Highly efficient extraction of thorium from aqueous solution by fungal mycelium-based microspheres fabricated via immobilization

Accepted Manuscript Highly efficient extraction of thorium from aqueous solution by fungal mycelium-based microspheres fabricated via immobilization Hanlin Ding, Xiaonuo Zhang, Hao Yang, Xuegang Luo, Xiaoyan Lin PII: DOI: Reference:

S1385-8947(19)30347-X https://doi.org/10.1016/j.cej.2019.02.116 CEJ 21029

To appear in:

Chemical Engineering Journal

Received Date: Revised Date: Accepted Date:

24 November 2018 9 February 2019 15 February 2019

Please cite this article as: H. Ding, X. Zhang, H. Yang, X. Luo, X. Lin, Highly efficient extraction of thorium from aqueous solution by fungal mycelium-based microspheres fabricated via immobilization, Chemical Engineering Journal (2019), doi: https://doi.org/10.1016/j.cej.2019.02.116

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Highly efficient extraction of thorium from aqueous solution by fungal mycelium-based microspheres fabricated via immobilization Hanlin Dinga,b, Xiaonuo Zhanga,c, Hao Yanga,b, Xuegang Luoa,b,* and Xiaoyan Linb,c a

School of Life Science and Engineering, Southwest University of Science and

Technology, Mianyang, 621010 Sichuan, China b

Engineering Research Center of Biomass Materials, Ministry of Education,

Southwest University of Science and Technology, Mianyang, 621010 Sichuan, China c

School of Materials Science and Engineering, Southwest University of Science and

Technology, Mianyang, 621010 Sichuan, China

*Corresponding author e-mail address: [email protected] Postal address: Engineering Research Center of Biomass Materials, Ministry of Education, Southwest University of Science and Technology, Mianyang, Sichuan 621010, China. Tel: +86 13668316169

Co-authors emails address: Hanlin Ding: [email protected] Xiaonuo Zhang: [email protected] Hao Yang: [email protected] Xiaoyan Lin: [email protected]

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Highly efficient extraction study of thorium from aqueous solution by fungal mycelium-based microspheres fabricated via immobilization Hanlin Dinga,b, Xiaonuo Zhanga,c, Hao Yanga,b, Xuegang Luoa,b,* and Xiaoyan Linb,c a

School of Life Science and Engineering, Southwest University of Science and Technology, Mianyang, 621010 Sichuan, China

b

Engineering Research Center of Biomass Materials, Ministry of Education,

Southwest University of Science and Technology, Mianyang, 621010 Sichuan, China c

School of Materials Science and Engineering, Southwest University of Science and Technology, Mianyang, 621010 Sichuan, China

Abstract: In this paper, a facile immobilization method was applied to load alginate, ferric oxide and dopamine onto fungal mycelium to prepare a series of spherical composites as potential adsorbents for the separation and removal of thorium from aqueous solution. The structure and chemical properties of the as-prepared adsorbents were characterized in detail via scanning electron microscopy-energy-dispersive X-ray spectroscopy (SEM-EDX), Fourier transform infrared spectrometry (FT-IR), X-ray photoelectron spectroscopy (XPS), pH value at the point of zero charge (pHPZC) and thermogravimetric (TG) analysis. Based on the adsorption studies, the magnetic gamma-ferric oxide (γ-Fe2O3) and polydopamine (PDA) cofunctionalized fungal microspheres (FPFMs) exhibited excellent adsorption performance for thorium and could represent convenient agents for the removal and recovery of thorium. The equilibrium adsorption data for the FPFMs were well fitted by the Langmuir model, and a high maximum thorium adsorption capacity of 326.346 mg·g-1 was obtained. The thermodynamic parameter values (ΔH0 > 0, ΔS0 > 0, ΔG0 < 0) demonstrated that the thorium adsorption process was feasible, endothermic and spontaneous in nature. This work indicated that FPFMs have great potential to be employed as effective adsorbents for practical industrial water pollution treatment. Importantly, the possible

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mechanism of thorium adsorption on the homogeneous surface of FPFMs represented a combination of chelation interactions, coordination and ion exchange. Key word: Thorium; fungal; immobilization; PDA; adsorption. Highlights FPFMs are based on the conjunction of both γ-Fe2O3 and PDA onto fungal mycelia. FPFMs fabricated via immobilization exhibit excellent Th(IV) adsorption performance. The chelation, coordination and ion-exchange play an important role in adsorption. FPFMs can be used for repairing multiple types of nuclide-polluted aqueous system. 1 Introduction From the beginning of the nuclear era, radionuclides have been common pollutant sources in aqueous environments, such as surface water and groundwater [1]. Radionuclides with high mobility in aqueous environments gradually transfer into the soil and eventually into plants. The entry of radionuclides into the food chain can potentially cause severe progressive and irreversible damage to human health. Once radionuclides become enriched in an organism, they can form insoluble colloids in the body and remain in reticuloendothelial tissues. Although the partially insoluble radionuclide thorium can be excreted via feces through the hepatobiliary system, the process is extremely slow [2-4]. Thorium is a toxic radionuclide and also an energy material with very promising prospects [5]. Therefore, the removal and adsorption of thorium from aqueous environment are crucial for the aspect of environmental protection and human health. A current literature survey reveals that many methods have been developed for the treatment of industrial aqueous pollution, including ion-exchange [6], chemical precipitation [7], solvent extraction [8], membrane separation [9], reverse osmosis [10] and solid-phase adsorption [11-14]. Among these methods, adsorption is the most 3

