPS and Cd(II) all bound on the surface of kaolinite and not intercalated into the interlayers.
The main absorption bands corresponding to C–O, C=O, and O–H are presented in EPS in this study. They are in consistent with previous studies that polysaccharides are the main constituents of bacterial EPS (Xu et al. 2013). Compared with the vibrational spectra of kaolinite + EPS before Cd(II) adsorption, no new absorption band was found after Cd(II) adsorption for this treatment. However, we also noted that the vibration intensity of the band corresponding to –OH was strong in the treatment of kaolinite + EPS before Cd(II), but it became weak after Cd(II) adsorption. Thus, we deduced that hydroxyl groups were involved in the adsorption of Cd(II) by the composite of kaolinite + EPS.
Langmuir model is known as monolayer sorption, while the Freundlich model is suitable to multilayer sorption (He and Chen 2014). Our results indicated that both Langmuir model and Freundlich model were all well fitted by the data originated from the adsorption of Cd(II) by kaolinite, and the deduced q max from Langmuir model was in consistent with experimental data. However, the adsorption isotherm of Cd(II) by the composite of kaolinite + EPS was only suitable to Freundlich model but not Langmuir model since the deduced q max from Langmuir model was far lower than experimental data. Thus, we deduce that the addition of cyanobacterial EPS increased the heterogeneity on the surface of kaolinite. The parameter n from Freundlich model reflects the affinity between adsorbent and adsorbate. The value of n for the composite of kaolinite + EPS is higher than that of pure kaolinite, suggesting that the composite of kaolinite + EPS has higher affinity toward Cd(II) than pure kaolinite.
As for the thermodynamics of the adsorption of Cd(II) by kaolinite, previous studies gave complex and contradictory conclusions. For example, Sari and Tuzen (2014) reported that the adsorption of Cd(II) onto kaolinite was an exothermic reaction while it was described as an endothermic reaction by Angove et al. (1998). Results in this study supported the conclusion that it was an exothermic reaction since the increase of temperature decreased the adsorption of Cd(II) by kaolinite. As for the composite of kaolinite + EPS, the adsorption of Cd(II) by this composite increased along with the increase of temperature, and it exhibited as an endothermic process. The adsorptions of EPS toward Pb(II) and Zn(II) were reported as endothermic processes (Wang et al. 2013). Thus, we deduced that the adsorption of EPS on the surface of kaolinite response for the shift from exothermic process (kaolinite) to endothermic process (composite of kaolinite + EPS).
The fractions of Cd(II) desorbed by deionised water corresponding to physical adsorption ones (Fang et al. 2011). Ammonium nitrate could release the part of Cd(II) adsorbed by physical adsorption and ion exchange (Brady and Tobin 1995). EDTA could release the part of Cd(II) adsorbed through physical adsorption, ion exchange, and the complexation with carboxylic groups, acetylated amino and phosphate (Volesky and Holan 1995; Li et al. 2010). Compared with the treatment of pure kaolinite, the ratio of desorbed Cd(II) by H2O, NH4NO3, and EDTA all increased in the treatment of kaolinite + EPS, suggesting that EPS addition increased the adsorption of Cd(II) by kaolinite through physical adsorption, ion exchange, and complexation.
Cyanobacterial EPS bound on the surface of kaolinite. The composite of kaolinite + EPS showed higher adsorption capacity toward Cd(II) than pure kaolinite, and hydroxyl groups were involved in the adsorption process. The addition of cyanobacterial EPS increased the heterogeneity on the surface of kaolinite, and change the thermodynamics from exothermic process to endothermic one.
The experiments were conceived and designed by JS and JG. The experiments were performed by XK, SL and LP. The reagents/materials/analysis tools were provided by JS and GW. The manuscript was written by JS. All the authors read and approved the final manuscript.
The work was supported by the National Natural Science Foundation of China (No. 31470511); the Foundation of National Water Science and Technology Projects of China (2014ZX07206001-03); Foundation from Education Department of Hunan Province (14B084).
The authors declare that they have no competing interests.
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