Adsorption of natural composite sandwich-like nanofibrous mats for heavy metals in aquatic environment

Accepted Manuscript Regular Article Adsorption of Natural Composite Sandwich-like Nanofibrous Mats for Heavy Metals in Aquatic Environment Yang Wu, Xiaodan Qiu, Shiyi Cao, Jiajia Chen, Xiaowen Shi, Yumin Du, Hongbing Deng PII: DOI: Reference:

S0021-9797(18)31540-6 https://doi.org/10.1016/j.jcis.2018.12.099 YJCIS 24476

To appear in:

Journal of Colloid and Interface Science

Received Date: Revised Date: Accepted Date:

23 August 2018 27 December 2018 28 December 2018

Please cite this article as: Y. Wu, X. Qiu, S. Cao, J. Chen, X. Shi, Y. Du, H. Deng, Adsorption of Natural Composite Sandwich-like Nanofibrous Mats for Heavy Metals in Aquatic Environment, Journal of Colloid and Interface Science (2018), doi: https://doi.org/10.1016/j.jcis.2018.12.099

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Adsorption of Natural Composite Sandwich-like Nanofibrous Mats for Heavy Metals in Aquatic Environment Yang Wua, Xiaodan Qiua, Shiyi Caoa, Jiajia Chena, Xiaowen Shia, Yumin Dua and Hongbing Denga, *

a

Hubei International Scientific and Technological Cooperation Base of Sustainable Resource and Energy, Hubei Key Lab of Biomass Resource Chemistry and Environmental Biotechnology, School of Resource and Environmental Science, Wuhan University, Wuhan 430079, China

* Corresponding author: Tel.: +86 27 68778501, Fax: +86 27 68778501; E-mail address: [email protected]; [email protected]

Abstract: Natural polymer cellulose acetate (CA) and natural rectorite (REC) were employed to fabricate nanofibrous mats and then immobilized with biosorbent saccharomyces cerevisiae (SCV) to construct a sandwich-like structure. The hydroxyl and carbonyl groups in the CA endowed the nanofibrous mats with a strong affinity for removing heavy metals, allowing them to act as an adsorbent for heavy metals. The REC, which was blended with CA to fabricate the CA/REC nanofibrous mats, increased the specific surface area of the nanofibers and provided ideal scaffolds for the attachment of SCV, resulting in more contact reactions between the nanofibrous mats and heavy metal ions. The adsorption equilibrium was reached within 30 min at the optimum pH of 7, and the saturated adsorption capacities of Zn (II) and Cd (II) were 104.31 and 99.33 mg/g, respectively. The adsorption for Zn (II) and Cd (II) decreased to 47.44 and 62.11 mg/g in the co-system, but the total amount of adsorption (111.36 mg/g) was remarkably higher than that for the single system, indicating that the all-natural composite mats had great potential to simultaneously adsorb multiple heavy metals. After three cycles adsorption-desorption, the composite mats maintained a high adsorption efficiency.

Keywords:

Cellulose acetate/rectorite; Saccharomyces cerevisiae; Sandwich-like

nanofibrous mats; All-natural composite; Metals adsorption

1. Introduction The current situation of heavy metal pollution in water environments is disturbing. Additionally, our inadequate use of natural resources is a significant problem[1-4]. In various methods of environmental problem management, it is best to use natural materials to deal with natural problems for ensuring that the environmental burden is no longer increased and new pollutants are introduced. Turning natural materials such as cellulose into functional and efficient materials has always been the main goal of scientists. Cellulose is the oldest and most abundant natural polymer on the earth. It is inexhaustible and the most precious[5-7] natural renewable resource of mankind[8, 9]. Cellulose chemistry and the cellulose industry arose 160 years ago, and since then, cellulose has been used in various areas[10-13]. In this study, we aim to produce an all-natural composite material that can absorb heavy metals in complex aquatic environments to satisfy the urgent requirement of modern society. The advantages of nanomaterials and biosorption materials for the treatment of heavy metals, such as their high efficiency and low consumption, are universally recognized[14-21]. In our previous work, it was demonstrated that biosorbent saccharomyces cerevisiae (SCV) could be well loaded by poly(ε-caprolactone) (PCL) nanofibrous mats, and the composite mats had good biosorption properties for Pb (II) [22]. This was the first time that the layer-by-layer (LBL) technique was employed for the immobilization of biosorbents for heavy metal removal[23, 24]. In this study, we used the natural polymer cellulose acetate (CA) to fabricate nanofibrous mats via the electrospinning

technique

and

then

immobilized

SCV

onto

them

via

the

bio-electrospraying technique. Compared with PCL, CA, a derivative of cellulose is,