popular method for the separation and recovery of thorium from the aqueous solution due to the advantages of high efficiency, simple and economical operation and practicality in practical applications [15]. To date, various and available adsorption materials have been applied to separate and recover thorium, such as siliceous material, aluminum material, carbon-based material and biomass materials [16-20]. Fungi are eukaryotes that can grow and multiply rapidly, and they are ubiquitous and abundant in the biosphere. Since the cell wall contains large quantities of functional groups, fungal mycelium can be used as an excellent biosorbent for the separation and recovery of metal ions from aqueous solution [21, 22]. However, due to factors such as the insufficient mechanical strength of the fungal mycelium and poor resistance to environmental perturbations, fungal mycelium must be immobilized to improve the corresponding capabilities [23]. In designing composite adsorbents, sodium alginate (SA) carriers have been selected for the immobilization of fine particles because of the ease of gelation via crosslinking and various other merits, such as environmental friendliness, degradability, and biocompatibility [24-25]. In recent years, magnetic nanoparticles, such as Fe3O4 and Fe2O3, have been extensively applied in environmental remediation due to their outstanding properties, such as high surface area, ease of separation and low toxicity [26-29]. To date, various types of magnetic nanoparticles have been used to address water resource pollution caused by conventional heavy metals [30-31], although to the best of our knowledge, few studies have been conducted on the remediation of aqueous environments contaminated by radionuclides, such as thorium. Dopamine (DA) is a biogenic catecholamine that is an attractive functional monomer that can undergo spontaneous self-polymerization into a wide variety of materials under a weak alkaline environment at room temperature to form polydopamine (PDA) [32-34]. Meanwhile, noncovalent functional groups (such as catechol and amine groups, as well as π-π bonds) of PDA can be readily employed to establish multiple interactions with target pollutants via coordination, chelation, and hydrogen bonding [35-36]. Therefore, PDA-coated materials have attracted tremendous interest from researchers in the fields of environmental remediation [37] and resource recovery [38]. For example, 4

Zhou and coworker reported that magnetic core-shell structured nanoparticles coated with PDA were used to effectively eliminate cationic and anionic dyes from contaminated aqueous solution [39]. Gao et al. developed a novel DA-functionalized mesoporous silica that exhibited selective adsorption performance towards uranium in aqueous solution [40]. Hence, based on the above investigations, the advantageous adhesive property of PDA and superparamagnetic feature of γ-Fe2O3 nanoparticles, PDA and γ-Fe2O3 can be used as versatile and suitable candidates for the preparation of adsorbents that possess efficient adsorption and excellent separation capacities. Encouraged by the above research, we chose magnetic γ-Fe2O3 nanoparticles, DA and SA as carriers to optimize and functionalize biomass from the strain Aspergillus niger by immobilization technology and successfully prepared a series of efficient adsorbents for the separation and recovery of thorium from radioactive wastewater. The primary aim of the present study was concentrated on the synthesis of adsorbents composed of magnetic γ-Fe2O3-immobilized fungal microspheres (Fe2O3/FMs, FFMs), PDA-conjugated fungal microspheres (PDA/FMs, PFMs) and magnetic γ-Fe2O3 and PDA cofunctionalized fungal microspheres (FPFMs) and their adsorption capacities for thorium. The adsorption performance of the as-prepared adsorbents with thorium was systematically investigated by static batch experiments under various adsorption factors, such as the solution pH, contact time, initial concentration and temperature. Additionally, kinetic, isotherm and thermodynamic models were explored to ascertain the adsorption process and mechanism of the as-prepared adsorbent. Moreover, the characterization of adsorbents was conducted to clarify the physical and chemical features before and after adsorption. 2 Experimental section 2.1 Materials and reagents The fungal strain Aspergillus niger (CICC 2487) was purchased from the China Center of Industrial Culture Collection (CICC, Beijing, China), and grown at 4 °C in a potato dextrose agar slant culture to subculture the strain. Subsequently, the strain was

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inoculated into potato dextrose agar medium and plated at 30 °C for 5 days to harvest the fungal spores. SA, hydrochloric acid (HCl), sodium hydroxide (NaOH) and anhydrous calcium chloride (CaCl2) were purchased from Kelong Chemical Reagent Co. Ltd. (Chengdu, China).

Thorium

nitrate

(Th(NO3)4·6H2O),

hexahydrate

γ-Fe2O3,

DA and

tris(hydroxymethyl)aminomethane-hydrochloric acid (tris-HCl) were purchased from Aladdin Chemical Reagent Co. Ltd. (Shanghai, China). All reagents and solvents used in the experiments were of analytical grade and used without further purification. All the solutions in this study were prepared using Milli-Q water (18.25 MΩ·cm−1). A thorium standard stock solution with a concentration of 1.0 g·L-1 was prepared by dissolving Th(NO3)4·6H2O in Milli-Q water. 2.2 Synthesis of adsorbents 2.2.1 Synthesis of the Fe2O3/FM adsorbent Anhydrous calcium chloride was dissolved in 100 mL Milli-Q water to generate a solution of 2 wt% (w/v) Ca2+ and sterilized at 121 °C for 20 min for use. A homogeneous SA and Fe2O3 mixed colloidal solution was prepared by dissolving 3.00 g of SA and 2.00 g of γ-Fe2O3 in 100 mL Milli-Q water under vigorous continuous magnetic stirring for 2 h and then autoclaved at 121 °C for 20 min. First, fungal spores cultured on potato dextrose agar medium plates were inoculated into the abovementioned mixed colloidal solution and evenly mixed, and then the mixture was added dropwise into the preconfigured sterile Ca2+ solution through a syringe controlled by an electronic injection pump with a constant speed of 45 mL·h-1 to shape the gel microspheres containing the fungal spores. Thereafter, the coagulated microspheres were continuously stirred for 6 h for gelation and then filtered and washed several times with sterile water. Subsequently, the gelated gel microspheres were pitched into a liquid medium consisting of peptone, cane sugar, and vitamin B1 and B2 at a natural pH and 30 °C with a constant rotating speed of 145 rpm and incubated for 3 days. The above procedure was carried out under aseptic conditions. Next, the fungal gel microspheres harvested from the liquid medium were washed thrice with sterile water and then soaked in HCl solution at a concentration of 0.2 M 6

