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Biosorption of uranium by immobilized Saccharomyces cerevisiae
Journal of Environmental Radioactivity 213 (2020) 106158
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Biosorption of uranium by immobilized Saccharomyces cerevisiae Can Chen a, Jun Hu a, Jianlong Wang a, b, * a b
Collaborative Innovation Center for Advanced Nuclear Energy Technology, INET, Tsinghua University, Beijing, 100084, PR China Beijing Key Laboratory of Radioactive Waste Treatment, Tsinghua University, Beijing, 100084, PR China
A R T I C L E I N F O
A B S T R A C T
Keywords: Uranium Biosorbent Biosorption Microbial immobilization Saccharomyces cerevisiae
A novel biosorbent was prepared and applied for the removal of uranium from aqueous solution. A new immobilization method was studied and used to embed living yeast cells of Saccharomyces cerevisiae (2% w/v) by sodium sulfate (0.5 mol/L) based on saturated boric acid-alginate calcium cross-linking method. The swelling ratio, hydraulic and chemical stability and bioactivity of immobilized microbial cells were examined. Their ultramicrostructure and property were observed by SEM, TEM and FTIR techniques. The influencing factors, such as contact time, initial uranium concentration, and initial pH were investigated. The adsorption capacity of bio sorbent increased from 0.75 to 113.4 μmol/g when the equilibrium concentration of U was 0.9, and 43.9 μmol/L, respectively. U adsorption followed pseudo first-order kinetic model. SEM-EDS and TEM-EDS observation indicated that uranium was adsorbed both on the surface and the inner parts of the biosorbent. FTIR and the XPS results confirmed the role of oxygen in capturing uranium from aqueous solution. XPS analysis showed that the mixture of U (VI) and U (IV) existed on the surface of biosorbent, which evidenced that uranium was micro biologically reduced.
1. Introduction Uranium pollution may originate from uranium mining and its application (Wang and Zhuang, 2019b). Adsorption process is regarded as a promising cost-effective biotechnology to take radionuclides including uranium away from (waste) water (Wang et al., 2018; Wang and Zhuang, 2019a). Biosorption is a promising technology for the removal of radionuclide from radioactive wastes (Wang and Chen, 2009; Zhu et al., 2012, 2014; Bagda et al., 2017). Preparation and use of “good” biosorbents for real application is still a big challenge (Wang and Chen, 2006, 2014). Cell immobilization is an alternative method to improve biosorbent with higher mechanical strength and/or stability. Suitable carrier materials are important. Natural polymer such as algi nate (SA) is widely explored due to its good cell compatibility, cheap and easy preparation using calcium chloride as the crosslinker. However, pure SA-Ca gel bead is unstable in alkaline or phosphate-containing wastewater. Polyvinyl alcohol (PVA) is non-toxic and cheap and owes high durability in water. Thus PVA become a popular synthetic polymer material to prepare immobilized cells using saturated boric acid as the crosslinker, which is regarded as a simple and economical technique of cell immobilization. However, the crosslinking rate is slow of PVA-boric acid method (Takei et al., 2011). PVA-SA gel beads cross-linked using
the mixed aqueous solution containing saturated boric acid and calcium chloride are thus supposed, reported and utilized for microorganism immobilization. Alginate can help PVA rapidly form spherical gel beads (Idris et al., 2008; Takei et al., 2011), decrease the agglomeration of the PVA beads and improve the surface properties of the beads (Zain et al., 2011). Graphene oxide (GO) as a new carbon material is reported to improve the polymer gel properties such as mechanical strength and thermal stability (Zhang et al., 2011; Abdullah et al., 2017; Ege et al., 2017). GO enhanced the performance of the immobilized dead cells entrapped in PVA-SA gel for uranium removal from aqueous solution (Chen and Wang, 2016). However, for living cell immobilization, the crosslinker boric acid is toxic to living microorganisms (Becker et al., 2011; Gunes, 2013). Saturated boric acid solution is highly acidic, which could cause the drastic cell viability loss of the microorganisms enclosed in the gel matrix (Takei et al., 2011; Li et al., 2014). Moreover, a large amount of the hydroxyl groups without involving reaction with boric acid on the beads are prone to form hydrogen with water, and show a high degree of swelling in aqueous solution. Some measures were suggested to improve the PVA-boric acid method. The freezing-thawing cycle method for PVA gel bead prepara tion is reported (Ariga et al., 1987; Lozinsky and Plieva, 1998). The
* Corresponding author. Energy Science Building, INET, Tsinghua University, Beijing, 100084, PR China. E-mail address: [email protected] (J. Wang). https://doi.org/10.1016/j.jenvrad.2020.106158 Received 11 November 2019; Received in revised form 31 December 2019; Accepted 2 January 2020 Available online 7 January 2020 0265-931X/© 2020 Elsevier Ltd. All rights reserved.
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freezing-thawing method is clean and ecofriendly. However, high en ergy consumption, unsatisfactory water resistance due to physical crosslinking and unavoidable loss of cell viability during freezing-thawing cycles blocked the real commercial application of cy clic freezing-thawing process in PVA gel bead preparation (Liao et al., 2018). Chemical crosslinking agents such as sodium sulfate (Zain et al., 2011), sodium nitrate (Chang and Tseng, 1998) or sodium phosphate (Wang et al., 2007) were utilized to strengthen the traditional PVA-boric gel beads. In our previous reported study, immobilization of activated sludge using sodium sulfate for PVA/SA-boric/calcium gel beads showed higher microbial activity and relatively high mechanical sta bility (Mao and Wang, 2013). Sodium sulfate was used to prepare the stable PVA-boric acid beads for invertase immobilization (Idris et al., 2008). X-ray diffraction results indicated that sodium sulfate promoted crystallization of PVA. Moreover, the toxicity of sodium sulfate to the yeast cells was lower than that of boric acid (Takei et al., 2011). The combination of sodium sulfate, GO from industrial scale pro duction, commercial active dry yeast (living Saccharomyces cerevisiae) and PVA/SA-boric/calcium chloride solution to prepare the gel beads for uranium removal has never been reported to the best of our knowledge. The sulfate-strengthened novel gel beads were character ized. The uranium adsorption performance of the gel beads under different contact time, initial uranium concentration and initial pH were presented. The process of cation (sodium, potassium, calcium, magne sium) release and the possible mechanism were analyzed using ICP-OES (Inductively Coupled Plasma Optical Emission Spectrometry), SEM (scanning electron microscopy with energy), TEM (transmission elec tron microscope), EDS (dispersive X-ray spectrum), FTIR (Fourier transform infrared spectroscopy) and XPS (X-ray photoelectron spec troscopy) technique methods.
2.3. Gel bead characterization The gel bead size was determined by measuring 20–30 gel beads using vernier calipers. The ratio of the dry weight and wet weight (dried at 80 � C to constant weight) was calculated. The diameters of gels beads before and after soaking in deionized water for 10 days were set as d1 and d2, respectively. The swelling ratio of beads (d2/d1) was determined. The hydraulic stability of the beads. The tubes containing 20 gel particles soaked in deionized water of 40 mL were put into a recipro cating oscillating machine. They were then acutely shaken (200 rpm) for 12 h. The broken ratio was calculated. The chemical stability. The gel beads were soaked in deionized water, hydrochloric acid (0.1 mol/L), sodium chloride (0.1 mol/L), 0.1 M sodium hydroxide (0.1 mol/L), 0.1 M sodium hydrogen carbonate (0.1 mol/L), or 0.1 M monosodium phosphate (0.1 mol/L) for 10 days, respectively. The swelling ratio and bead weight change before and after soaking in solutions were measured and calculated. The fermentation activity. YEPD solution contained glucose (20 g/L), tryptone (20 g/L) and yeast extract (10 g/L) was prepared. 4.0 g (wet weight) gel beads were put into 100 mL sterilized YEPD solution and then cultured for 24 h. High performance liquor chromatography (HPLC, Shimadzu LC-20AD, Tokyo) measured the level of glucose and the alcohol in solution. 2.4. Uranium biosorption experiments Ten gel beads were added to 10 mL uranium solution in a bottle. The bottles were shaken (150 rpm) at 30 � C. After reaction, the solution was screened by 0.22 μm filter membrane. The concentration of U, K, Ca, Na and Mg ions in the filtrate were analyzed by ICP-OES (IRIS Intrepid II, Thermo). The duplicate was performed. The uranium biosorption quantity by the gel beads was calculated as follows:
2. Materials and methods 2.1. Materials The commercial powder of living Saccharomyces cerevisiae was pur chased from a local supermarket, produced by Angel Yeast Co., Ltd in China. PVA, SA, calcium chloride, boric acid, sodium hydrate, hydro chloric acid, sodium chlorite, sodium hydrogen carbonate, monosodium phosphate, nitric acid, glucose, tryptone and yeast extract were bought from the market in China. SA was produced by Tianjin Guangfu Fine Chemical Research Institute, China. PVA was produced by Sinopharm Chemical Reagent Co., Ltd; calcium chloride, boric acid, sodium hy drate, hydrochloric acid, sodium chlorite, sodium hydrogen carbonate, monosodium phosphate, and nitric acid were offered by Sinopharm Chemical Reagent Co., Ltd. Glucose was produced by Xilong Chemical Co., China. tryptone and yeast extract were produced by Oxoid LTD. Graphene oxide produced at industrial scale were supplied by Ulanqab Darsen Graphite New Materials Co., Ltd. Uranium solution were sup plied by a nuclear institute in China.