eco-friendly, non-toxic, harmless, biodegradable and biocompatible, making it more suitable for environmental treatments applications[25, 26]. Moreover, the proper tensile strength, high modulus, and adequate flexibility of the CA fibers endow CA nanofibrous mats with additional functions, such as nanofiltration and reverse osmosis[27]. CA nanofibrous mats obtained by electrospinning also possess the typical characteristics of a high porosity, a huge surface area, and as mall interfibrous pore size[28]. Among these sandwich-like composite mats, nanofibrous mats used as templates for biosorption account for a large proportion, making them as important as the biosorption itself. Obviously, if the nanofiber has a large heavy metal adsorption capacity, the performance for removing heavy metals will be better for the overall material. The adsorption capacity of PCL nanofibrous mats for heavy metals is minuscule, requiring further improvement. However, the hydroxyl and carbonyl groups in CA endow it with a strong affinity for heavy metals and therefore it acts as not only a template for immobilizing biosorbents but also an adsorbent for heavy metals[29, 30]. Moreover, because CA is negatively charged, an electrostatic force can be generated between heavy metal ions and CA molecules, which increases the adsorption capacity. It can be reasonably conjectured that the advantages of CA nanofibrous mats may lead to its wide application in heavy metal pollution treatments. To enhance the adsorption performance, rectorite (REC, a type of layered silicate) was added to the composite adsorption material. REC has been widely used and has a large adsorption capacity owing to its lamellar structure, nanoscale-size and large specific surface area[31, 32]. On account of the intercalation between REC and the CA molecules, the addition of REC enlarges the specific surface area of the mats, leading to more

contact reactions between the nanofibrous mats and heavy metals ions[33]. Besides, the negatively charged REC renders a stronger synergistic effect compared with our previous work. The reason was that CA and REC used in this study were both negatively charged, but in our previous study CS were oppositely charged[34]. Obviously, the electrostatic force between CA/REC and heavy metal ions was stronger than that between PCL/CS/REC and heavy metal ions. With the rapid development of industrial production, natural water environments have been affected and are becoming increasingly complex[35-37]. In our previous work, we only discussed the adsorption of Pb ions in water. The present study in which, the adsorption of two kinds of heavy metal ions was discussed in this study, and the adsorption capacity of heavy metals in the mixed system was explored, has greater accordance with the requirements of complex water conditions. The total amount of adsorption in the co-system (111.36 mg/g) is remarkably higher than that in the single systems (Zn (II) 104.31 and Cd (II) 99.33 mg/g). Hence, all-natural composite sandwich-like nanofibrous mats for multiple heavy metals in complex aquatic environment were successfully manufactured in this study.

2. Experimental Details 2.1. Materials CA (Mn = 3.0104 Purity ≥ 97%) was supplied by Sigma-Aldrich Co., USA. REC (Purity 70 ~ 80%) was purchased from Hubei Mingliu Co., China. Acetone and N, N-dimethylacetamide (DMAC Purity ≥ 99.5%) were purchased from the Aladdin Chemical Reagent Co., China. SCV (Purity ≥ 70%) CCTCC AY92003 was obtained from

the China Center for Type Culture Collection, Wuhan University (Wuhan, China). The HNO3 used in the experiments was premium-grade (serviced by Sinopharm Group Pharmaceutical Co., Ltd Purity ≥ 99.5%), and Zn(NO3)2, Cd(NO3)2 , HCl and NaOH were analytical-grade (serviced by Sinopharm Group Pharmaceutical Co., Ltd Purity ≥ 96%). Deionized water was used to prepare all the aqueous solutions (Electrical resistivity = 18.2 MΩcm).

2.2. Fabrication and Characterization of (CA/REC-SCV)n mats 2.2.1. Activation and Expansion of SCV The purchased dry SCV powders were dissolved in 3 mL of a sterilized YPDA medium (1% yeast extract, 2% peptone and 2% glucose), and the mixture was shaken in a constant-temperature bath for 12 h. Then, it was transferred to 50 mL of a sterilized YPDA medium and, shaken in the constant-temperature bath oscillator for 12 h. The above liquid medium was transferred to 500 mL of a sterilized YPDA medium and, shaken in the constant temperature bath oscillator for 12 h. The supernatant was removed via high-speed centrifugation and the powder deposited on the bottom of the centrifuge tube after the high-speed centrifugation and was placed in a vacuum freeze dryer and lyophilized.

2.2.2. Fabrication of (CA/REC-SCV)n mats A CA solution was prepared by dissolving CA powder into a 2/1 (w/w) acetone/DMAC mixture under gentle magnetic stirring for 5 h at room temperature. Next, a CA/REC solution was obtained by adding REC (1% of CA mass) to the CA solution under gentle agitation for 12 h. Then, the CA or CA/REC solution was put into a plastic

syringe driven by a syringe pump (LSP02-1B, Baoding Longer Precision Pump Co., Ltd., China). The CA or CA/REC nanofibrous mats were prepared by electrospinning as shown in process I of scheme 1. The metal needle tip of the syringe, whose diameter was 0.8 mm was fastened by the positive electrode of a high voltage power supply (DW-P303-1ACD8, Tianjin Dongwen High Voltage Co., China). The electric field was 15 kV/15 cm. Besides, the feeding rate was set as 1 mL/h. The relative humidity and ambient temperature were maintained at 50% and 25°C, respectively. The prepared fibrous mats were dried in vacuum at 60°C for 24 h to remove the residual solvents.