at 30 °C for 4 h for the complete inactivation of the fungal mycelium. Finally, the inactivated fungal gel microspheres were collected and washed several times to obtain the Fe2O3/FM adsorbent for use in further adsorption studies. 2.2.2 Preparation of the PDA/FM adsorbent The PDA/FM adsorbent was synthesized by the following steps. First, a 3 wt% SA colloidal solution was prepared and autoclaved as described above. Second, the as-cultured fungal spores were transferred into the SA colloidal solution and stirred well until evenly mixed. Then, the mixture containing the fungal spores was dropped into the preconfigured sterile Ca2+ solution by using the abovementioned equipment and conditions and stirred for 6 h to complete gelation. Next, the formed gel microspheres were treated as described above and cultured in liquid medium for 3 days. The above procedure was carried out under aseptic conditions. After incubation, the fungal gel microspheres were immersed in a PDA solution with a concentration of 2 g·L-1 at pH 8.5 and adjusted by tris-HCl solution with a concentration of 0.5 M under stirring for 6 h to assure well-distributed coating by the PDA molecules. Subsequently, the as-prepared fungal gel microspheres were gathered after the filtration and washing procedures and labeled as PDA/FMs for further use. 2.2.3 Preparation of the FPFMs adsorbent A homogeneous SA and Fe2O3 mixed colloidal solution containing fungal spores was prepared by the method mentioned above. Afterwards, fungal gel microspheres were formed by dropwise addition of the mixed colloidal solution into the preconfigured sterile Ca2+ solution through a syringe with an electronic injection pump and continuously magnetically stirred for 6 h. Then, the gelated gel microspheres were cultured in liquid medium for 3 days after a series of treatments as described above, and the fungal gel microspheres after incubation were soaked in PDA solution as mentioned above under stirring for 6 h. The above procedure was carried out under aseptic conditions. Finally, the fungal gel microspheres were filtered and washed with sterile water until the filtrate was clear and then labeled as FPFMs for subsequent use. 2.3 Adsorption experiments 7

To investigate the adsorption performance and behavior of the three above-prepared adsorbents towards thorium, batch adsorption experiments were performed systematically, and the pH, temperature, contact time and initial concentration of thorium were recorded. All adsorption studies were performed in 150 mL conical flasks in a thermostatic shaker (HZQ-2) with a constant speed of 180 rpm for a predetermined time. The pH of the solution was adjusted in a range from 2 to 7 using negligible volumes of diluted HCl and NaOH solutions with concentrations of 0.01-1.0 M. Specifically, a quantitative amount of the as-prepared adsorbents was added to 50 mL of thorium solution with a known concentration under the desired conditions to conduct the adsorption experiment. At the end of each adsorption period, the adsorbents were separated from the bulk phase and the concentration of thorium in the bulk solution before and after adsorption was measured by inductively coupled plasma mass spectrometry (ICP-MS, AA700, USA). In this study, all experiments, including the blanks, were performed at least in triplicate, and the data illustrated in the figures were calculated as the mean values. The parameters related to the adsorption process were calculated by the following formulas: Re 

(C0  Ce ) 100 C0

(1)

qe 

(C0  Ce )V m

(2)

where Re (%) and qe (mg·g-1) represent the removal efficiency and adsorption capacity of the adsorbent, respectively; C0 (mg·L-1) is the initial concentration of thorium; Ce (mg·L-1) is the thorium concentration at time t; and V (L) and m (g) are the volume of thorium solution and the weight of adsorbent, respectively. 2.3 Characterization The physical/chemical features of the adsorbents were characterized by various analytical methods. The surface morphological properties and elemental distribution of the adsorbents before and after adsorption were observed by using cold-field emission scanning electron microscopy (SEM, Carl Zeiss Ultra 55, Germany) and energy-dispersive X-ray spectroscopy (EDX, Ultra 55, Carl Zeiss, Germany) after gold-plating at an accelerating voltage of 20 kV. The adsorption mechanism of 8

thorium on the adsorbents was investigated and elaborated via X-ray photoelectron spectrometry (XPS Escalab 250, Thermo Fisher Scientific Corporation, USA) and Fourier transform infrared spectrometry (FT-IR, Nicolet-5700, PerkinElmer Instruments Corporation, USA) in the range of 4000-400 cm-1. The charge condition on the surface of the adsorbents was measured using a zeta potential instrument (ZetaPALS). The thermal stability of the adsorbents was investigated by a simultaneous thermal analyzer (SDT Q600 V20.9 Build 20) from 20 to 800 °C at a heating rate of 10 °C·min-1. 2.4 Regeneration and reusability of the adsorbents The recyclability and stability of adsorbents are important for the development of adsorbents for environmental remediation. Regeneration of the thorium-saturated adsorbents was performed by the solvent adsorption-desorption technique. For the desorption studies, adsorbents loaded with thorium were placed in 0.05 M HCl solution for regeneration. After desorption, the adsorbents were separated and washed with Milli-Q water, and the regenerated adsorbents were used again in the thorium adsorption

experiments.

Recycling

was

performed

5

times

in

the

adsorption-desorption study to assess the recycling performance and stability of the adsorbents. All thorium solutions used in the adsorption-desorption studies were at a concentration of 100 mg·L-1. 3 Results and discussion 3.1 Synthetic process of adsorbents The immobilization of fungal spores was achieved through the gelation of SA. The ion-exchange reaction between Ca2+ in solution and Na+ in the alginate molecules occurred as the gelation process proceeded. The presence of empty orbits in Fe3+ could offset the electronic clouds in electron-rich atoms, which included oxygen-containing and nitrogen-containing groups in the alginate and fungal hyphae, to fully immobilize γ-Fe2O3. The immobilized spores continued to grow and form hyphae that could interact with the active functional groups on the alginate to construct intertwined mycelium microspheres. When the mycelium microspheres were completely immersed in the alkaline DA solution, the functional groups (hydroxyl and amino groups) in the PDA molecule achieved the conjugation of DA by interaction with the active functional groups (amino and carboxyl groups) on the

