Preparation of N,S-codoped magnetic bagasse biochar and adsorption characteristics for tetracycline

Agricultural waste disposal and purification of polluted water are always the key issues of environmental restoration. In this work, thiourea-functionalized magnetic bagasse biochar (MFeBC) was prepared for tetracycline (TC) removal from aqueous solutions. Firstly, MFeBC was prepared by a combined impregnation and chemical coprecipitation method. Furthermore, MFeBC was characterized by Brunauer–Emmett–Teller surface area analysis, Fourier transform infrared spectrometry, X-ray diffraction analysis, scanning electron microscopy, X-ray photoelectron spectroscopy and the magnetic hysteresis curves. For the TC adsorption, the effects of different solution pH level, adsorbent dosage, initial TC concentration and temperature on the adsorption performance were studied respectively. Moreover, the results indicated that the Freundlich isotherm models appropriately described the adsorption process. The kinetic data were better fitted by the pseudo-second-order kinetic model. The maximum TC adsorption capacity of MFeBC reached 69.26 mg g−1. Hydrogen bonding and Π–Π interactions played a dominant role in the adsorption process. Therefore, MFeBC can be used as an effective adsorbent for tetracycline removal from aqueous solution.


Introduction
With the increasing consumption of antibiotics year by year, antibiotics pollution problems and the potential hazards have attracted many domestic or foreign researchers. 1 Among them, TC antibiotics are a broad-spectrum class of antibiotics discovered in the 1940s and widely used against infections caused by Gram-positive and Gram-negative bacteria, intracellular mycoplasma and chlamydia. 2 Due to its stable structure containing naphthalene, TC can hardly be metabolized by animals. 3 70-90% of TC antibiotics is excreted to the environment, posing potential threats (acute or chronic) to human health. 4 Therefore, tetracycline (TC) has one of the highest concentrations and frequency detection in aquatic environments. 5 Thus, an effective handing of TC is of great signicance.
Many efforts have been made to effectively remove TC from wastewater, such as advanced oxidation, 6 photocatalytic degradation, 7 electrochemical treatment, 8 membrane separation, 9 biodegradation 10 and adsorption. 11,12 Among these methods, adsorption is considered to be an economic and effective method for its' advantages of convenient operation, high removal efficiency, no secondary pollution and easy recycling. 13 For traditional adsorbent materials were expensive, such as activated carbon and ion exchange resin, the research of industrial by-products or agricultural wastes as low-cost carbonbased adsorbent materials has been paid more and more attention. With fascinating characteristics, high electrical conductivity, environmental benignity, stable electrochemistry and large specic surface area, carbon-based materials have been widely used in the eld of adsorption and supercapacitor. 14 Sugarcane is widely used in sugar industry and a large amount of bagasse waste was produced. 15 Bagasse mainly consists of cellulose (50%), polyoses (27%) and lignin (23%), so it is an excellent precursor for biochar preparation. 16 Many studies have shown that bagasse can be used to remove different antibiotics. [17][18][19] However, its adsorption capacities for antibiotics were poor, and more importantly it was very difficult to separate the adsorbent from solution in practical application. Therefore, how to improve its adsorption capacity, effectively recycle and utilize biochar is the current research hotspot. 20 In recent years, magnetic separation technique has been developed and attracted much attention for its unique separation performance. 21 Modied biochar with magnetic media (Fe, Co, Ni, or their oxides) could achieve rapid separation and recovery in an external magnetic eld. 22 There were two main methods of magnetic attachment, one was co-pyrolysis aer impregnation with magnetic precursors, 23 the other was chemical co-precipitation of ferric and ferrous ions on the surfaces of biochar under alkaline conditions. 24 The magnetic intensity of biochar always affects the adsorption performance, so the innovative methods and the specic adsorption mechanism still needs to be further studied.
In addition to strong magnetic, the strength of adsorption performance was the fundamental factor to measure the performance of biochar. Thiourea is a kind of non-pollution and lowtoxicity reagent rich in nitrogen and sulfur. 25 Many studies have shown that thiourea modication can improve the adsorption properties of biochar for many pollutants. [26][27][28] Wei Mao et al., 29 used thiourea to introduce N-S elements to the surface of corn stalk biochar, the adsorption performance of ciprooxacin and Cr was improved greatly. Therefore, thiourea can be a potential modier for preparation of high-performance magnetic biochar.
In this study, thiourea-functionalized magnetic bagasse biochar (MFeBC) was successfully prepared by combined copyrolysis and co-precipitation. The co-precipitation reaction was carried out on the carbon precursors, and the bagasse was impregnated with Fe 2+ /Fe 3+ mixed solution, followed by calcination carbonization, which can further enhance the magnetism. 30 And the effects of magnetic and thiourea-magnetic modications on characteristics of biochar were explored. Then, the TC adsorption behavior, including the adsorption kinetics, isotherms and adsorption mechanisms were studied. This research provided important theoretical and technical support for the potential application of highly adsorption magnetic biochar for antibiotics.