q (μmol/g) ¼ (C0-Ct) � V/W The removal efficiency (η) was calculated as follows:
η (%) ¼ (C0-Ct) / C0 Where: t was contact time (min); C0 was the initial uranium concen tration (μmol/L); Ct was residual uranium concentration at the time t (μmol/L); V was the solution volume for biosorption (mL); W is the dry weight of the biosorbent (g). 2.5. Characterization of biosorbent The gel beads were cleaned and dried for SEM–EDS analysis using a FEI Quanta 200 FEG SEM (Holland) or SU-8010 (Hitachi, Japan) with EDS equipment. The ultrathin section specimen of the gel beads were obtained by an ultramicrotome (Leica EM UC6) for TEM-EDS analysis (JEM2010 or HT7700, Japan). The gel beads were washed and lyophilized for FTIR analysis using potassium bromide (Potassium bromide) method (FTIR spectrometer, Bruker). The XPS spectra of the gel beads were recorded on a spectrometer (PHI Quantro SXM, ULVAC-PHI Co., Japan). Surface charging effect was corrected with C1s peak at 284.8 eV as the reference. High resolution U 4f, O 1s, C 1s peaks and Ca 2p were fitted using the XPS PEAK 4.1 program after subtracting the background (Shirley baseline correction).
2.2. Immobilization procedure The homogeneous solution containing PVA (5%, w/v), SA (1%, w/v), GO (0.05%, w/v) and the living yeast power (2%, w/v) was dropped into the saturated boric acid -calcium chloride (1% w/v) solution and immersed for 0.5 h with gentle stirring. The beads were then transferred to 0.5 M sodium sulfate aqueous solution and immersed for 2–4 h with gentle stirring. The gel beads were then washed and then stored at 4 � C for further use, called sulfate treated-gel bead. The homogeneous solution containing PVA (5%, w/v), SA (1%, w/v), GO (0.05%, w/v) and the living yeast power (2%, w/v) was dropped into the saturated boric acid -calcium chloride (1% w/v) solution and immersed for 4 h, without sulfate treatment. The gel beads were then washed and then stored at 4 � C for further use, called PVA-SA-GO-yeast gel beads.
3. Results and discussion 3.1. Characterization of gel beads The sulfate-improved novel gel beads were successfully prepared. 2
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Fig. 1. Surface morphologies of the PVA-SA-GO-yeast gel beads before (upper: a � 2000, b � 5000) and after (lower: c � 2000, d � 5000) sulfate treatment.
The mean size of the wet gel beads was 0.38 � 0.00 cm. The ratio of dry weight and wet weight was 0.106. None bead was broken in water after acutely shaken for 12 h. The swelling ratio of the wet gel beads after contact for 10 days with H2O, 0.1 M NaCl, 0.1 M NaOH, 0.1 M NaHCO3 and 0.1 M NaH2PO4 reached 1.31, 1.05, 1.21, 1.19, 1.22 and 1.19, respectively. The gel beads were able to maintain their raw spherical shape in the above mentioned aqueous solution. Compared with pure water, the gel beads tend to shrink in acid, salt or alkaline. The sulfatemade gel beads were thus expected to adapt good to the real wastewater usually containing acid, alkaline or salt. The 4 g gel beads utilized the 99.4% glucose of YEPD culture with initial glucose concentration of 16.3 g/L. The ethanol yield (6748.5 mg/L within 24 h) reached 81.0% theoretical ethanol yield. The 50.60%~93.40% (Prakasham et al., 1999), 83.1% (Sanchez and Cardona, 2008) or 95.4% (Liu et al., 2009) of theoretical ethanol yield by the yeast cells were reported. Here the novel beads showed a relatively high or medium cell activity. Before and after sodium sulfate treatment, the surface and crosssection morphologies of the gel beads under SEM observation were shown in Fig. 1 and Fig. 2, respectively. Obviously, after sulfate treat ment, bead surface became much dense, owned less yeast cells, and had more compact structure and lower porosity. The formation mechanism of the solid surface for sulfate-treated gel beads could be explained as the strong hydration force of sulfate ions (Takei et al., 2011) and Hofmeister effect on the artificial polymer PVA (Zhang and Cremer, 2006). The kosmotropic ions SO24 is believed to lead to higher hydrogel crystal linity of PVA and to made the PVA more stable in aqueous solution (Salavagione et al., 2009). The kosmotropes are strongly hydrated and have stabilizing and salting-out effects on proteins and macromolecules, and generally was regarded as ‘water structure makers’ (Zhang and Cremer, 2006). By comparing the different part of a sulfate treated-gel bead (Fig. 2 c ~ f), larger-size pores and less microorganism cells were observed. The
edges and submarginal sections of the beads preferentially formed highly crosslinked matrix and obtained high crystallinity than the bead’s center. Sulfate reaction with the inner PVA was more difficult due to the matrix resistance. The FTIR spectra of PVA-SA-GO-yeast gel beads before and after sulfate treatment were shown in Fig. 3. Based on some reported refer ences (Hug, 1997; Lawrie et al., 2007; Hui et al., 2014; Patel, 2014; Peng, 2015; Chen and Wang, 2016), Fig. 3 showed the strong interaction between the PVA-SA-GO-yeast chains and SO24 salts. The peak at 1083 cm 1 and 1036 cm 1 could be assigned to the different C–O vibrations, partly reflecting the characteristic peak of polysaccharide skeleton and complex interaction of PVA, SA, GO and yeast cells (Chen and Wang, 2016). After sulfate treatment, new strong peak of 1099 cm 1 appeared (C–O stretch, O–H bind, C–H vibration, etc.) and 1083/1036 cm 1 greatly weakened and even disappeared. The peak around 1099 cm 1 reflected the S–O vibration (around 1100 cm 1), originating from the interaction between sulfate and PVA mol ecules. New peak at 612 cm 1 occurred indicating the presence of sul – C from fate (Shen et al., 2008). Moreover, the band at 1606.4 cm 1 (C– aromatic ring skeleton or COO from alginate) shifted to higher wave number 1614.7 cm 1 further indicated the good interaction of sulfate and PVA. Moreover, the intensity ratio of band near 1606.4 cm 1 to band near 1417.6 cm 1 and 1333 cm 1 (indicating CO2 stretch or C–H vibration) decreased greatly after sulfate treatment. It was supposed some sulphur atoms substituted some boron atoms from the PVA mo lecular, which changed the micro environment of PVA-SA-GO-yeast crosslinking state. Zain et al. (2011) reported the similar results. 3.2. Uranium biosorption The U removal efficiency and sorption quantity at 360 min reached 51.5% and 5.49 μmol/g, respectively, which occupied the 97.1% of the 3
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Fig. 2. Cross-section morphologies of the PVA-SA-GO-yeast gel beads before (upper: a � 2000, b � 5000) and after (lower: c, d, e and f) sulfate treatment. c and d: near the outer surface; e and f: at the center of the gel bead.
corresponding U sorption amount and the removal efficiency at 1290 min (21.5 h) (Fig. 4). Biosorption was usually fast and completed in several hours for both the dead and the living biomass (Wang and Chen, 2009). Living cells may involve in other processes such as precipitation, reduction and actively uptake, which could exhibit the more complex kinetics. Longer time was suggested to study living cells in future. Time course of U sorption quantity was fitted by the pseudo firstorder model and pseudo second-order model (Chen and Wang, 2016; Guo and Wang, 2019). The pseudo first order model fitted better than the pseudo second order model (Fig. 4). The kinetic parameters of the fitting results were listed in Table 1. As shown in Fig. 5, uranium uptake quantity increased from 0.75 to 4.40–113.4 μmol/g when the equilibrium concentration of U reached 0.9, 27.3 and 43.9 μmol/L after 5 days’ contact with the gel beads, respectively. The sorption capacity reached a The removal efficiency
(30.7%~90.7%) decreased firstly and then increased when initial U concentration increased from 3.7 to 472.2 μmol/L. In this study, ura nium sorption capacity reached 27.0 mg/g of the gel beads, which was lower than many reported maximum sorption capacity such as 152 mg/g of the green algae (Bagda et al., 2017). The equilibrium concentration of metal such as uranium in solution and other experimental conditions influenced performance of the adsorbents (Saleh et al., 2017). According to the nonlinear fitting results of Langmuir model and Freundlich model (Chen and Wang, 2016), Freundlich equilibrium could describe the uranium sorption equilibrium by the sulfate-treated gel beads. Many dead biomass or non-living substances for uranium adsorption followed the Langmuir models, such as green algae powder (Bagda et al., 2017) and polyethylenimine modified activated carbon (Saleh et al., 2017). Here the isotherm was unusual and the sorption capacity increased fast. This could relate to the cell viability and/or cell 4
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Fig. 3. FTIR. Upper: PVA-SA-GO- yeast gel beads; Below: pristine sulfate-treated gel beads.