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mycelium microsphere. The synthesis processes of the as-prepared adsorbents are shown in Fig. 1. 3.2 Characterization 3.2.1 SEM-EDX analysis The morphology and structure analysis of all as-prepared adsorbents before and after thorium adsorption is illustrated in Fig. 2a-f. The microimages of both the FFMs and PFMs presented filamentous structures with a slightly smooth surface. Moreover, tiny particles were observed on the surface of the fungal mycelium (Fig. 2c and 2e). This phenomenon was attributed to the self-deposition of PDA particles and formation of a PDA coating on the surface of the mycelium. In our study, the DA solution was continuously in contact with the mycelium surface and penetrated the microspores at gaps of the mycelium surface to form a deposited PDA particle membrane. In contrast, the FFM adsorbent (Fig. 2a) exhibited a relatively smooth surface. However, after cofunctionalization with γ-Fe2O3 and PDA, the mycelium surface displayed some small wrinkles, which was attributed to the water-loss process due to the inactivation treatment and alkaline conditions, and the subsequent adsorption of thorium was enabled by the large specific surface area. After thorium adsorption, some enrichment appeared on the surface of the fungal mycelium, which might have been related to the precipitation of thorium under supersaturation conditions. The elemental composition of all the as-prepared adsorbents was characterized by EDX analysis, and the results are illustrated in Fig. 2g and 3a. Generally, the elemental components of the fungal mycelium were C, O, N, P, S and Fe, and elemental mapping revealed that all elements were evenly distributed on the surface of the adsorbent. 3.2.2 FT-IR and XPS analyses The FT-IR spectra of all three as-prepared adsorbents were obtained in the wavenumber range of 4000-400 cm-1. Fig. 3b shows the spectra of FFMs, PFMs and FPFMs. For all the spectra, the strong characteristic absorption peaks at approximately 3400 cm-1 belonged to the overlap of stretching vibrations of both O-H and N-H bonds in the fungal mycelium, PDA and alginate molecule, and the peaks at approximately 2900 cm-1 were ascribed to the C-H antisymmetric stretching vibration of methylene and methine in the adsorbent molecules [41]. The absorption bands at approximately 1620, 1410, 1315 and 1040 cm-1 for all as-prepared adsorbents corresponded to the stretching vibrations of C=O (carboxyl and amine groups in the 10

fungal mycelium and alginate molecules), C-N (fungal mycelium and PDA molecular skeleton), C-O (alcoholic hydroxyl groups in the PDA and alginate molecules) and C-O-C (alginate molecular skeleton), respectively [42]. The absorption peak at approximately 780 cm-1 was assigned to the aromatic C-H out-of-plane bending vibration of the PDA molecular skeleton [43]. For the FFMs and FPFMs, the weak characteristic bands at 556 cm-1 were attributed to vFe-O in the γ-Fe2O3 nanoparticles immobilized in the as-prepared adsorbents [44]. The XPS wide-scan spectra and elemental contents of the three adsorbents before thorium adsorption are shown in Fig. 3c. The clear C 1s, Ca 2p, N 1s, O 1s, S 2p and P 2p spectra centered at ~282.95 eV, ~347.92 eV, ~397.37 eV, ~531.32 eV, ~169.96 eV and ~134.16 eV, respectively, corresponded to the elemental composition of fungal mycelium immobilized by calcium alginate [45]. In the FFM and FPFM spectra, two peaks at binding energies of approximately 711.27 and 720.46 eV appeared, and these peaks were assigned to Fe 2p3/2 and Fe 2p1/2 in the γ-Fe2O3 nanoparticles, respectively [46]. 3.2.3 Thermogravimetric analysis To investigate the thermal stability of the FFMs, PFMs and FPFMs, a thermogravimetric (TG) analysis was carried out in a high-purity nitrogen atmosphere (Fig. 3d). Fig. 1 shows that the weight loss of the three adsorbents could be approximately divided into three individual stages with increasing temperature. The first degradation stage of all products at approximately 199.86 °C corresponded to the volatilization of the adsorbed and bound water, and the weight loss of all the samples was approximately 10%. The weight loss of the FPFMs, PFMs and FFMs obviously increased to 51.80%, 53.98% and 55.29%, respectively, due to the pyrolysis of some functional groups, such as -COOH, and a delayed weight loss process occurred below 336.93 °C, which corresponded to the breaking and decomposition of the molecular chains and basic skeletons of the three samples [47]. The TG profiles reached plateaus at or near 600 °C, and the residual masses of FPFMs, PFMs and FFMs were 39.04%, 37.04% and 33.30%, respectively, indicating that the FPFMs possessed better thermal stability than the other two samples. 3.3 Adsorption performance study 3.3.1 Effect of pH and comparative adsorption Generally, the pH of a solution is an important parameter because pH not only affects aqueous metal ion speciation in solution but also influences the charge at adsorption sites on the adsorbent [48-49]. The distribution of thorium species in 11