Scheme 1. Fabrication process of all-natural composite sandwich-like nanofibrous mats. SCV was added into the aqueous solutions and homogenized with ultrasonic vibration for 1 h (0.05 g/mL). The SCV suspension was electrosprayed onto the electrospun CA or CA/REC nanofibrous mats by using a voltage of 20 kV with a tip-collector distance of 10 cm and a flow rate of 1 mL/h (Process Ⅱ in scheme 1). Repeat

process I and Ⅱ to build the composite nanofibrous mats. Herein, the electrospun and an electrosprayed layers are denoted as a bilayer, called (CA-SCV)n or (CA/REC-SCV)n, where n is the number of bilayers and one layer means 0.5 bilayer. For instance, (CA/REC-SCV)3.5 means that the outermost layer was CA/REC nanofibrous mats, and (CA/REC-SCV)3 means that the outermost layer was SCV.

2.2.3. Characterizations The morphology of the nanofibrous mats (1  1 mm2) was observed by using field emission scanning electron microscopy (FE-SEM) (Zeiss, Germany) at 25℃, 30% humidity. Energy-dispersive X-ray spectroscopy (EDX) was performed using a JEM-2100 (HR, JEOL, Japan). Fourier transform infrared spectra (FT-IR) were recorded by a Nicolet170-SX (Thermo Nico-let Ltd, USA). The detection wave number ranges from 4000 - 400 cm-1 and the number of detection cycles is 64, with air as the background. The small angle X-ray diffraction (SAXRD) was carried out by using a diffractometer type D/max-rA (Rigaku Co., Japan) with Cu target and K-alpha (λ= 0.154 nm) at 40 kV. The scanning range and scanning speed were 1-10° and 1°/min, respectively. The Brunauer Emmett Teller (BET) surface area and pore volume (Barrett-Joyner-Halenda method) of the nanofibrous mats were measured via a nitrogen adsorption-desorption test using a surface area and pore size analyzer (Belprep mini II, Japan) at 77 K in the relative-pressure (P/Po) range of 0.005–0.990.

2.3. Adsorption and Desorption Experiments 2.3.1. Preparation of Metal Solution

1:499 HNO3 was prepared by adding 1 mL of HNO3 to 499 mL of deionized water and used it to obtain stock solutions of 1 g·L−1 Zn(NO3)2 and Cd(NO3)2, diluted as necessary to obtain the standard and working solutions. NaOH and HCl were used to adjust the pH of the initial solution. Fresh dilutions were a prerequisite for each biosorption study.

2.3.2. Adsorption Experiments The biosorption capacity of the SCV-loaded nanofibrous mats for the removal of Zn (II) and Cd (II) was tested in a batch system. First, 20 mg of the composite nanofibrous mats were added to a 100.0 mL solution of multiple metal ions for 12 h in the constant-temperature oscillator. The pH, initial concentration, sorption time, and weight of the composite nanofibrous mats were evaluated to optimize the adsorption efficiency. The concentrations of the metal ions after biosorption were determined using atomic absorption spectroscopy (TAS-990, Persee, China). The biosorption capacity of metal ions (qe (mg g-1)) and the removal rate (Y%) of metal ions were calculated using the following equations: (1) (2)

where C0 and Ce are the initial and equilibrium concentrations of metal ions (mg/L), V is the liquid volume (mL), and W is the mass of the composite nanofibrous mats (mg).

2.3.3. Desorption Experiments

After the adsorption of Zn (II) and Cd (II), 0.1 mol/L HCl was used to regenerate the

SCV-immobilized

composite

nanofibrous

mats

(CA/REC-SCV)3.5.

The

(CA/REC-SCV)3.5 after Zn (II) and Cd (II) adsorption was immersed in the HCl solution and kept for 12 h. It was then washed with deionized water and dried for recycling. Three adsorption-desorption cycles were conducted for each metal, and the Zn (II) and Cd (II) concentrations were measured after each sorption and desorption step.

2.4. Biosorption Kinetics and Equilibrium Models Kinetic equations of pseudo-first-order (3) and pseudo-second-order (4) models were used to describe the adsorption types of heavy metal ions. In this experiment, 20 mg (CA/REC-SCV)3.5 was added to a volume of 100 mL, a concentration of 10 mg/L Zn (II) or Cd solution, and placed in a bench-top constant temperature oscillator with a speed of 170 r/min. Samples were taken at intervals of 5 min, 10 min, 15 min, 30 min, 60 min, 90 min, 180 min, 270 min, 360 min, and 480 min, and then the metal concentration after adsorption was measured by atomic absorption spectrometry. The equations are as follows: (3) (4) Here, qt (mg/g) is the amount of biosorption at different time t (min), K1 and K2 (g·mg-1·min-1) are the rate constants and qe (mg/g) is the amount of biosorption at equilibrium. 20 mg (CA/REC-SCV)3.5 were added to 100 mL Zn (II) or Cd (II) solutions with different concentrations, respectively. The initial concentrations of Zn (II) or Cd (II) in