Fig. 5. U sorption isotherm (C0 ¼ 3.7–472.2 μmol/L, initial pH ¼ 5.0, 37 � C, 5d).
Fig. 4. Time course of U sorption and fitting: pseudo first-order model fitting better than pseudo second-order model (C0 ¼ 48.6 μmol/L, the gel bead con centration ¼ 4.6 g/L, 30 � C, initial pH ¼ 5.0).
Table 1 Parameters of kinetic models for U (VI) adsorption. models
parameters
Pseudo first-order qt ¼ qe(1e-k1t)
k1 (min 1) � 10 3
Pseudo second-order qt ¼ k2qe2t/(1þtqek2) v2 ¼ k2qe2
9.84 k2 (g/(μmol min) � 10 3 1.89
qe (μmol/ g) 5.80 qe (μmol/ g) 6.55
v2(μmol/(g min))
R2
0.027 v2(μmol/(g min))
0.99 R2
0.081
0.95
permeability even with the leakage of some substance which can bind uranium from the gel beads due to long time of biosorption for five days. This need further investigation. Solution pH greatly influenced uranium adsorption by the sulfatetreated active dry yeast cell gel beads, shown in Fig. 6. Solution was undoubtedly one of the most important parameters affecting the
Fig. 6. Initial solution pH on U uptake (initial U concentration was about 10 mg/L before pH adjustment, the gel bead concentration was 4.6 g/L, 30 � C, t ¼ 24 h). 5
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Fig. 7. SEM of the sulfate-treated gel beads. Surface gel beads before contact with U: a � 1000, b � 5000; surface gel beads after contact with U: c � 1000, d � 5000; inner part of the gel beads after contact with uranium: e � 5000; f: EDS results at site of 1# in Fig. 7e. (U0 ¼ 472.2 μmol/L, initial pH ¼ 5.0, 30 � C, 21 h, 4.6 g/L).
biosorption process. At pH 3 uranium biosorption efficiency (74.6%) was higher than that at pH 5 (64.8%) and at pH 7 (63.7%), shown in Fig. 6. In this study, the relative standard deviation for U sorption under different pH arrived at 31.8%. S. cerevisiae, as fungus cells, showed the strong resistance to metal toxicity and extreme environment conditions at lower pH (T.S. Wang et al., 2017). Solution pH values influences both the relative distribution of U (VI) species in solutions and the surface properties of the gel beads. The predominant uranium species at pH 5þ 2þ 3.0–4.5 were UO2þ and (UO2)4(OH)þ 2 , (UO2)2(OH)2 , (UO2)3(OH) 7 (Y. S. Wang et al., 2017). Higher pH could result in negative/non com plexible uranium species such as UO2 (OH)-3 and UO3 (OH)-7 species due to uranium hydrolysis (Li et al., 2015). The repulsion between these anions and the negatively charged surface of the gel beads (active binding groups such as carboxyl, hy droxyl, sulfate, phosphate, etc.) was enhanced at high pH, which decreased U removal from aqueous solution. The dissociation constants of sulfate, carboxyl and phosphate in aqueous solution were in the range
of 2–5. Acidic condition was favorable for U biosorption for many bio sorption system (Chen and Wang, 2016). For uranium removal or extraction from aqueous solution, optimum pH 4.0 or pH 5.0 for green algae (Bagda et al., 2017; Heidari et al., 2017), optimum pH 4.0 for a kind of sulfide derivatives (Pu et al., 2017), optimum pH 4.0–5.0 for living Bacillus vallismortis (Ozdemir et al., 2017), optimum pH 6.5 for dual-dispersive liquid–liquid microextraction (Khan et al., 2017), opti mum pH 4.0 for marine sponge Sarcotragus foetidus (Celik et al., 2016) were reported. Among pH 2.0–8.0, optimum pH for magnetic nano biosorbent (sugarcane bagasse) was 3.0 (Rahnama et al., 2014). 3.3. SEM and TEM-EDS analysis before and after biosorption Fig. 7 shows the surface and the inner part of the gel beads before and after contact uranium under SEM observation. For convenient compar ison the SEM photos of the surface of the pristine gel beads before contact uranium at the magnification of 1000 and 5000 were 6
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Fig. 8. TEM-EDS result of the section on the inner gel beads (C0 ¼ 472.2 μmol/L, initial pH ¼ 5.0, 30 � C, 21 h, 4.6 g/L).
simultaneously offered in Fig. 7a and b, respectively. The yeast cells were entrapped in the gel matrix and typical ellipse cells were hard to be observed on the gel bead surface. The crosslinked matrix covered the cells. Irregular protruding due to the embedded cells occurred. It’s postulated that some yeast cells in elliptical-shape stretched and change to rod-shape during gel bead preparation. After the gel beads contact with U, no obvious precipitation were observed under SEM observation at the magnification of 1000 and 5000. After U sorption, more elliptical-shape cell embedded in the matrix appeared on the gel bead surface (Fig. 7c and d). Form the microstructure of the inner part of the gel beads (Fig. 7e and f), the embedded yeast cells in the matrix basically retain the plump egg shapes. Uranium were detectable in the inner gel beads but U level varied in different place of the gel beads. Semi quantification of U (wt %) at the position of 1 (cell), 2(cell), 3(matrix) and 4 (matrix) position reached 6.12%, 3.20%, 2.36% and 0.00%, respectively. Part uranium transported to the inner gel beads from aqueous solution. The yeast cell could uptake more U than the matrix and thus played a more important role in U binding. The matrix offered better protection for the yeast cells to keep normal ellipse shape. No obvious change in the topography of the cells in the inner gel beads after uranium biosorption. Ultrathin section of the yeast cell and the matrix of the gel beads were observed by TEM-EDS, shown in Fig. 8. The yeast cells and the embedded matrix partly separated due to the sample preparation of TEM ultrathin section. The element uranium was detectable in the position of matrix (1#, 0.3 wt U %), marginal part of yeast cells (2#: 1.6 wt U %) and the inner part of the yeast cells (3#:1.4 wt U %) although U level was not high. The yeast cell biomass appeared to play a more important role than the crosslinking matrix. U uptake quantity onto the matrix was usually lower than the immobilized biomass and much lower than the free biomass. SEM-EDS and TEM-EDS indicated that U element was detectable both in the surface or the inner gel beads, but the U level was not high and no apparent precipitation can be observed. SEM-EDS and TEM analysis also convinced that strontium were adsorbed both on the living S. cerevisiae cellular surface and the inner parts of the cells (Qiu et al., 2018).
Fig. 9. FTIR: sulfate-treated gel beads after contact with uranium (U0 ¼ 472.2 μmol/L, initial pH ¼ 5.0, 37 � C, 5 d, 4.4 g/L).
hydrogen bonds) (Mansur et al., 2008), 2912.88 (red shit of 26 cm 1, alkyl groups C–H stretching vibrations), 2031.66 (red shift of 7 cm 1), 1098.96 (red shift of 8.66 cm 1, hydroxyl C–O stretching band (Wu et al., 2006; Salavagione et al., 2009) or in-plane ring C–H bending (Kara – C/C–C bonds (Dobre et al., 2004), 827.92 (red shift of 20.56 cm 1, C– et al., 2012; N Diaye and Lian, 2018) or B–O (Spoljaric et al., 2014) or C–O–C stretching (Liu et al., 2014) or C–H out-of-plane bending mode of quinoid units (Dispenza et al., 2006) or substituted aromatic rings and 621.10 cm 1 (disappear). The band around 1100 cm 1 shifted to a lower wavenumber (1091 cm 1) after uranium biosorption, which may indicated the oxygen involving in U binding and U diminished the PVA crystallinity (Sala vagione et al., 2009). The peak at 1030 cm 1 strengthened after U biosorption may present the interaction of hydroxyl with U (Mahmud et al., 2006; Sedlarik et al., 2006). The presence of 848 cm 1 indicated the symmetric uranyl stretching bands which evidenced the U adsorbed by the gel bead (Sun et al., 2010). Aromatic C–H band peak shifted from 827 to 848 cm 1 after U sorption indicated that U sorption process influenced crosslinked ma terial structure (Ravindrachary et al., 2011). The peak around 620 cm 1 originating from O–H twisting of PVA disappeared after U sorption (Mahmud et al., 2006), indicating O containing group binding U uranium. Weak peak shift (less 5 cm 1) also occurred at the positions near 1614.71 cm 1, 1416.48 cm 1 and 1333.61 cm 1. This indicated that the element U changed the environment of benzene ring structure.