aqueous solution under various pH values is shown in Fig. 4a, which shows that the hydrolyzation process of thorium was clearly pH dependent. According to Fig. 4a, at pH < 6, the distribution of thorium species in the solution mainly consisted of positively charged species, such as Th4+, Th(OH)3+, Th4(OH)88+, Th6(OH)159+, Th(OH)3+, and Th(OH)22+. In addition, soluble thorium, such as Th4+, was the dominant species in strongly acidic solution, while Th4+ tended to precipitate out as Th(OH)4 at higher pH, which was consistent with the results of previous studies [50]. Because thorium precipitates at high pH conditions according to the species distribution for thorium hydrolysis, the zeta potential and pH effect were limited to pH values below 7 in the designed system in this work. The zeta potential study is illustrated in Fig. 4b, and the results show that the pH value at the point of zero charge (pHPZC) of the three adsorbents was 3.278 (FFMs), 3.037 (PFMs), and 3.141 (FPFMs). That is, the adsorbents themselves were negatively charged when the solution pH was higher than the pHPZC, which might be favorable for the adsorption of thorium. Fig. 4c demonstrates the effect of the solution pH on thorium adsorption from the aqueous phase by the three adsorbents, and the thorium adsorption capacity varied as the solution pH increased. As the pH of the solution increased from 2.0 to 5, the adsorption capacity increased drastically until reaching the maximum adsorption capacity (255.876 mg·g-1). A large amount of H+ in solution may have competed with Th4+ for the active adsorption sites on the adsorbents. The presence of an electrostatic repulsion force between thorium and the active functional groups on the adsorbents due to protonation was the other reason for the observed behavior. When the solution pH exceeded 5, the adsorption capacities of the three adsorbents began to decrease at equilibrium, which might be due to the precipitation of insoluble thorium at higher pH. This behavior made true adsorption studies impossible. A comparison of the adsorption capacities of the three adsorbents showed that the FPFM adsorbent was the most suitable adsorbent for thorium removal under the same conditions, which might be related to the comprehensive effects of the high affinity of magnetic particles to thorium and the abundance of hydroxyl and amine groups in the PDA molecules [51]. As a result, pH 5 was determined to be the optimum pH in the adsorption process of thorium. 3.3.2 Effect of ionic strength To study the adsorption performance of thorium on FPFMs more systematically and comprehensively, the effect of various background salt concentrations on thorium 12

adsorption was investigated. These salts included KCl, NaCl, MgCl2 and CaCl2. Fig. 4d shows the relationship between ionic strength and the adsorption capacity of thorium onto FPFMs. The results show that the adsorption of thorium onto FPFMs was not significantly affected by an increase in ionic strength from 0.000 to 0.100 M, indicating that under these experimental conditions, particle surface complexation between thorium and FPFMs had occurred [52]. Based on these observations and the previously mentioned results, the adsorption was dependent on the initial pH of the solution instead of the ionic strength. 3.3.3 Adsorption kinetics Contact time was considered an influential factor in the adsorption rate of thorium on the adsorbent. Fig. 5a illustrates the thorium adsorption capacity curve with respect to contact time on the FPFM adsorbent at various concentrations. The figure revealed that the thorium adsorption process was composed of two stages: an initial rapid enrichment that was followed by sluggish diffusion to reach equilibrium by internal driving forces and then an equilibrium state with a maximum adsorption capacity of 302.827 mg·g-1 (corresponding to 160 mg·L-1), which was reached at a contact time of approximately 480 min. The reason for this rapid enrichment phenomenon was insufficient contact between the thorium and the adsorption sites on the adsorbent and the inadequate exposure of available active sites at the beginning. Moreover, the change in the equilibrium adsorption phase might be related to the gradual completion of occupation of the available active adsorption sites in the late period [53]. Adsorption kinetic studies are essential for the analysis of the adsorption process, and they also furnish valuable experimental and theoretical data for designing water treatment systems. Thus, to investigate the time-dependent adsorption of thorium and the controlling mechanism of the thorium adsorption process, the widely used “pseudo-first-order” and “pseudo-second-order” adsorption kinetic models were applied in this study. The pseudo-first-order model assumes that the adsorption process is dominated by physical interactions, while the hypothesis proposed by the pseudo-second-order model is that chemical adsorption occurs throughout the whole adsorption process [54]. Detailed information about both adsorption kinetic models is provided in the Supporting Information. The fitting results of thorium adsorption onto FPFMs and the corresponding parameters are illustrated in Fig. 5b and c and Table S1, respectively. Apparently, the pseudo-second-order fitting curves provided a better fit 13

than the pseudo-first-order curves since the pseudo-second-order results displayed higher correlation coefficients (R2=0.997 (40 mg·L-1), 0.999 (80 mg·L-1), 0.999 (120 mg·L-1), and 0.998 (160 mg·L-1)), which indicated that rate-limiting step of the adsorption process of thorium on the FPFMs was chemisorption. Therefore, the complexation interaction between thorium and the active functional groups in the adsorbent related to valence forces caused by sharing electrons might be observed in the adsorption process [55]. To further clarify the particle transfer path during the adsorption process, the intra-particle diffusion (provided in the Supplementary Materials) was investigated in this work. The fitting plots of qt vs. t1/2 are shown in Fig. 5d, and the corresponding parameters are listed in Table S1. As shown in Fig. 5d, the curves are composed of three stages and do not pass through the origin point, indicating that the adsorption process was not controlled by a single factor. Furthermore, the diffusion rate constant values follow the order of k1 > k2 > k3, thus demonstrating that thorium was initially adsorbed on the external surface of the FPFMs. Subsequently, the adsorbed thorium was transferred into the interior of the FPFMs through the internal mass transfer driving force, and internal saturation was ultimately achieved [56]. Overall, the presence of a surface PDA coating enhanced the thorium adsorption due to the large amount of active functional groups in the PDA, and chemical induction effects caused by the internal Fe-O bond promote the diffusion of thorium adsorbed on the surface PDA coating. 3.3.4 Adsorption isotherm The adsorption isotherm expresses the relationship between the quantity adsorbed by a unit mass of adsorbent and the amount of solute remaining in the liquid phase at equilibrium [57]. The effect of the initial concentration on thorium adsorption by FPFMs was investigated under varying initial concentrations of thorium from 25 to 175 mg·L-1 at different temperatures ranging from 293.15 to 313.15 K. Fig. 6a illustrates the effect of the initial concentration on the adsorption of thorium. The results showed that the adsorption capacity of the FPFMs steadily increased as the initial concentration increased until reaching equilibrium, and the maximum adsorption capacity of 304.276 mg·g-1 was observed under an initial thorium concentration of 175 mg·L-1 and 313.15 K. This behavior might be based on the hypothesis that the mass transfer driving force of the concentration at the solid-liquid interface was promoted by an increase in the initial concentration, which could cause 14