the different solutions were 20, 40, 60, 80, 120 and 160 mg/mL. Each reaction was allowed to proceed for 120 min until the reaction reached equilibrium. After, interface equilibrium was achieved between the metal ions concentration and the biosorbent, the biosorption was completed[38]. Langmuir and Freundlich isotherms were used as models to describe the equilibrium for the batch system equation. The linear Langmuir isotherm equation is as follows: (5) The linear Freundlich isotherm equation is as follows: (6) Here, qm was the maximum sorption amount, KF, KL and n were constants.

3 Results and Discussion 3.1. Characterization of Materials 3.1.1. Morphology of Composite Nanofibrous Mats The SEM image can represent the microstructure of the material, which helps us to have an intuitive understanding of the material appearance[39, 40]. The morphology of the composite nanofibrous mats changed with respect to the applied voltage, the distance from the needle to the receiver, the injection speed and other solution parameters such as the ratio of solute to solution. The optimized electrospinning and electrospraying parameters for immobilizing objectives to prepare composite nanofibrous mats were determined in our previous works[22, 41, 42].

Under the optimized parameters, there were no spindle-like beads among the uniform nanofibrous mats (Fig. 1a), and the SCV could be evenly dispersed on the surface of the composite nanofibrous mats for 1 h. (Fig. 1b). To avoid the stacking of SCV and obtain a larger exposed surface, a multilayered nanofibrous mats with alternating CA/REC and SCV layers were prepared. In Fig. 1c, the SCV was covered with nanofibrous mats, which confirmed that the LBL technique could well separate and immobilize the SCV layer. As shown in the image of the nanofiber pad (Fig. d), the SCV layer and nanofibrous mats layers were alternately stacked, with a sandwich-like structure. Thus, it could be concluded that enough SCV was loaded to satisfy the adsorption application simply by increasing the number of layers using alternating electrospinning and electrospraying technology.

Figure 1. The morphology of composite nanofibrous mats with LBL construction obtained by alternating electrospinning and bio-electrospraying: (a) CA/REC-SCV, (b) CA/REC-SCV, (c) cross-section of (CA/REC-SCV)3 and (d) cross-section of (CA/REC-SCV)3.5.

3.1.2. Composition and Structure Analysis

Figure 2. (a) FT-IR spectra of the bulks and the composite nanofibrous mats, (b) SAXRD patterns of the bulks and composite nanofibrous mats and (c) The nitrogen adsorption-desorption isotherms and surface area data of the nanofibrous mats. Error bars represent the standard deviation (n = 3). The cell wall of yeast cells is mainly composed of polysaccharides (D-glucan and D-mannan), and also includes a small amount of protein, fat, minerals, etc.[43]. In Fig. 2a, the peaks at 1,157 and 1,043 cm-1 are related to the C-OH tensile and skeletal vibrations, confirming the presence of D-glucan[44]. The absorption peak at 2,881 cm-1 indicates the presence of a small amount of lipid, and the absorption peaks around 1,566, 1,658 ,and 1,265 cm-1 correspond to the stretching of the C=O, -CN and -NH groups of the protein causing by the stretching of the amide group[45-47]. The peak at 1,740 cm-1 is the absorption peak of the C=O functional group in CA, the peak at 1,050 cm-1 is the

symmetric stretching of C-O, and the peak at 1,640 cm-1 represents the C-O-C group[48]. For REC, the absorption peaks at 1,025 and 1,050 cm-1 are caused by the stretching vibration of Si-O, the characteristic peaks at 467 and 546 cm-1 are caused by the bending vibration of Si-O, and the absorption peaks of -OH are at 3,643 and 910 cm-1[26]. Comparing the spectra of CA and REC reveals that the spectrum of CA/REC contains CA-related characteristic peaks, and the characteristic peaks at 467 and 546 cm-1 confirm that REC was successfully introduced into the composite nanofibrous mats. As shown in Fig. 2a, the spectrum of (CA/REC-SCV)3.5 exhibits an absorption peak of -OH at 3643 cm-1, and peaks at 467 and 546 cm-1 based on the Si-O bending vibration, indicating the existence of REC. Additionally, the absorption peak at 2,881 cm-1 and the C-OH stretching vibration peak at 1,043 cm-1 indicate the presence of SCV. The analysis of the absorption peaks of the aforementioned characteristic functional groups further confirms the successful preparation of the all-natural composite sandwich-like nanofibrous mats. Notably, the absorption peaks of each functional group in the spectrum of (CA/REC-SCV)3.5 dose not move compared with the single component, indicating that no chemical change occurred in the preparation process[49, 50]. SAXRD was used to detect the interaction between the REC and the polymer molecular chains. The results are shown in Fig. 2b. No remarkable peak is observed in CA, SCV, and (CA-SCV)3.5 composite nanofibrous mats in the range of 2-10°. However, the REC and (CA/REC-SCV)3.5 exhibited obvious diffraction peaks at 2θ values of approximately 3.60° and 3.28°, and calculations using Bragg’s equation revealed the corresponding interlayer spacing to be 2.45 and 2.69 nm, respectively. The characteristic diffraction peak of all the REC-containing simples shifted to lower value, indicating that