3.4. FTIR analysis FTIR is an important tool that identifies functional groups. The FTIR spectra from samples were collected from 4000 to 600 cm 1. According to Fig. 9 (for more clear display, data at 4000–1700 cm 1 were not shown), comparing the sulfate-treated gel beads before and after contact with U, main changes in the FTIR spectra (above 5 cm 1) occurred in the wavenumber of 3300.42 (red shift of 7 cm 1, OH broadening stretching peak from the intermolecular and intramolecular 7
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Fig. 10. XPS spectra for the gel beads before (C 1s and O 1s) and after (U 4f) contact with uranium (U0 ¼ 472.2 μmol/L, initial pH ¼ 5.0, 30 � C, 5 d, 4.6 g/L).
3.5. XPS analysis
aqueous U (VI) onto the sulfate-treated gel beads surfaces, followed by a partial U (VI) reduction to U (IV). The U (VI) reduction to U (IV) within a bio system was reported in many references (Lovley et al., 1991), such as of U (VI)-live S. cerevisiae. This reduction was also probably caused by non-living process. Reduction of U (VI) to U (IV) on the surface of magnetite was observed, which was facilitated by electron transfer be tween the Fe and U. The fitting C1s spectrum from the control gel beads consisted four peaks at 284.8 eV, 285.8 eV, 286.6 eV and 288.2 eV (Fig. 10c). After uranium biosorption, the four peaks occurred at 284.8 eV, 285.7 eV, 286.6 eV and 288.0 eV. From the peak shift (0.2 eV shift for the peak at
The full XPS spectrum of the sulfate-treated gel beads before and after uranium biosorption were shown in Fig. 10a. The XPS measurements clearly indicated the presence of uranium at the surface of the gel beads. Spectral fitting of the U 4f7/2 and U4f5/2 photoelectron peaks revealed the coexistence of U (IV) and U (VI) phases. First peaks corresponding to U(IV) phase centers at 380.5 eV and 391.5 eV, respectively, close to the reported UO2 (Scott et al., 2005). Second peaks corresponding to U (VI) phase located at 381.9 eV and 393.0 eV, respectively. XPS results demonstrated the adsorption of 8
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– O changed about 5–6%, 288.2 eV) and the ratio of C–O/C–O–C and C– carbon ions bound with two oxygen ions could partly involve in U binding. O 1s of the control gel bead consisted of three component peaks at 531.5 eV, 532.4 eV, 533.3 eV (Fig. 9e), respectively. After U biosorption, the corresponding peaks shifted to 531.9 eV, 532.7 eV and 533.20 eV. – O and C–O or O–H (Zhang et al., 2018) The binding energy of C– increased 0.3–0.4 eV, with more characteristic of uranium oxides.
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4. Conclusion A novel sulfate-strengthened immobilized gel beads containing living yeast cells were successfully prepared based on the traditional boric acid-calcium cross-linked method. The gel beads contained PVA (5 w/v %), alginate (1 w/v %), industrial scale produced-graphene oxide (0.05 w/v %), commercial active dry yeast cells (2 w/v %). Sulfate strengthened the gel bead gel structure. The living yeast cell captured in the gel beads obtained the 81.0% theoretical ethanol yield by glucose fermentation. The U uptake quantity at 360 min reached 5.49 μmol/g, which occupied the 97.1% of the corresponding U sorption amount at 1290 min. The pseudo first order model and Freundlich model could describe U sorption process. Uranium occurred on the surface and inside of the gel beads confirmed by SEM/TEM-EDS. FTIR and XPS analysis evidenced the role of oxygen in binding uranium. U (VI) was partly reduced to U (IV) by the sulfate-treated gel beads containing active yeast cells. Declaration of competing interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. Acknowledgements The research was supported by the National Key Research and Development Program (2016YFC1402507) and the Program for Changjiang Scholars and Innovative Research Team in University (IRT13026). References Abdullah, Z.W., Dong, Y., Davies, I.J., Barbhuiya, S., 2017. PVA, PVA blends, and their nanocomposites for biodegradable packaging application. Polym. Plast. Technol. Eng. 56, 1307–1344. Ariga, O., Takagi, H., Nishizawa, H., Sano, Y., 1987. Immobilization of microorganisms with PVA hardened by iterative freezing and thawing. J. Ferment. Technol. 65, 651–658. Bagda, E., Tuzen, M., Sari, A., 2017. Equilibrium, thermodynamic and kinetic investigations for biosorption of uranium with green algae (Cladophora hutchinsiae). J. Environ. Radioact. 175, 7–14. Becker, L., Scheffczyk, A., Forster, B., Oehlmann, J., Princz, J., Rombke, J., Moser, T., 2011. Effects of boric acid on various microbes, plants, and soil invertebrates. J. Soils Sediments 11, 238–248. Celik, F., Camas, M., Camas, A.S., Ozalp, H.B., 2016. Uranium (VI) biosorption on marine sponge, Sarcotragus foetidus (Schmidt, 1862) and its statistical investigation using central composite design. Turk. J. Fish. Aquat. Sci. 16, 899–911. Chang, C.C., Tseng, S.K., 1998. Immobilization of Alcaligenes eutrophus using PVA crosslinked with sodium nitrate. Biotechnol. Tech. 12, 865–868. Chen, C., Wang, J.L., 2016. Uranium removal by novel graphene oxide-immobilized Saccharomyces cerevisiae gel beads. J. Environ. Radioact. 162, 134–145. Dispenza, C., Presti, C.L., Belfiore, C., Spadaro, G., Piazza, S., 2006. Electrically conductive hydrogel composites made of polyaniline nanoparticles and poly (Nvinyl-2-pyrrolidone). Polymer 47, 961–971. Dobre, L.M., Stoica-Guzun, A., Stroescu, M., Jipa, I.M., Dobre, T., Ferdes, M., Ciumpiliac, S., 2012. Modelling of sorbic acid diffusion through bacterial cellulosebased antimicrobial films. Chem. Pap. 66, 144–151. Ege, D., Kamali, A.R., Boccaccini, A.R., 2017. Graphene oxide/polymer-based biomaterials. Adv. Eng. Mater. 19, 1700627. Gunes, Y., 2013. Inhibition of boric acid and sodium borate on the biological activity of microorganisms in an aerobic biofilter. Environ. Technol. 34, 1117–1121. Guo, X., Wang, J.L., 2019. A general kinetic model for adsorption: theoretical analysis and modeling. J. Mol. Liq. 288, 111100.
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Journal of Environmental Radioactivity 213 (2020) 106158 Wang, T.S., Zheng, X.Y., Wang, X.Y., Lu, X., Shen, Y.H., 2017. Different biosorption mechanisms of Uranium(VI) by live and heat-killed Saccharomyces cerevisiae under environmentally relevant conditions. J. Environ. Radioact. 167, 92–99. Wang, Y.J., Yang, X.J., Tu, W., Li, H.Y., 2007. High-rate ferrous iron oxidation by immobilized Acidithiobacillus ferrooxidans with complex of PVA and sodium alginate. J. Microbiol. Methods 68, 212–217. Wang, Y.S., Chen, Y.T., Liu, C., Yu, F., Chi, Y.L., Hu, C.L., 2017. The effect of magnesium oxide morphology on adsorption of U(VI) from aqueous solution. Chem. Eng. J. 316, 936–950. Wu, L.C., Hsu, H.W., Chen, Y.C., Chiu, C.C., Lin, Y.I., Ho, J., 2006. Antioxidant and antiproliferative activities of red pitaya. Food Chem. 95, 319–327. Zain, N., Suhaimi, M.S., Idris, A., 2011. Development and modification of PVA-alginate as a suitable immobilization matrix. Process Biochem. 46, 2122–2129. Zhang, L., Wang, Z., Xu, C., Li, Y., Gao, J., Wang, W., Liu, Y., 2011. High strength graphene oxide/polyvinyl alcohol composite hydrogels. J. Mater. Chem. 21, 10399–10406. Zhang, Y.J., Cremer, P.S., 2006. Interactions between macromolecules and ions: the Hofmeister series. Curr. Opin. Chem. Biol. 10, 658–663. Zhang, Z.W., Li, Z.J., Zheng, L.R., Zhou, L.M., Chai, Z.F., Wang, X.L., Shi, W.Q., 2018. Simultaneous elimination of cationic uranium (vi) and anionic rhenium (vii) by graphene oxide–poly (ethyleneimine) macrostructures: a batch, XPS, EXAFS, and DFT combined study. Environ. Sci. Nano 5, 2077–2087. Zhu, Y.H., Hu, J., Wang, J.L., 2012. Competitive adsorption of Pb(II), Cu(II) and Zn(II) onto xanthate-modified magnetic chitosan. J. Hazard Mater. 221, 155–161. Zhu, Y.H., Hu, J., Wang, J.L., 2014. Removal of Co2þ from radioactive wastewater by polyvinyl alcohol (PVA)/chitosan magnetic composite. Prog. Nucl. Energy 71, 172–178.