Chemicals and materials
Bagasse was collected from a fruit market in Pingdingshan of Henan province, China. All chemicals including KOH, HCl, ethyl alcohol, thiourea, FeCl 3 and FeSO 4 $7H 2 O were analytically pure reagents purchased from Sinopharm Chemical Reagent Co., Ltd (Shanghai, China). Tetracycline hydrochloride (TC) (purity $ 95%) was purchased from Sigma. The pH of the TC solution was adjusted by HCl or NaOH aqueous solution with suitable concentration.

Preparation of MFeBC
The collected bagasse was washed by distilled water and soaked for 24 h to remove excess sugar from the bagasse. Then dried in an oven at 80 C for 24 h. Finally, they were crushed into small pieces and sied.
Magnetic composite was synthesized in an ultrasound clean bath operating at 25 kHz with a power of 140 W (KQ-200KDE, China). 5 g screened bagasse was added to 200 mL solution (FeCl 3 : 0.05 mol L À1 , FeSO 4 : 0.025 mol L À1 ). Then, ammonia water (3.5 mol L À1 ) was added dropwise into mixed Fe 2+ /Fe 3+ solution until pH > 10.0. The magnetic bagasse was collected aer 30 min reaction. The collected solid was rinsed repeatedly with distilled water to remove excess iron ions and makes the solution neutral. Then, the magnetic bagasse was calcined at 300 C for 60 min to obtain magnetized bagasse biochar (FeBC). Particle between 100-mesh (0.15 mm) and 120-mesh (0.12 mm) was used.
At last, magnetic bagasse biochar was modied by thiourea. FeBC (1 g) was immersed in a mixed water solution (25 mL) with 0.0625 mol L À1 KOH, 0.0821 mol L À1 thiourea and 33% ethanol. Then the resultant suspension was heated in a water-bath at 90 C for 30 min. Aer washing the product to pH ¼ 7.0 and drying it in an oven, the nal product magnetized modied biochar (MFeBC) was obtained.

Characterization of biochar
The specic surface area (S BET ) was evaluated from the N 2 adsorption isotherms with a surface area and porosity analyzer (Micromeritics ASAP 2020, America). The surface morphology was characterized using scanning electron microscopy (SEM, S-4800, Hitachi). The X-ray diffractometer (XRD, F-7000, Shimadzu) was used to detect the crystal structure of the biochar. Additionally, the functional groups on biochar were analyzed by Fourier Transform Infrared Spectroscopy (FTIR, NEXUS 670, Thermo Fisher Nicolet, USA). The surface chemical composition was conrmed by the X-ray photoelectron spectroscopy (XPS, Escalab 250xi, Thermo Fisher, USA). The magnetic properties of MFeBC were assessed using a vibrating sample magnetometer (SQUID-VSM, Quantum Design, USA).

Adsorption experiments
Batch adsorption experiments were carried out to study the adsorption behaviors of TC on MFeBC. The impact of different factors was studied, such as solution pH, adsorbent doses, contact time, initial TC concentration and temperature. In a typical run, adsorbent was added to the TC solution with different pH or TC concentration. The samples were taken out at different reaction time, and then the adsorbent was quickly separated from the solution by centrifuge. The residual TC concentration was detected by UV-vis spectrophotometer (TU- Fig. 1 The XRD patterns of BC, FeBC and MFeBC. 1810, Persee) at 271 nm. Each experiment was repeated three times to get the average.
The TC removal efficiency and TC equilibrium adsorption capacity were calculated according to the following equation eqn (1) and eqn (2): (1) where R (%) was the removal rate; C 0 and C e (mg L À1 ) indicated the TC initial concentration and TC equilibrium concentration; q e (mg g À1 ) was the TC equilibrium adsorption capacity; V (L) was the initial TC volume; m (mg) was the mass of adsorbent.