the interlayer distance of REC was increased. Compared with that of REC, the characteristic diffraction peak of (CA/REC-SCV)3.5 shifted toward a slightly lower angle, and the interlayer distance was increased to 2.69 nm, indicating that the CA chains were successfully intercalated. The table in Fig. 2c presents the specific surface area of CA, CA/REC and (CA/REC-SCV)3.5. Compared with that of the CA nanofibrous mats, the surface area of the CA-RCE nanofibrous mats was increased by 163% because of the addition of REC, indicating that the REC could significantly increase the surface area of the composite nanofibrous mats. Despite the decrease in the BET surface area of the nanofibrous mats after SCV immobilization, it (2.5 m2/g) was still much higher than that (1.6 m2/g) of the pure CA nanofibrous mats. In summary, REC played a significant role in improving the specific surface area of CA, affecting its application, as follow. 3.1.3. Hydrophobicity and Mechanical Properties

Figure 3. (A) A histogram of the time distribution when the contact angle became 0°for the nanofibrous mat, (B) images of water contact angle of the nanofibrous mats with different contact times, (C) representative stress-strain behavior and (D) the tensile strength and elastic modulus of the nanofibrous mats in dry and wet state: (CA/REC-SCV)3 dry (a) and wet (b) state and (CA/REC-SCV)3.5 dry (c) and wet (d) state. Error bars represent the standard deviation (n = 3). Figs.3 (A) and (B) show the water contact angle data for the nanofibrous mats, indicating the hydrophilicity and wettability of the mats. For all the nanofibrous mats, the contact angle ultimately became 0°, indicating that the mats had certain wetting properties, which makes them advantageous for application in water environment treatment. The contact angle of CA/REC (133.9°) is larger than that of CA (120.5°). The reason for this might be that when the water contact angle was greater than 90°, it was

positively correlated with the roughness of the surface, and the addition of REC increased the roughness of the nanofibers. When the outermost layer was SCV, the water contact angle of (CA/REC-SCV)3 was substantially reduced, demonstrating the good hydrophilicity of (CA/REC-SCV)3. The time was also greatly shortened, and the contact angle became 0° within 1.6 s, clarifying the wettability of (CA/REC-SCV)3. This may due to the abundant hydrophilic groups of the SCV cells which could facilitate the extension and immersion of water droplets. For (CA/REC-SCV)3.5, although the outermost layer was CA/REC, the water contact angle was relatively small (113.9°), and the water droplet was immersed quickly (13.1 s). This is possibly because the CA/REC layer that covered the SCV layer was fluffy owing to the electric charge, which was beneficial for the infiltration of water droplets. The hydrophilicity and wettability of the composite nanofiber mats with SCV immobilized were better than those of the mats without SCV, which is conducive to application in heavy metal adsorption. In the process of heavy metal adsorption, whether the mats can maintain a good physical form under the action of water flow is one of the key factors for the reuse of the mats. Therefore, the mechanical properties of the mats under dry and wet conditions were analyzed, as shown in Figs 3 (C) and (D). The addition of REC greatly enhanced the tensile strength of the nanofibrous mats, and the tensile strength of the nanofibrous mats was increased from 0.24 MPa (CA) to 0.57 MPa (CA/REC). In the wet state, although the tensile strength of the mats was slightly reduced, the elastic modulus of the mats was significantly improved, illustrating that the film maintained mechanical strength and had good flexibility in water. As the number of layers increased, the tensile strength of the

mats increased remarkably. The tensile strength was the largest (1.12 MPa) when the number of layers was 3.5. The mechanical properties of the mats, especially the elastic modulus, were affected by the outermost layer. When the outermost layer was SCV, the elastic modulus of the mats was higher than that when the outermost layer was CA-REC, probably because SCV has good hydrophilicity. When the SCV layer absorbs moisture, it can be wrapped in CA/REC fibers, making it more resistant to elastic deformation. The aforementioned results indicate that the composite nanofibrous mats have good mechanical properties, which make them advantageous for resisting to water flow in heavy metal adsorption, and prolong their service life.

3.2. Adsorption Efficiency Investigation

Figure 4. Optimization of parameters during biosorption process. The removal rate of Zn (II) and Cd (II) was varied by different (a and b) pH value, (c and d) biosorption time, (e and f) initial concentration and (g and h) adsorbent dose. Error bars represent the standard deviation (n = 3).