Sedlarik, V., Saha, N., Kuritka, I., Saha, P., 2006. Characterization of polymeric biocomposite based an poly(vinyl alcohol) and poly(vinyl pyrrolidone). Polym. Compos. 27, 147–152. Shen, Y.Q., Wu, H.L., Wu, C.C., Lv, L.F., 2008. Research on the structure design and performance of textile decorateive wall covering. J. Xi’an Polytech. Univ. China 22, 265–274. Spoljaric, S., Salminen, A., Luong, N.D., Seppala, J., 2014. Stable, self-healing hydrogels from nanofibrillated cellulose, poly(vinyl alcohol) and borax via reversible crosslinking. Eur. Polym. J. 56, 105–117. Sun, D., Zhang, N., Xu, Q.J., Huang, R.B., Zheng, L.S., 2010. A new clover-shaped trinuclear uranium(VI) complex: synthesis, structure and photoluminescence property. Inorg. Chem. Commun. 13, 859–862. Takei, T., Ikeda, K., Ijima, H., Kawakami, K., 2011. Fabrication of poly(vinyl alcohol) hydrogel beads crosslinked using sodium sulfate for microorganism immobilization. Process Biochem. 46, 566–571. Wang, J.L., Chen, C., 2006. Biosorption of heavy metals by Saccharomyces cerevisiae: a review. Biotechnol. Adv. 24, 427–451. Wang, J.L., Chen, C., 2009. Biosorbents for heavy metals removal and their future. Biotechnol. Adv. 27, 195–226. Wang, J.L., Chen, C., 2014. Chitosan-based biosorbents: modification and application for biosorption of heavy metals and radionuclides. Bioresour. Technol. 160, 129–141. Wang, J.L., Zhuang, S.T., Liu, Y., 2018. Metal hexacyanoferrates-based adsorbents for cesium removal. Coord. Chem. Rev. 374, 430–438. Wang, J.L., Zhuang, S.T., 2019. Covalent organic frameworks (COFs) for environmental applications. Coord. Chem. Rev. 400, 213046. Wang, J.L., Zhuang, S.T., 2019. Extraction and adsorption of U(VI) from aqueous solution using affinity ligand-based technologies: an overview. Rev. Environ. Sci. Biotechnol. 18, 437–452.
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Contents lists available at ScienceDirect
Journal of Environmental Radioactivity journal homepage: http://www.elsevier.com/locate/jenvrad
Biosorption of uranium by immobilized Saccharomyces cerevisiae Can Chen a, Jun Hu a, Jianlong Wang a, b, * a b
Collaborative Innovation Center for Advanced Nuclear Energy Technology, INET, Tsinghua University, Beijing, 100084, PR China Beijing Key Laboratory of Radioactive Waste Treatment, Tsinghua University, Beijing, 100084, PR China
A R T I C L E I N F O
A B S T R A C T
Keywords: Uranium Biosorbent Biosorption Microbial immobilization Saccharomyces cerevisiae
A novel biosorbent was prepared and applied for the removal of uranium from aqueous solution. A new immobilization method was studied and used to embed living yeast cells of Saccharomyces cerevisiae (2% w/v) by sodium sulfate (0.5 mol/L) based on saturated boric acid-alginate calcium cross-linking method. The swelling ratio, hydraulic and chemical stability and bioactivity of immobilized microbial cells were examined. Their ultramicrostructure and property were observed by SEM, TEM and FTIR techniques. The influencing factors, such as contact time, initial uranium concentration, and initial pH were investigated. The adsorption capacity of bio sorbent increased from 0.75 to 113.4 μmol/g when the equilibrium concentration of U was 0.9, and 43.9 μmol/L, respectively. U adsorption followed pseudo first-order kinetic model. SEM-EDS and TEM-EDS observation indicated that uranium was adsorbed both on the surface and the inner parts of the biosorbent. FTIR and the XPS results confirmed the role of oxygen in capturing uranium from aqueous solution. XPS analysis showed that the mixture of U (VI) and U (IV) existed on the surface of biosorbent, which evidenced that uranium was micro biologically reduced.
1. Introduction Uranium pollution may originate from uranium mining and its application (Wang and Zhuang, 2019b). Adsorption process is regarded as a promising cost-effective biotechnology to take radionuclides including uranium away from (waste) water (Wang et al., 2018; Wang and Zhuang, 2019a). Biosorption is a promising technology for the removal of radionuclide from radioactive wastes (Wang and Chen, 2009; Zhu et al., 2012, 2014; Bagda et al., 2017). Preparation and use of “good” biosorbents for real application is still a big challenge (Wang and Chen, 2006, 2014). Cell immobilization is an alternative method to improve biosorbent with higher mechanical strength and/or stability. Suitable carrier materials are important. Natural polymer such as algi nate (SA) is widely explored due to its good cell compatibility, cheap and easy preparation using calcium chloride as the crosslinker. However, pure SA-Ca gel bead is unstable in alkaline or phosphate-containing wastewater. Polyvinyl alcohol (PVA) is non-toxic and cheap and owes high durability in water. Thus PVA become a popular synthetic polymer material to prepare immobilized cells using saturated boric acid as the crosslinker, which is regarded as a simple and economical technique of cell immobilization. However, the crosslinking rate is slow of PVA-boric acid method (Takei et al., 2011). PVA-SA gel beads cross-linked using
the mixed aqueous solution containing saturated boric acid and calcium chloride are thus supposed, reported and utilized for microorganism immobilization. Alginate can help PVA rapidly form spherical gel beads (Idris et al., 2008; Takei et al., 2011), decrease the agglomeration of the PVA beads and improve the surface properties of the beads (Zain et al., 2011). Graphene oxide (GO) as a new carbon material is reported to improve the polymer gel properties such as mechanical strength and thermal stability (Zhang et al., 2011; Abdullah et al., 2017; Ege et al., 2017). GO enhanced the performance of the immobilized dead cells entrapped in PVA-SA gel for uranium removal from aqueous solution (Chen and Wang, 2016). However, for living cell immobilization, the crosslinker boric acid is toxic to living microorganisms (Becker et al., 2011; Gunes, 2013). Saturated boric acid solution is highly acidic, which could cause the drastic cell viability loss of the microorganisms enclosed in the gel matrix (Takei et al., 2011; Li et al., 2014). Moreover, a large amount of the hydroxyl groups without involving reaction with boric acid on the beads are prone to form hydrogen with water, and show a high degree of swelling in aqueous solution. Some measures were suggested to improve the PVA-boric acid method. The freezing-thawing cycle method for PVA gel bead prepara tion is reported (Ariga et al., 1987; Lozinsky and Plieva, 1998). The
* Corresponding author. Energy Science Building, INET, Tsinghua University, Beijing, 100084, PR China. E-mail address: [email protected] (J. Wang). https://doi.org/10.1016/j.jenvrad.2020.106158 Received 11 November 2019; Received in revised form 31 December 2019; Accepted 2 January 2020 Available online 7 January 2020 0265-931X/© 2020 Elsevier Ltd. All rights reserved.
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freezing-thawing method is clean and ecofriendly. However, high en ergy consumption, unsatisfactory water resistance due to physical crosslinking and unavoidable loss of cell viability during freezing-thawing cycles blocked the real commercial application of cy clic freezing-thawing process in PVA gel bead preparation (Liao et al., 2018). Chemical crosslinking agents such as sodium sulfate (Zain et al., 2011), sodium nitrate (Chang and Tseng, 1998) or sodium phosphate (Wang et al., 2007) were utilized to strengthen the traditional PVA-boric gel beads. In our previous reported study, immobilization of activated sludge using sodium sulfate for PVA/SA-boric/calcium gel beads showed higher microbial activity and relatively high mechanical sta bility (Mao and Wang, 2013). Sodium sulfate was used to prepare the stable PVA-boric acid beads for invertase immobilization (Idris et al., 2008). X-ray diffraction results indicated that sodium sulfate promoted crystallization of PVA. Moreover, the toxicity of sodium sulfate to the yeast cells was lower than that of boric acid (Takei et al., 2011). The combination of sodium sulfate, GO from industrial scale pro duction, commercial active dry yeast (living Saccharomyces cerevisiae) and PVA/SA-boric/calcium chloride solution to prepare the gel beads for uranium removal has never been reported to the best of our knowledge. The sulfate-strengthened novel gel beads were character ized. The uranium adsorption performance of the gel beads under different contact time, initial uranium concentration and initial pH were presented. The process of cation (sodium, potassium, calcium, magne sium) release and the possible mechanism were analyzed using ICP-OES (Inductively Coupled Plasma Optical Emission Spectrometry), SEM (scanning electron microscopy with energy), TEM (transmission elec tron microscope), EDS (dispersive X-ray spectrum), FTIR (Fourier transform infrared spectroscopy) and XPS (X-ray photoelectron spec troscopy) technique methods.