an increase in the adsorption capacity of thorium on the FPFM adsorbent [58]. The adsorption isotherm study was fit by four types of models: Langmuir, Freundlich, Temkin and Dubinin-Radushkevich (D-R) isotherm models. The Langmuir model assumes that the adsorption process takes place on a homogeneous surface with equivalent adsorption sites [59]. As an empirical model, the Freundlich model is based on the assumption that the adsorption process is multilayer adsorption on a heterogeneous surface [60]. The D-R model assumes that the surface of the adsorbent is not uniform and that adsorption is a process in which the adsorbate fills the pores of the adsorbent [61]. The Temkin model is a theoretical model for chemical adsorption based on strong electrostatic interactions between positive and negative charges [62]. Detailed information about these isotherm models is described in the Supplementary Materials. The nonlinear regression fitting analysis of the four models is presented in Fig. 6b-d, and the corresponding parameters are listed in Table S2. The fitting degree follows the sequence Langmuir > Temkin > Freundlich > D-R. The Langmuir isotherm model better fit the adsorption process than did the other isotherm models. Thus, when KL > 0, adsorption is favorable [63]. The above results indicate that the adsorption process of thorium onto the FPFMs likely occurred on specific homogeneous functional sites within the FPFMs, i.e., thorium formed an evenly distributed monolayer on the surface of the FPFMs and was captured by related functional groups (such as amino, hydroxyl and carboxyl groups) based on a site-to-site adsorption mechanism. In summary, the lower correlation coefficients of the other three models demonstrated that the adsorption process of thorium was dominated by chemisorption accompanied by physical adsorption. 3.3.5 Thermodynamic adsorption Fig. 7a shows the effect of temperature on the adsorption of thorium and indicates that the adsorption capacity of the FPFMs for thorium increased with increasing temperature. The adsorption thermodynamics were defined through widely used temperature-dependent thermodynamic parameters, including the changes in enthalpy (ΔH0), entropy (ΔS0) and Gibbs free energy (ΔG0). All parameters were represented by the Van’t Hoff equation (detailed information is illustrated in the Supplementary Materials) and are shown in Fig. S1 and Table S3. As shown in Table S3, the consistently negative ΔG0 values (-0.215 KJ·mol-1 at 293.15 K, -0.561 KJ·mol-1 at 303.15 K, and -0.907 KJ·mol-1 at 313.15 K) indicated the spontaneous nature of the thorium adsorption process on the FPFMs, and the absolute values of ΔG0 increased 15

with increasing temperature, demonstrating that higher temperatures correspond to greater degrees of spontaneity [64]. The positive values of ΔH0 (9.914 KJ·mol-1) and ΔS0 (34.556 J·(mol·K)-1) showed that the thorium adsorption process was typically endothermic and indicated increasing randomness at the solid-liquid interface. 3.3.6 Effect of coexisting ions Coexisting ions influence the adsorption process of target ions through competition for limited active sites [65]. The effect of coexisting cations (such as UO22+, Cs+, Sr+, Mg2+, Mn2+, and Ni2+) in nuclear industrial wastewater on thorium adsorption was investigated in a binary cationic system, and the results are illustrated in Fig. 7c. The influence of the abovementioned cations on thorium adsorption was not obvious at arbitrary concentrations except for UO22+, which was because the ionic radius of uranium (~89 pm) is close to that of thorium (~94 pm) and could compete with thorium for active adsorption sites. In addition, thorium and uranium are lanthanides, and the internal structure and the extranuclear electronic arrangements of thorium are similar to that of uranium; therefore, similar adsorption behavior occurs. Moreover, the organic groups (amino, hydroxyl, and carboxyl) possess higher affinity towards uranium in aqueous solution than the other metal ions because of electron-induced effects. Therefore, these effects might increase the potential for uranium to compete for active adsorption sites, thereby resulting in a decrease in the adsorption capacity of thorium. To more accurately investigate the influence of coexisting ions on thorium adsorption, a corresponding adsorption study of ideal and actual water systems (detailed indicators are displayed in Supporting Information, Table S1) was carried out, and the results are presented in Fig. 7d. The adsorption efficiency had clear differences among the various types of water systems, although the adsorption efficiency was excellent for the FPFMs in all the water systems. Among these systems, the adsorption efficiency of mine water was lower than that of the other water systems, which might be attributed to the interference of coexisting ions and the lower pH, which was not the optimum pH for thorium adsorption by FPFMs. In summary, FPFMs may represent an excellent candidate for thorium removal in certain aqueous systems. 3.3.7 Regeneration of adsorption performance According to a previous study, the regeneration ability and stable performance of the as-prepared adsorbent is a crucial factor for evaluating their potential for industrial 16

practical applications [66]. The as-prepared adsorbents loaded with thorium are immersed in 0.05 M HCl solution for regeneration. After the regeneration process, the FPFMs are instantly reused in a new adsorption operation. The results are illustrated in Fig. 7b, and they show that after the five regeneration operations, the FPFMs still retained over 87% thorium removal efficiency and no obvious fluctuations in adsorption capacity occurred. The slight decline in thorium adsorption capacity might have been related to the incomplete desorption of thorium from the interior of the adsorbent. Moreover, with the desorption treatment, the removal efficiency could reach up to 91.31%, which indicated the excellent regeneration and recycling abilities possess by the FPFMs. This excellent performance suggests that the as-prepared adsorbent FPFMs have the potential for use in further practical applications for pollutant decontamination of large volumes of aqueous solution. 3.4 Adsorption mechanism FT-IR and XPS analyses were used to confirm the thorium adsorption mechanism onto FPFMs. The FT-IR spectra of bare and thorium-loaded FPFMs are presented in Fig. 8a. The appearance of a new very sharp peak at 1384.64 cm-1 in the FPFMs loaded with thorium corresponded to the stretching vibration of Th-O, suggesting that there might be certain chemical bonds between the thorium and active functional groups on the FPFMs [48, 67]. A broad FPFM peak located at 3411.45 cm-1 was attributed to the overlap of stretching vibrations of -OH and -NH2 groups from the fungal mycelium, alginate and PDA molecules. After thorium loading, the characteristic absorption peak was redshifted, and the peak shape became wider and stronger, suggesting that the -OH and -NH2 groups might participate in the thorium adsorption process through chelation interactions [68]. The characteristic peaks at 1621.84, 1415.49, 1315.21 and 1033.65 cm-1 likely originated from the asymmetrical stretching and deformation vibrations of the carboxylate and alcoholic hydroxyl groups of the alginate molecules and PDA molecular skeleton [69]. The locations of these