The adsorption of heavy metals was a sophisticated process, influenced by many different factors, including the pH, adsorption time, initial concentration of heavy metals, and dose of adsorbents for the biosorption of Zn (II) and Cd (II). A biosorption study on the coexistence of Zn (II) and Cd (II) was performed under optimized parameters. All the reaction systems were put into the oscillator at a speed of 200 r/min.

3.2.1. Effect of Different Values First, 20 mg SCV-immobilized composite nanofibrous mats with different layers were added to a 10 mg/L Zn(NO3)2 and Cd(NO3)2 solution under different pH values(Figs. 4a and b). Overall, the adsorption capacity for each metal ion was increased with the gradual increase of solution pH, and the optimum solution pH for both Zn (II) and Cd (II) was approximately 7. At a low pH, the ligands on the SCV combined with the H ions owing to the competition between the H ions and the Zn (II) and Cd (II) metal ions for binding sites. With the increase of pH, the positively charged metal ions were associated with the free binding sites, and the adsorption capacity of the mats towards the metals was greatly improved, which is in agreement with the previous reports. The optimal adsorption effect occurred when the waste water was nearly neutral, making the composite nanofibrous mats loaded with SCV beneficial for practical industrial applications. Notably, Zn (II) and Cd (II) could precipitate when the pH was higher than 7.0. As previously mentioned, the metal ions Zn (II) and Cd (II) as congeners exhibited the same adsorption tendency (Figs. 5a and b). With the addition of REC, the adsorption capacity of the nanofibrous mats for Zn (II) and Cd (II) increased slightly compared with the pure CA mats, possibly owing to the increased surface area between the interlayers of REC[22, 51]. The adsorption capacity of (CA/REC-SCV)3.5 was slightly larger than that

of (CA/REC-SCV)3, confirming that the LBL structure immobilized the SCV efficiently and reduced the loss of SCV. The adsorption ability of (CA/REC-SCV)3.5 was significantly better than that of CA/REC owing to the ionization of functional groups, and most microbial surfaces were negatively charged, thereby contributing adsorption sites to the binding of metal ions[17]. As shown in Figs. 4c and d, both Zn (II) and Cd (II) achieved adsorption equilibrium within 100 min. However, the adsorption capacity for Zn (II) and Cd (II) reached a maximum in 30 min, and then decreased slightly. This is because the ion-exchange process was fast, and a few metal ions could have been dissociated from the mats. As shown in Figs. 4e and f, when the concentration of the metal ions increased from 20 to 160 mg/L, the adsorption capacity of (CA/REC-SCV)3.5 for Zn (II) and Cd (II) was significantly enhanced. The reason is that a higher concentration yielded, more contacts between the composite mats and the metal ions, making adsorption more likely to occur. However, as the concentration of metal ions increased beyond a certain point, the adsorption capacity remained constant. The saturated adsorption capacities for Zn (II) and Cd (II) were 104.31 and 99.33 mg/g, respectively. Additionally, the removal rate of metal ions was inversely proportional to the initial concentration. At a low concentration, the removal rate was higher than 60%. Thus, this material has good application prospects for the treatment of low-concentration metal solutions, which was more suitable for natural water environment. As shown in Figs. 4g and h, the removal rate of (CA/REC-SCV)3.5 increased with the adsorbent dose. When the adsorbent dose increased from 5 to 30 mg, the removal rate for Zn (II) and Cd (II) increased significantly, as confirmed by the larger amount of binding

sites provided by SCV with the increase of the number of the layers[52]. The amount of Zn (II) and Cd (II) biosorption decreased from 103.02 to 55.14 mg/g and 106.68 to 55.67 mg/g, respectively, which is attributed to the solute availability, electrostatic interaction, and interference between the binding sites[53, 54].

3.2.2. Effect of Coexistence of Metal Ions Fig. 5a shows the adsorption process of (CA/REC-SCV)3.5 for metal ions. For CA/REC nanofibers, REC molecules can be intercalated by CA molecules, and the expansion of specific surface area is beneficial for heavy metal adsorption. The hydroxyl and carbonyl groups in CA endow it with a strong affinity for heavy metals. K+, Na+ and Ca2+ in the REC can be ion exchanged with heavy metals. There are four main ways to adsorb metal in SCV: native biosorption, metal-binding proteins, ion exchange and metal precipitation. We applied 20 mg of (CA/REC-SCV)3.5 to examine the effect of the coexistence of metal ions on the biosorption. The concentrations of Zn (II) and Cd (II) were both 10 mg/L, the pH value was approximately 7.0, and the temperature was approximately 25℃. The adsorption effect for different contact time was investigated in a mono-solvent (Zn (II), Cd (II)) a binary system (Zn (II)—Cd (II)). As shown in Figs. 5b and c, with coexistence of Zn (II) and Cd (II), the adsorption for Zn (II) and Cd (II) deceased to 47.44 and 62.11 mg/g, respectively. Compared with the mono-solvent case, the adsorption capacity was greatly reduced, because these coexisting ions competed for the limited negatively charged groups on the mats, resulting in a decrease in the amount of adsorption of single metal ions. However, the total amount of adsorption in the binary system (111.36 mg/g) was remarkably higher than that in the single system. Additionally,

the adsorption ratio of Cd (II) and Zn (II) was 0.96 in the mono-solvent system and increased to 1.31 in the binary systems, indicating that the all-natural composite nanofibrous mats had a large selective adsorption capacity for Cd (II) while maintaining a large adsorption capacity of Zn (II)[55].