2.3. Gel bead characterization The gel bead size was determined by measuring 20–30 gel beads using vernier calipers. The ratio of the dry weight and wet weight (dried at 80 � C to constant weight) was calculated. The diameters of gels beads before and after soaking in deionized water for 10 days were set as d1 and d2, respectively. The swelling ratio of beads (d2/d1) was determined. The hydraulic stability of the beads. The tubes containing 20 gel particles soaked in deionized water of 40 mL were put into a recipro cating oscillating machine. They were then acutely shaken (200 rpm) for 12 h. The broken ratio was calculated. The chemical stability. The gel beads were soaked in deionized water, hydrochloric acid (0.1 mol/L), sodium chloride (0.1 mol/L), 0.1 M sodium hydroxide (0.1 mol/L), 0.1 M sodium hydrogen carbonate (0.1 mol/L), or 0.1 M monosodium phosphate (0.1 mol/L) for 10 days, respectively. The swelling ratio and bead weight change before and after soaking in solutions were measured and calculated. The fermentation activity. YEPD solution contained glucose (20 g/L), tryptone (20 g/L) and yeast extract (10 g/L) was prepared. 4.0 g (wet weight) gel beads were put into 100 mL sterilized YEPD solution and then cultured for 24 h. High performance liquor chromatography (HPLC, Shimadzu LC-20AD, Tokyo) measured the level of glucose and the alcohol in solution. 2.4. Uranium biosorption experiments Ten gel beads were added to 10 mL uranium solution in a bottle. The bottles were shaken (150 rpm) at 30 � C. After reaction, the solution was screened by 0.22 μm filter membrane. The concentration of U, K, Ca, Na and Mg ions in the filtrate were analyzed by ICP-OES (IRIS Intrepid II, Thermo). The duplicate was performed. The uranium biosorption quantity by the gel beads was calculated as follows:
2. Materials and methods 2.1. Materials The commercial powder of living Saccharomyces cerevisiae was pur chased from a local supermarket, produced by Angel Yeast Co., Ltd in China. PVA, SA, calcium chloride, boric acid, sodium hydrate, hydro chloric acid, sodium chlorite, sodium hydrogen carbonate, monosodium phosphate, nitric acid, glucose, tryptone and yeast extract were bought from the market in China. SA was produced by Tianjin Guangfu Fine Chemical Research Institute, China. PVA was produced by Sinopharm Chemical Reagent Co., Ltd; calcium chloride, boric acid, sodium hy drate, hydrochloric acid, sodium chlorite, sodium hydrogen carbonate, monosodium phosphate, and nitric acid were offered by Sinopharm Chemical Reagent Co., Ltd. Glucose was produced by Xilong Chemical Co., China. tryptone and yeast extract were produced by Oxoid LTD. Graphene oxide produced at industrial scale were supplied by Ulanqab Darsen Graphite New Materials Co., Ltd. Uranium solution were sup plied by a nuclear institute in China.
q (μmol/g) ¼ (C0-Ct) � V/W The removal efficiency (η) was calculated as follows:
η (%) ¼ (C0-Ct) / C0 Where: t was contact time (min); C0 was the initial uranium concen tration (μmol/L); Ct was residual uranium concentration at the time t (μmol/L); V was the solution volume for biosorption (mL); W is the dry weight of the biosorbent (g). 2.5. Characterization of biosorbent The gel beads were cleaned and dried for SEM–EDS analysis using a FEI Quanta 200 FEG SEM (Holland) or SU-8010 (Hitachi, Japan) with EDS equipment. The ultrathin section specimen of the gel beads were obtained by an ultramicrotome (Leica EM UC6) for TEM-EDS analysis (JEM2010 or HT7700, Japan). The gel beads were washed and lyophilized for FTIR analysis using potassium bromide (Potassium bromide) method (FTIR spectrometer, Bruker). The XPS spectra of the gel beads were recorded on a spectrometer (PHI Quantro SXM, ULVAC-PHI Co., Japan). Surface charging effect was corrected with C1s peak at 284.8 eV as the reference. High resolution U 4f, O 1s, C 1s peaks and Ca 2p were fitted using the XPS PEAK 4.1 program after subtracting the background (Shirley baseline correction).
2.2. Immobilization procedure The homogeneous solution containing PVA (5%, w/v), SA (1%, w/v), GO (0.05%, w/v) and the living yeast power (2%, w/v) was dropped into the saturated boric acid -calcium chloride (1% w/v) solution and immersed for 0.5 h with gentle stirring. The beads were then transferred to 0.5 M sodium sulfate aqueous solution and immersed for 2–4 h with gentle stirring. The gel beads were then washed and then stored at 4 � C for further use, called sulfate treated-gel bead. The homogeneous solution containing PVA (5%, w/v), SA (1%, w/v), GO (0.05%, w/v) and the living yeast power (2%, w/v) was dropped into the saturated boric acid -calcium chloride (1% w/v) solution and immersed for 4 h, without sulfate treatment. The gel beads were then washed and then stored at 4 � C for further use, called PVA-SA-GO-yeast gel beads.
3. Results and discussion 3.1. Characterization of gel beads The sulfate-improved novel gel beads were successfully prepared. 2
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Fig. 1. Surface morphologies of the PVA-SA-GO-yeast gel beads before (upper: a � 2000, b � 5000) and after (lower: c � 2000, d � 5000) sulfate treatment.
The mean size of the wet gel beads was 0.38 � 0.00 cm. The ratio of dry weight and wet weight was 0.106. None bead was broken in water after acutely shaken for 12 h. The swelling ratio of the wet gel beads after contact for 10 days with H2O, 0.1 M NaCl, 0.1 M NaOH, 0.1 M NaHCO3 and 0.1 M NaH2PO4 reached 1.31, 1.05, 1.21, 1.19, 1.22 and 1.19, respectively. The gel beads were able to maintain their raw spherical shape in the above mentioned aqueous solution. Compared with pure water, the gel beads tend to shrink in acid, salt or alkaline. The sulfatemade gel beads were thus expected to adapt good to the real wastewater usually containing acid, alkaline or salt. The 4 g gel beads utilized the 99.4% glucose of YEPD culture with initial glucose concentration of 16.3 g/L. The ethanol yield (6748.5 mg/L within 24 h) reached 81.0% theoretical ethanol yield. The 50.60%~93.40% (Prakasham et al., 1999), 83.1% (Sanchez and Cardona, 2008) or 95.4% (Liu et al., 2009) of theoretical ethanol yield by the yeast cells were reported. Here the novel beads showed a relatively high or medium cell activity. Before and after sodium sulfate treatment, the surface and crosssection morphologies of the gel beads under SEM observation were shown in Fig. 1 and Fig. 2, respectively. Obviously, after sulfate treat ment, bead surface became much dense, owned less yeast cells, and had more compact structure and lower porosity. The formation mechanism of the solid surface for sulfate-treated gel beads could be explained as the strong hydration force of sulfate ions (Takei et al., 2011) and Hofmeister effect on the artificial polymer PVA (Zhang and Cremer, 2006). The kosmotropic ions SO24 is believed to lead to higher hydrogel crystal linity of PVA and to made the PVA more stable in aqueous solution (Salavagione et al., 2009). The kosmotropes are strongly hydrated and have stabilizing and salting-out effects on proteins and macromolecules, and generally was regarded as ‘water structure makers’ (Zhang and Cremer, 2006). By comparing the different part of a sulfate treated-gel bead (Fig. 2 c ~ f), larger-size pores and less microorganism cells were observed. The
edges and submarginal sections of the beads preferentially formed highly crosslinked matrix and obtained high crystallinity than the bead’s center. Sulfate reaction with the inner PVA was more difficult due to the matrix resistance. The FTIR spectra of PVA-SA-GO-yeast gel beads before and after sulfate treatment were shown in Fig. 3. Based on some reported refer ences (Hug, 1997; Lawrie et al., 2007; Hui et al., 2014; Patel, 2014; Peng, 2015; Chen and Wang, 2016), Fig. 3 showed the strong interaction between the PVA-SA-GO-yeast chains and SO24 salts. The peak at 1083 cm 1 and 1036 cm 1 could be assigned to the different C–O vibrations, partly reflecting the characteristic peak of polysaccharide skeleton and complex interaction of PVA, SA, GO and yeast cells (Chen and Wang, 2016). After sulfate treatment, new strong peak of 1099 cm 1 appeared (C–O stretch, O–H bind, C–H vibration, etc.) and 1083/1036 cm 1 greatly weakened and even disappeared. The peak around 1099 cm 1 reflected the S–O vibration (around 1100 cm 1), originating from the interaction between sulfate and PVA mol ecules. New peak at 612 cm 1 occurred indicating the presence of sul – C from fate (Shen et al., 2008). Moreover, the band at 1606.4 cm 1 (C– aromatic ring skeleton or COO from alginate) shifted to higher wave number 1614.7 cm 1 further indicated the good interaction of sulfate and PVA. Moreover, the intensity ratio of band near 1606.4 cm 1 to band near 1417.6 cm 1 and 1333 cm 1 (indicating CO2 stretch or C–H vibration) decreased greatly after sulfate treatment. It was supposed some sulphur atoms substituted some boron atoms from the PVA mo lecular, which changed the micro environment of PVA-SA-GO-yeast crosslinking state. Zain et al. (2011) reported the similar results. 3.2. Uranium biosorption The U removal efficiency and sorption quantity at 360 min reached 51.5% and 5.49 μmol/g, respectively, which occupied the 97.1% of the 3
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Fig. 2. Cross-section morphologies of the PVA-SA-GO-yeast gel beads before (upper: a � 2000, b � 5000) and after (lower: c, d, e and f) sulfate treatment. c and d: near the outer surface; e and f: at the center of the gel bead.