peaks

moved

after

adsorption,

which

indicated

that

the

oxygen/nitrogen-containing groups in the FPFMs might be involved in the thorium adsorption process. Additionally, the modifications to these absorption peaks suggested that ion exchange between thorium in solution and calcium crosslinked in the fungal mycelium immobilized by alginate might occur in the thorium adsorption process. The offset of the aromatic C-H out-of-plane bending vibration located at 781.03 cm-1 provided an additional explanation for the involvement of PDA 17

molecules in the thorium adsorption process. Finally, the weak absorption peak of the stretching vibration of Fe-O at 556.39 cm-1 was redshifted to 552.04 cm-1, demonstrating possible coordination among the stretching vibrations of Fe-O-Th [70]. The XPS full survey spectrum (Fig. 8b) clearly presented an apparent double peak at 335.45 and 344.82 eV after thorium adsorption, and these peaks were assigned to the binding energies of Th 4f7/2 and Th 4f5/2, respectively [5], thus providing direct evidence for the existence of thorium in the FPFMs. The detailed spectra of the FPFMs after adsorption included C 1s, O 1s, N 1s and Fe 2p XPS spectra. The high-resolution C 1s spectra of FPFMs before and after adsorption are illustrated in Fig. 8c, which indicates that these spectra before adsorption were composed of three component peaks at 284.65 (C-C/C-H groups in alginate, PDA and mycelium skeleton), 285.97 (C-O/C-O-C/C-N bonds in alcoholic hydroxyl and/or ether groups and PDA skeleton) and 288.12 eV (C=O/O-C=O groups of both mycelium and residual alginate rings) [71, 72]. After thorium was loaded on the FPFMs, the C 1s peaks of each group showed different degrees of binding energy offsets. These results implied that C species might be involved in chelation with thorium. Fig. 8d displays the high-resolution O 1s peaks of FPFMs before and after thorium adsorption. The O 1s spectrum could be deconvolved into three individual component peaks occurring at 529.72, 531.93 and 532.90 eV, which were attributed to lattice oxygen in the metal oxide (Fe-O), double-bonded oxygen atoms of carbonyl groups (C=O) and single-bonded oxygen in surface hydroxyl groups and/or ether groups (O-H/C-O-C), respectively. However, a significant shift occurred in the O 1s peak position after thorium was adsorbed onto the FPFMs, suggesting that the corresponding active oxygen-containing functional groups might participate in the thorium adsorption process. The three components of the N 1s peak (Fig. 8e) corresponded to primary amine groups (-NH2) at 401.17 eV, secondary amine groups (-NH-) at 399.69 eV and tertiary amine groups (>N-) at 399.13 eV [47]. After thorium adsorption, the peaks of the protonation process were integrated into two sets of peaks assigned to primary and secondary amine groups. These results indicated that chelation occurred between thorium and the nitrogen-containing active functional groups on the FPFMs. The deconvolution analysis of Fe 2p is shown in Fig. 8f, and the peaks can be attributed to the binding energy of the Fe 2p1/2 and Fe 2p3/2 levels. The observed satellite peaks (710.68-712.96 and 724.52 eV) are representative of the oxidation states of Fe 2p3/2 and Fe 2p1/2. As seen from the spectra of thorium-loaded samples (Fig. 8f), new 18

satellite peaks occurred at binding energies of 711.33-714.18 and 724.25 eV, which might also provide acceptable evidence that thorium not only was deposited on the surface of the mycelium but also might coordinate with the Fe-O bond of the magnetic body on the FPFMs [70]. In addition, the disappearance of the Ca 2p peak and the presence of double Th 4f peaks indicate the possibility of ion-exchange between calcium ions in the FPFM adsorbent and thorium in the solution. Based on the above results and discussion, the proposed thorium adsorption mechanism onto FPFMs in this study is schematically illustrated in Fig. 9. The adsorption performance of FPFMs for thorium removal might be related to chelation between the thorium in solution and the oxygen-containing (nitrogen-containing) active functional groups in the FPFMs. Moreover, the ion-exchange between thorium in the solution and calcium crosslinked with oxygen-containing active functional groups in the fungal mycelium immobilized by alginate and the coordination between thorium in the solution and the Fe-O bond through an electron-induced effect are the adsorption driving forces. Specifically, the target thorium initially rapidly covers and bonds onto the PDA coating, which involves numerous adsorption sites that possess lone pair electrons, which present a tendency to attract thorium to form a thorium complex. After this stage, thorium gradually diffused into the interior of the sphere, which resulted in thorium being trapped onto and complexing with functional sites of the fungal mycelium (i.e., -OH, -COOH and -NH2) and complexing via Fe-O bonds in γ-Fe2O3 nanoparticles. In addition, thorium diffused into crosslinking-binding sites on the Ca-alginate hydrogel beads (i.e., -OH and -COOH) to finish the ion-exchange with calcium, thereby leading the formation of more stable metal complexes. Conclusively, thorium adsorption mainly depends on the active functional sites on the surface of the as-prepared adsorbents and coordinates with the sphere via inner complexation and ion-exchange processes. 3.5 Comparison of various adsorbents To assess the adsorption performance of the as-prepared adsorbents, the adsorption capacities of the FPFMs, FFMs and PFMs used in the present study for the elimination of thorium from aqueous solution were compared with those of other adsorbents reported in the literature, and the values are listed in Table 1. The FPFM values were higher than most of the reported values for thorium adsorbents in the literature, indicating that the as-prepared FPFMs had good adsorption performance towards thorium. Hence, in consideration of their environmental friendliness, facile 19