Figure 5. (a) Schematic diagram of adsorption process and the effect of coexistence of (b) Zn (II) and (c) Cd (II) metal ions for biosorption. Error bars represent the standard deviation (n = 3).

3.3. Kinetic Models and Isotherm Models 3.3.1. Composition Analysis Before and After Biosorption EDX analyses were performed for investigating the surface composition of the composite nanofibrous mats before and after biosorption (Fig. 6). C, N, O, Si, Al, P, K, and Ca on the surface of the mats were detected using EDX. The peaks of Si and Al for both CA/REC and (CA/REC-SCV)3 correspond to REC, confirming that REC was

successfully assembled on the surface of the CA fibrous mats. The peaks of N, P, K, and Ca, correspond to SCV, whose composition included N, P, small amounts of K, Ca and so on. After biosorption, distinct peaks of Zn (II) and Cd (II) emerged for the (CA/REC-SCV)3 composite nanofibrous mats (Figs. 6c and d), indicating that the biosorption process was implemented effectively. Besides, the peaks of K and Ca disappeared after biosorption, suggesting that ion exchange of K+/Ca2+ and Zn (II)/Cd (II) occurred during biosorption via the release of a large amount of K+/Ca2+.

Figure 6. The elemental composition of SCV loaded composite nanofibrous mats before (a and b) and after (c and d) biosorption: (a) CA/REC, (b) (CA/REC-SCV)3, (c) (CA/REC-SCV)3 after adsorbing Zn (II), (d) (CA/REC-SCV)3 after adsorbing Cd (II). The previous study reported the release of K+ and other cations during the adsorption of Zn (II) by SCV, confirming that ion exchange is one of the important mechanisms for the biosorption of metal ions by SCV. In addition, Zn and Cd were

congeners, exhibiting similar adsorption mechanism. Hence, ion exchange possibly occurred during the removal of Zn (II) and Cd (II) in this system. Other adsorption mechanisms, such as surface complexation and electrostatic adsorption, were not explored in this study.

3.3.2. Sorption Interpretation Based on Mechanistic Modelling Table 1 pseudo-first-order qe

K1 -1

(mg·g )

Zn (II) Cd (II)

qe

-1

-1

-1

0.0488 ±

82.37 ±

0.9999 ±

0.8471

0.0024

0.0010

1.5236

0.0007

0.0078 ±

3.503 ±

0.2617 ±

0.0348 ±

86.96 ±

0.9980 ±

0.0025

0.5105

0.0009

0.0045

1.9457

0.0011

2.828 ±

0.0011

-1

R2

0.2617±

0.0039 ±

-1

qe (mg·g-1)

(mg·g )

83.34

K2

R2

(g·mg ·min )

(g·mg ·min )

83.13

pseudo-second-order

Table 2 Langmuir Model -1

Zn (II) Cd (II)

-1

Reactivity sites

Freundlich Model 2

-1

2

KL/(g·mg )

qm/(mg·g )

R

KF/(mg·g )

n

R

0.0700 ±

114.9 ±

0.9937 ±

27.73 ±

3.471 ±

0.8615 ±

0.0875

5.374

0.0007

7.864

0.1574

0.0218

0.087 ±

107.5 ±

0.9976 ±

34.419 ±

4.357 ±

0.9109 ±

0.6662

3.421

0.0004

2.758

0.0781

0.0893

(mmol/kg) 1756 ± 82

956 ± 30

Error bars represent the standard deviation (n = 3). The correlation coefficients and isotherm parameters of the Kinetic models were utilized to investigate the mechanisms of metal ions biosorption and to evaluate the performance of the composite nanofibrous mats. Table 1 shows the results for the rate constant of the pseudo-first-order and pseudo-second-order models. For Zn (II) and Cd (II), the correlation coefficients R2 of the pseudo-second-order adsorption model were 0.9999 and 0.9980, respectively. The biosorption capacities calculated by this model were similar to those determined via experiments. However, the pseudo-first-order model had