corresponding U sorption amount and the removal efficiency at 1290 min (21.5 h) (Fig. 4). Biosorption was usually fast and completed in several hours for both the dead and the living biomass (Wang and Chen, 2009). Living cells may involve in other processes such as precipitation, reduction and actively uptake, which could exhibit the more complex kinetics. Longer time was suggested to study living cells in future. Time course of U sorption quantity was fitted by the pseudo firstorder model and pseudo second-order model (Chen and Wang, 2016; Guo and Wang, 2019). The pseudo first order model fitted better than the pseudo second order model (Fig. 4). The kinetic parameters of the fitting results were listed in Table 1. As shown in Fig. 5, uranium uptake quantity increased from 0.75 to 4.40–113.4 μmol/g when the equilibrium concentration of U reached 0.9, 27.3 and 43.9 μmol/L after 5 days’ contact with the gel beads, respectively. The sorption capacity reached a The removal efficiency
(30.7%~90.7%) decreased firstly and then increased when initial U concentration increased from 3.7 to 472.2 μmol/L. In this study, ura nium sorption capacity reached 27.0 mg/g of the gel beads, which was lower than many reported maximum sorption capacity such as 152 mg/g of the green algae (Bagda et al., 2017). The equilibrium concentration of metal such as uranium in solution and other experimental conditions influenced performance of the adsorbents (Saleh et al., 2017). According to the nonlinear fitting results of Langmuir model and Freundlich model (Chen and Wang, 2016), Freundlich equilibrium could describe the uranium sorption equilibrium by the sulfate-treated gel beads. Many dead biomass or non-living substances for uranium adsorption followed the Langmuir models, such as green algae powder (Bagda et al., 2017) and polyethylenimine modified activated carbon (Saleh et al., 2017). Here the isotherm was unusual and the sorption capacity increased fast. This could relate to the cell viability and/or cell 4
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Fig. 3. FTIR. Upper: PVA-SA-GO- yeast gel beads; Below: pristine sulfate-treated gel beads.
Fig. 5. U sorption isotherm (C0 ¼ 3.7–472.2 μmol/L, initial pH ¼ 5.0, 37 � C, 5d).
Fig. 4. Time course of U sorption and fitting: pseudo first-order model fitting better than pseudo second-order model (C0 ¼ 48.6 μmol/L, the gel bead con centration ¼ 4.6 g/L, 30 � C, initial pH ¼ 5.0).
Table 1 Parameters of kinetic models for U (VI) adsorption. models
parameters
Pseudo first-order qt ¼ qe(1e-k1t)
k1 (min 1) � 10 3
Pseudo second-order qt ¼ k2qe2t/(1þtqek2) v2 ¼ k2qe2
9.84 k2 (g/(μmol min) � 10 3 1.89
qe (μmol/ g) 5.80 qe (μmol/ g) 6.55
v2(μmol/(g min))
R2
0.027 v2(μmol/(g min))
0.99 R2
0.081
0.95
permeability even with the leakage of some substance which can bind uranium from the gel beads due to long time of biosorption for five days. This need further investigation. Solution pH greatly influenced uranium adsorption by the sulfatetreated active dry yeast cell gel beads, shown in Fig. 6. Solution was undoubtedly one of the most important parameters affecting the
Fig. 6. Initial solution pH on U uptake (initial U concentration was about 10 mg/L before pH adjustment, the gel bead concentration was 4.6 g/L, 30 � C, t ¼ 24 h). 5
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Fig. 7. SEM of the sulfate-treated gel beads. Surface gel beads before contact with U: a � 1000, b � 5000; surface gel beads after contact with U: c � 1000, d � 5000; inner part of the gel beads after contact with uranium: e � 5000; f: EDS results at site of 1# in Fig. 7e. (U0 ¼ 472.2 μmol/L, initial pH ¼ 5.0, 30 � C, 21 h, 4.6 g/L).
biosorption process. At pH 3 uranium biosorption efficiency (74.6%) was higher than that at pH 5 (64.8%) and at pH 7 (63.7%), shown in Fig. 6. In this study, the relative standard deviation for U sorption under different pH arrived at 31.8%. S. cerevisiae, as fungus cells, showed the strong resistance to metal toxicity and extreme environment conditions at lower pH (T.S. Wang et al., 2017). Solution pH values influences both the relative distribution of U (VI) species in solutions and the surface properties of the gel beads. The predominant uranium species at pH 5þ 2þ 3.0–4.5 were UO2þ and (UO2)4(OH)þ 2 , (UO2)2(OH)2 , (UO2)3(OH) 7 (Y. S. Wang et al., 2017). Higher pH could result in negative/non com plexible uranium species such as UO2 (OH)-3 and UO3 (OH)-7 species due to uranium hydrolysis (Li et al., 2015). The repulsion between these anions and the negatively charged surface of the gel beads (active binding groups such as carboxyl, hy droxyl, sulfate, phosphate, etc.) was enhanced at high pH, which decreased U removal from aqueous solution. The dissociation constants of sulfate, carboxyl and phosphate in aqueous solution were in the range
of 2–5. Acidic condition was favorable for U biosorption for many bio sorption system (Chen and Wang, 2016). For uranium removal or extraction from aqueous solution, optimum pH 4.0 or pH 5.0 for green algae (Bagda et al., 2017; Heidari et al., 2017), optimum pH 4.0 for a kind of sulfide derivatives (Pu et al., 2017), optimum pH 4.0–5.0 for living Bacillus vallismortis (Ozdemir et al., 2017), optimum pH 6.5 for dual-dispersive liquid–liquid microextraction (Khan et al., 2017), opti mum pH 4.0 for marine sponge Sarcotragus foetidus (Celik et al., 2016) were reported. Among pH 2.0–8.0, optimum pH for magnetic nano biosorbent (sugarcane bagasse) was 3.0 (Rahnama et al., 2014). 3.3. SEM and TEM-EDS analysis before and after biosorption Fig. 7 shows the surface and the inner part of the gel beads before and after contact uranium under SEM observation. For convenient compar ison the SEM photos of the surface of the pristine gel beads before contact uranium at the magnification of 1000 and 5000 were 6
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Fig. 8. TEM-EDS result of the section on the inner gel beads (C0 ¼ 472.2 μmol/L, initial pH ¼ 5.0, 30 � C, 21 h, 4.6 g/L).
simultaneously offered in Fig. 7a and b, respectively. The yeast cells were entrapped in the gel matrix and typical ellipse cells were hard to be observed on the gel bead surface. The crosslinked matrix covered the cells. Irregular protruding due to the embedded cells occurred. It’s postulated that some yeast cells in elliptical-shape stretched and change to rod-shape during gel bead preparation. After the gel beads contact with U, no obvious precipitation were observed under SEM observation at the magnification of 1000 and 5000. After U sorption, more elliptical-shape cell embedded in the matrix appeared on the gel bead surface (Fig. 7c and d). Form the microstructure of the inner part of the gel beads (Fig. 7e and f), the embedded yeast cells in the matrix basically retain the plump egg shapes. Uranium were detectable in the inner gel beads but U level varied in different place of the gel beads. Semi quantification of U (wt %) at the position of 1 (cell), 2(cell), 3(matrix) and 4 (matrix) position reached 6.12%, 3.20%, 2.36% and 0.00%, respectively. Part uranium transported to the inner gel beads from aqueous solution. The yeast cell could uptake more U than the matrix and thus played a more important role in U binding. The matrix offered better protection for the yeast cells to keep normal ellipse shape. No obvious change in the topography of the cells in the inner gel beads after uranium biosorption. Ultrathin section of the yeast cell and the matrix of the gel beads were observed by TEM-EDS, shown in Fig. 8. The yeast cells and the embedded matrix partly separated due to the sample preparation of TEM ultrathin section. The element uranium was detectable in the position of matrix (1#, 0.3 wt U %), marginal part of yeast cells (2#: 1.6 wt U %) and the inner part of the yeast cells (3#:1.4 wt U %) although U level was not high. The yeast cell biomass appeared to play a more important role than the crosslinking matrix. U uptake quantity onto the matrix was usually lower than the immobilized biomass and much lower than the free biomass. SEM-EDS and TEM-EDS indicated that U element was detectable both in the surface or the inner gel beads, but the U level was not high and no apparent precipitation can be observed. SEM-EDS and TEM analysis also convinced that strontium were adsorbed both on the living S. cerevisiae cellular surface and the inner parts of the cells (Qiu et al., 2018).