preparation and cost effectiveness, FPFMs could be adopted as potential candidates for the sequestering of thorium from aqueous solution. 4 Conclusion In the present work, a series of fungi-based adsorbents for thorium removal were synthesized via immobilization with alginate, ferric oxide and DA. A comparison of the results of the adsorption study showed that FPFMs exhibited the best adsorption performance with thorium and presented maximum adsorption capacities of 304.276 (qe,exp) and 326.346 (qe,cal) mg·g-1. The analysis of various models revealed that the adsorption data presented good agreement with the pseudo-second-order kinetic model and Langmuir isotherm model. In addition, the thermodynamic analysis indicated that the adsorption process of thorium onto FPFMs was endothermic and spontaneous in nature. The combination of chelation interactions, coordination and ion exchange on the heterogeneous surface of FPFMs represent the possible mechanisms underlying thorium adsorption as determined through FT-IR and XPS analyses. Practical application studies showed that FPFMs can be effectively used as efficient thorium removal agents that have the potential for use in the separation of thorium in the treatment of thorium-containing sewage. Acknowledgments This research was financially supported by the Country National Defense Fundamental Research Program (Grant 16ZG6101). The authors gratefully acknowledge the technological support of the Engineering Research Center for Biomass Materials, Ministry of Education, Southwest University of Science and Technology.

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29

Figure Captions.

Fig. 1. Preparation scheme of the FFM, PFM and FPFM adsorbents

30

Fig. 2. SEM spectra of the FFMs, PFMs and FPFMs (a, c and e) before and (b, d and f) after adsorption, and elemental mapping spectra of FPFMs (g), C (g1), N (g2), O (g3), Fe (g4) and Th (g5).

31

Fig. 3. (a) EDX spectra of the FPFMs before and after adsorption, (b) FT-IR spectra of the FFMs, PFMs and FPFMs, (c) XPS spectra of the FFMs, PFMs and FPFMs and (d) TG analysis of the FFMs, PFMs and FPFMs.

32

Fig. 4. (a) Distribution of thorium species as a function of pH (total thorium concentration of 1.0 mmol·dm-3 in 1.0 mol·dm-3 KCl at 298.15 K); (b) zeta potential study of the FFMs, PFMs and FPFMs; (c) effect of pH on thorium adsorption by the FFMs, PFMs and FPFMs (initial thorium concentration: 100 mg·L-1, m/v: 0.04 g·L-1); and (d) effect of ionic strength on thorium adsorption by the FPFMs (pH: 5, initial thorium concentration: 100 mg·L-1, m/v: 0.04 g·L-1).

33

Fig. 5. (a) Effect of contact time on thorium adsorption by the FPFMs (pH: 5, m/v: 0.04 g·L-1) and fitting plots of the pseudo-first-order (b), pseudo-second-order (c) and intra-particle diffusion models (d).

34

Fig. 6. (a) Effect of the initial concentration on thorium adsorption by the FPFMs and fitting plots of the Langmuir and Freundlich (b), Temkin (c) and D-R isotherm models (d).

35

Fig. 7. (a) Effect of temperature on thorium adsorption by the FPFMs (pH: 5, contact time: 480 min, m/v: 0.04 g·L-1), (b) effect of the cycle on thorium adsorption by the FPFMs (pH: 5, initial thorium concentration: 100 mg·L-1, m/v: 0.04 g·L-1, contact time: 480 min), (c) effect of coexisting ions on thorium adsorption by the FPFMs (pH: 5, initial thorium concentration: 100 mg·L-1, m/v: 0.04 g·L-1, contact time: 480 min), and (d) comparison adsorption study of the different water systems.

36

Fig. 8. (a) FT-IR spectra of the FPFMs before and after adsorption, (b) XPS survey of the FPFMs and high-resolution C 1s (c), O 1s (d), N 1s (e) and Fe 2p (f) before and after adsorption.

37

Fig. 9. Adsorption mechanism of thorium by the FPFMs.

38

Table 1 Comparison of various adsorbents for thorium removal. Adsorbents

Temperature (K)

Types

pH

qm (mg·g-1)

References

Poly(methacrylic acid) -grafted-cellulose/bent onite

323.15

Organic/inorganic composite

5

188.1

[3]

298

Carbonaceous

4

10.58

[11]

288

Organic composite

2.5

12.75

[13]

Polyamidoxime chelating resin

293.15

Polymer resin

3

227.27

[14]

Titanium dioxide-densified cellulose

303.15

Polysaccharide

5

92.23

[19]

Ginkgo leaf

298

Biomass

4

103.8

[48]

296

Carbonaceous

3

70

[55]

318

Siliceous

4.5

83.4

[57]

CaCl2-modified Giant Kelp biomass

293

Biomass

4

135.13

[70]

Ambelite XAD-7 resin beads

298

Polymer resin

2.6

136.36

[74]

FPFMs

303.15

Biomass

5

326.35

This study

Diglycolamide functionalized multi-walled carbon nanotubes Sulfated-β-CD@NAA

Oxidized biochar fibers 3-aminopropyltriethox ysilane-modified titanosilicate

39

Graphical Abstract

40

Highlights FPFMs are based on the conjunction of both γ-Fe2O3 and PDA onto fungal mycelia. FPFMs fabricated via immobilization exhibit excellent Th(IV) adsorption performance. The chelation, coordination and ion-exchange play an important role in adsorption. FPFMs could be used for repairing multiple types of nuclide-polluted aqueous system.

41