an unsatisfactory fitting, which is consistent with previous results[56, 57]. According to the above analysis of the adsorption kinetics, the adsorption process was dominated by chemisorption. Langmuir and Freundlich isotherm models derived from the fitting of experimental points are presented in Table 2. The correlation coefficients R2 for Zn (II) and Cd (II) were both 0.9996. The maximum amount of adsorption derived from the formula was close to the experimental results, clarifying the good fit of the Langmuir model to the biosorption of Zn (II) and Cd (II) by the SCV-immobilized composite nanofibrous mats. However, the correlation coefficients R2 for Zn (II) and Cd (II) according to the Freundlich model were 0.8428 and 0.9147, respectively. Summarizing the relevant parameters of Table 2, compared with the Freundlich model, the Langmuir model was more adequate for modeling the isotherm of the removal of Zn (II) and Cd (II) by the composite nanofibrous mats in this study. The calculation results of the activity sites are shown in Table 2. The difference in the activity sites of the two metals on the same adsorbent suggests the existence of multiple activity sites. According to the results of the previous adsorption efficiency, it can be seen that in the two metal coexistence systems, the total adsorption amount of the two heavy metals is greater than the adsorption amount of each metal in the single system, proving the existence of different adsorption sites too. And, the total amount of the two heavy metals is smaller than the sum of the adsorption amounts of the two heavy metals in the single system, indicating that the two metals have a competitive relationship with some active sites. Under the optimum conditions, the experimental data of the adsorption of heavy metals on different concentrations were compared with the data simulated by Langmuir

model (Table 3). It was found that the model was consistent in the concentration range of 40 to 120 mg/L. When the concentration is greater than 120 or less than 40, the actual adsorption amount is less than the analog value, the simulated relative error is greater than 3%, and the error increases with the concentration. Table 3 Ce (mg/L) -1

Cd (Ⅱ)

Qe（mg·g ）

10

20

40

60

80

100

120

140

18.14 ±1.17

38.27 ± 0.89

65.65 ± 1.14

82.35 ± 1.87

92.77 ± 1.79

96.64 ± 1.87

95.67 ± 0.11

97.04 ± 0.78

96.32 ± 0.11

32.49

49.90

68.16

83.44

90.17

93.97

96.39

98.39

99.33

18.64 ±0.79

35.38 ± 1.83

60.87 ± 1.14

85.90 ± 1.51

97.67 ± 1.78

99.73 ± 1.87

100.82 ± 0.47

100.75 ± 0.83

100.27 ± 0.83

29.82

47.35

67.07

84.71

92.85

97.54

100.58

102.72

104.31

-1

qe（mg·g ） -1

Zn (Ⅱ)

5

Qe（mg·g ） -1

qe（mg·g ）

Qe represents the actual equilibrium adsorption amount by experiments. q e represents the equilibrium adsorption amount simulated by the Langmuir model. Error bars represent the standard deviation (n = 3). In summary, it was found that the Langmuir isothermal adsorption model had a higher correlation coefficient than the Freundlich isotherm model, revealing that the adsorption was dominated by the chemical process of monolayer adsorption. The conditions of this Langmuir model are at the concentration of 40 to 120 mg/L at pH 7, 25℃. And Zn (II) and Cd (II) compete for some activity sites during the adsorption process, making the adsorption process complicated.

3.4. Desorption Assay

Figure 7. Desorption properties and reusability of composite nanofibrous mats for (a) Zn (II) and (b) Cd (II). Error bars represent the standard deviation (n = 3). A highlight of the adsorbent prepared in this study is its reusability, which not only aids the removal of heavy metals but also increases the cost-effectiveness. Therefore, a 0.1 mol/L HCl solution was used to elute Zn (II) and Cd (II) absorbed by (CA/REC-SCV)3.5. The results are shown in Fig. 7. The H ions and metal ions in the solution competed for the sites on the adsorbent surface, causing the desorption of the heavy metal ions. After three repeated adsorption desorption tests, the biosorption capacity for Zn (II) was 82.55, 73.96, and 56.89 mg/g, and that for Cd (II) was 82.33, 73.00 and 62.59 mg/g, respectively. (CA/REC-SCV)3.5 maintained a desorption rate above 60%. Hence, according to the aforementioned biosorption and desorption experiments, the SCV-immobilized composite nanofibrous mats are suitable adsorbents for industrial application.

4. Conclusion Highly efficient and affordable composite nanofibrous mats were prepared using pure natural components. The adsorption capacity of Zn (II) and Cd (II) in water was significant, and cyclic experiments proved that the materials could be reused. The all-natural composite nanofibrous mats had a high removal rate for low concentrations of heavy metals, which is particularly suitable for micro-contaminated waters in natural water bodies, suggesting their practical applicability. Compared with our previous work, this study considered the adsorption performance of the nanofibers, which greatly improved the utilization efficiency of the whole material. Additionally, we evaluated the adsorption capacity of two heavy metal ions (Zn (II) and Cd (II)) (rather than one heavy

metal ion Pb (II) in the previous), and found that the SCV-immobilized composite nanofibrous mats had better adsorption performance for Cd (II). This discovery is interesting and might be the focus of our next study. The composite nanofibrous mats were taken from nature and eventually return to nature. They demonstrate a benign method of environment treatment, providing new ideas for further research.

Acknowledegments This work was supported by the National Natural Science Foundation of China (No. 51473125), partially supported by the Natural Science Foundation of Hubei Province of China (Team Project, No.2015CFA017) and the Fundamental Research Funds for the Central Universities of China (No. 2042017kf0175).

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Graphical abstract