Fig. 9. FTIR: sulfate-treated gel beads after contact with uranium (U0 ¼ 472.2 μmol/L, initial pH ¼ 5.0, 37 � C, 5 d, 4.4 g/L).
hydrogen bonds) (Mansur et al., 2008), 2912.88 (red shit of 26 cm 1, alkyl groups C–H stretching vibrations), 2031.66 (red shift of 7 cm 1), 1098.96 (red shift of 8.66 cm 1, hydroxyl C–O stretching band (Wu et al., 2006; Salavagione et al., 2009) or in-plane ring C–H bending (Kara – C/C–C bonds (Dobre et al., 2004), 827.92 (red shift of 20.56 cm 1, C– et al., 2012; N Diaye and Lian, 2018) or B–O (Spoljaric et al., 2014) or C–O–C stretching (Liu et al., 2014) or C–H out-of-plane bending mode of quinoid units (Dispenza et al., 2006) or substituted aromatic rings and 621.10 cm 1 (disappear). The band around 1100 cm 1 shifted to a lower wavenumber (1091 cm 1) after uranium biosorption, which may indicated the oxygen involving in U binding and U diminished the PVA crystallinity (Sala vagione et al., 2009). The peak at 1030 cm 1 strengthened after U biosorption may present the interaction of hydroxyl with U (Mahmud et al., 2006; Sedlarik et al., 2006). The presence of 848 cm 1 indicated the symmetric uranyl stretching bands which evidenced the U adsorbed by the gel bead (Sun et al., 2010). Aromatic C–H band peak shifted from 827 to 848 cm 1 after U sorption indicated that U sorption process influenced crosslinked ma terial structure (Ravindrachary et al., 2011). The peak around 620 cm 1 originating from O–H twisting of PVA disappeared after U sorption (Mahmud et al., 2006), indicating O containing group binding U uranium. Weak peak shift (less 5 cm 1) also occurred at the positions near 1614.71 cm 1, 1416.48 cm 1 and 1333.61 cm 1. This indicated that the element U changed the environment of benzene ring structure.
3.4. FTIR analysis FTIR is an important tool that identifies functional groups. The FTIR spectra from samples were collected from 4000 to 600 cm 1. According to Fig. 9 (for more clear display, data at 4000–1700 cm 1 were not shown), comparing the sulfate-treated gel beads before and after contact with U, main changes in the FTIR spectra (above 5 cm 1) occurred in the wavenumber of 3300.42 (red shift of 7 cm 1, OH broadening stretching peak from the intermolecular and intramolecular 7
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Fig. 10. XPS spectra for the gel beads before (C 1s and O 1s) and after (U 4f) contact with uranium (U0 ¼ 472.2 μmol/L, initial pH ¼ 5.0, 30 � C, 5 d, 4.6 g/L).
3.5. XPS analysis
aqueous U (VI) onto the sulfate-treated gel beads surfaces, followed by a partial U (VI) reduction to U (IV). The U (VI) reduction to U (IV) within a bio system was reported in many references (Lovley et al., 1991), such as of U (VI)-live S. cerevisiae. This reduction was also probably caused by non-living process. Reduction of U (VI) to U (IV) on the surface of magnetite was observed, which was facilitated by electron transfer be tween the Fe and U. The fitting C1s spectrum from the control gel beads consisted four peaks at 284.8 eV, 285.8 eV, 286.6 eV and 288.2 eV (Fig. 10c). After uranium biosorption, the four peaks occurred at 284.8 eV, 285.7 eV, 286.6 eV and 288.0 eV. From the peak shift (0.2 eV shift for the peak at
The full XPS spectrum of the sulfate-treated gel beads before and after uranium biosorption were shown in Fig. 10a. The XPS measurements clearly indicated the presence of uranium at the surface of the gel beads. Spectral fitting of the U 4f7/2 and U4f5/2 photoelectron peaks revealed the coexistence of U (IV) and U (VI) phases. First peaks corresponding to U(IV) phase centers at 380.5 eV and 391.5 eV, respectively, close to the reported UO2 (Scott et al., 2005). Second peaks corresponding to U (VI) phase located at 381.9 eV and 393.0 eV, respectively. XPS results demonstrated the adsorption of 8
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– O changed about 5–6%, 288.2 eV) and the ratio of C–O/C–O–C and C– carbon ions bound with two oxygen ions could partly involve in U binding. O 1s of the control gel bead consisted of three component peaks at 531.5 eV, 532.4 eV, 533.3 eV (Fig. 9e), respectively. After U biosorption, the corresponding peaks shifted to 531.9 eV, 532.7 eV and 533.20 eV. – O and C–O or O–H (Zhang et al., 2018) The binding energy of C– increased 0.3–0.4 eV, with more characteristic of uranium oxides.
Heidari, F., Riahi, H., Aghamiri, M.R., Shariatmadari, Z., Zakeri, F., 2017. Isolation of an efficient biosorbent of radionuclides (Ra-226, U-238): green algae from highbackground radiation areas in Iran. J. Appl. Phycol. 29, 2887–2898. Hug, S.J., 1997. In situ Fourier transform infrared measurements of sulfate adsorption on hematite in aqueous solutions. J. Colloid Interface Sci. 188, 415–422. Hui, B., Zhang, Y., Ye, L., 2014. Preparation of PVA hydrogel beads and adsorption mechanism for advanced phosphate removal. Chem. Eng. J. 235, 207–214. Idris, A., Zain, N., Suhaimi, M.S., 2008. Immobilization of Baker’s yeast invertase in PVAalginate matrix using innovative immobilization technique. Process Biochem. 43, 331–338. Kara, A., Uzun, L., Besirli, N., Denizli, A., 2004. Poly(ethylene glycol dimethacrylate-nvinyl imidazole) beads for heavy metal removal. J. Hazard Mater. 106, 93–99. Khan, N., Tuzen, M., Kazi, T.G., 2017. 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4. Conclusion A novel sulfate-strengthened immobilized gel beads containing living yeast cells were successfully prepared based on the traditional boric acid-calcium cross-linked method. The gel beads contained PVA (5 w/v %), alginate (1 w/v %), industrial scale produced-graphene oxide (0.05 w/v %), commercial active dry yeast cells (2 w/v %). Sulfate strengthened the gel bead gel structure. The living yeast cell captured in the gel beads obtained the 81.0% theoretical ethanol yield by glucose fermentation. The U uptake quantity at 360 min reached 5.49 μmol/g, which occupied the 97.1% of the corresponding U sorption amount at 1290 min. The pseudo first order model and Freundlich model could describe U sorption process. Uranium occurred on the surface and inside of the gel beads confirmed by SEM/TEM-EDS. FTIR and XPS analysis evidenced the role of oxygen in binding uranium. U (VI) was partly reduced to U (IV) by the sulfate-treated gel beads containing active yeast cells. Declaration of competing interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. Acknowledgements The research was supported by the National Key Research and Development Program (2016YFC1402507) and the Program for Changjiang Scholars and Innovative Research Team in University (IRT13026). References Abdullah, Z.W., Dong, Y., Davies, I.J., Barbhuiya, S., 2017. PVA, PVA blends, and their nanocomposites for biodegradable packaging application. Polym. Plast. Technol. Eng. 56, 1307–1344. Ariga, O., Takagi, H., Nishizawa, H., Sano, Y., 1987. Immobilization of microorganisms with PVA hardened by iterative freezing and thawing. J. Ferment. Technol. 65, 651–658. Bagda, E., Tuzen, M., Sari, A., 2017. Equilibrium, thermodynamic and kinetic investigations for biosorption of uranium with green algae (Cladophora hutchinsiae). J. Environ. Radioact. 175, 7–14. Becker, L., Scheffczyk, A., Forster, B., Oehlmann, J., Princz, J., Rombke, J., Moser, T., 2011. Effects of boric acid on various microbes, plants, and soil invertebrates. J. Soils Sediments 11, 238–248. Celik, F., Camas, M., Camas, A.S., Ozalp, H.B., 2016. Uranium (VI) biosorption on marine sponge, Sarcotragus foetidus (Schmidt, 1862) and its statistical investigation using central composite design. Turk. J. Fish. Aquat. Sci. 16, 899–911. Chang, C.C., Tseng, S.K., 1998. Immobilization of Alcaligenes eutrophus using PVA crosslinked with sodium nitrate. Biotechnol. Tech. 12, 865–868. Chen, C., Wang, J.L., 2016. Uranium removal by novel graphene oxide-immobilized Saccharomyces cerevisiae gel beads. J. Environ. Radioact. 162, 134–145. Dispenza, C., Presti, C.L., Belfiore, C., Spadaro, G., Piazza, S., 2006. Electrically conductive hydrogel composites made of polyaniline nanoparticles and poly (Nvinyl-2-pyrrolidone). Polymer 47, 961–971. Dobre, L.M., Stoica-Guzun, A., Stroescu, M., Jipa, I.M., Dobre, T., Ferdes, M., Ciumpiliac, S., 2012. Modelling of sorbic acid diffusion through bacterial cellulosebased antimicrobial films. Chem. Pap. 66, 144–151. Ege, D., Kamali, A.R., Boccaccini, A.R., 2017. Graphene oxide/polymer-based biomaterials. Adv. Eng. Mater. 19, 1700627. Gunes, Y., 2013. Inhibition of boric acid and sodium borate on the biological activity of microorganisms in an aerobic biofilter. Environ. Technol. 34, 1117–1121. Guo, X., Wang, J.L., 2019. A general kinetic model for adsorption: theoretical analysis and modeling. J. Mol. Liq. 288, 111100.
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