Result and discussion
3.1 Biochar characterization 3.1.1 XRD. The XRD patterns of BC, FeBC and MFeBC were presented in Fig. 1 to analyze the crystalline mineral structure of adsorbents. The broad peak around at 26.4 was graphitic carbon, which described their good carbonization degree during the pyrolysis process. 31   were observed, which were indexed to (220), (311), (400), (511) and (400) planes of Fe 3 O 4 , 32,33 based on the analysis of the soware Jade 6.0 (JCPDS no. . The XRD patterns of MFeBC and FeBC were identical and identied as Fe 3 O 4 . But the peak intensity reduced slightly, suggesting that thiourea modication will affect the crystal structure of Fe 3 O 4 to a certain extent. In general, Fe 3 O 4 was successfully loaded on the surface of biochar. 3.1.2 SEM. The surface morphology and pore structure have an obvious inuence on adsorption performance. Further, it was very helpful for the research on the adsorption performance. In this research, the surface morphology and pore structure of BC, FeBC and MFeBC was analyzed, and the results were presented in Fig. 2. Using bagasse as the precursor material, its morphological structure with open macroporosity (Fig. 2(a)) allowed for the penetration of iron ions (both Fe 2+ and Fe 3+ ) into the inner pore space, as well as for deposition of these ions on the outside surfaces. 34 The incorporation of iron ions occurred onto electron-rich oxygen atoms of the polar hydroxyl/ ether groups in cellulose. This immobilized the iron ions onto the BG surfaces, both in the inner and the outer macropores. 19 From Fig. 2(d), the surface of BC was relatively smooth and had no obvious particle coverage. Aer magnetization (Fig. 2(e)), a large number of Fe 3 O 4 spherical particles were observed on the surface. In additional, more pores were formed (as Fig. 2(f)), which can be attributed to the load of Fe 3 O 4 nano-particles. The conclusion of Zhou et al. and Jaegwan Shin et al. 35,36 have also conrmed our point of view. For MFeBC, spherical particles can also be seen (Fig. 2(c)). Further, more pore structures developed pore in the surface of MFeBC. The presence of S and N in Fig. 2(h) was account for the modication of thiourea introducing amidogen and sulfur-containing groups to MFeBC. Therefore, it was conrmed that MFeBC contained C, N, O, S and Fe, which was matched with SEM mapping.
3.1.3 BET. N 2 adsorption-desorption method was carried out to study the porous structure of the original BC and MFeBC. As shown in Fig. 3, both curves displayed stable or slow downward trend at low relative press then a steep rise when P/P 0 > 0.8. The adsorption of N 2 decreases with the increase of P/P 0 , which may be due to the fact that the overall pore structure of the biochar calcined at low temperature (300 C) was not developed and the material itself is ne powder particles (100-120 mesh). According to IUPAC classication, 37 the isotherms of BC and MFeBC were exhibited as type II isotherms, indicating a large fraction of macropores. The specic surface area of BC and MFeBC reached 2.0710 m 2 g À1 and 10.0525 m 2 g À1 , respectively. The Fe 3 O 4 particles loaded on the surface of biochar can produce more pore structure, which was benecial to the increase of specic surface area. Although the surface area of MFeBC was improved, the surface area was still at a low level. It was proved indirectly that the high adsorption of TC by MFeBC was due to the chemical adsorption rather than physical adsorption.
3.1.4 FTIR. The functional groups in BC, FeBC and MFeBC were investigated by FTIR analysis (Fig. 4). Aer magnetization, a distinctive IR peak of the Fe-O band in relation to Fe 3 O 4 was detected at 572.4 cm À1 in FeBC and MFeBC. 38 The adsorption peaks at around 818.1 cm À1 and 906.0 cm À1 were due to the presence of aromatic/heteroaromatic structures, 39 which could provide p-electron and had the potential to capture TC ions. 40 The peak at 3309 cm À1 corresponded to the O-H stretching vibration of -OH. 41 For MFeBC, the peak was wider and stronger, which due to the existence of hydrogen bond between -OH and -NH 2 . 42 The peaks at 1372 cm À1 and 1579 cm À1 were associated with C-N bonding and C]S of thiourea moiety, respectively. 25 These observations conrmed that MFeBC was successfully modied with thiourea. The other peaks were found at 2901 cm À1 (CH-stretching of aliphatic groups) 43 and 1312 cm À1 (C-H bending of aldehyde groups). From the above results, abundant oxygen polar functional groups produced in MFeBC and they can facilitate the p-p conjugation between aromatic rings of biochar and TC. 44 3.1.5 XPS analysis. High resolution XPS spectra of C, O, N, S, Fe and survey spectra of MFeBC are exhibited in Fig. 5. A dominant C 1s peak ($285.0 eV), an O 1s peak ($533.0 eV), a N 1s peak ($400.0 eV), a S 2p peaks ($165.0 eV) and a Fe 2p ($710.0 eV) can be observed in the survey spectrum ( Fig. 5(a)), conrming the existence of N, S and Fe. The high-resolution   spectrum of C 1s shown that C existed in many forms in MFeBC (Fig. 5(b)). The strongest peak located at 285.4 eV and referred to C-O (alcoholic, phenolic, hydroxyl and/or other). The peak at 284.4 eV represented for C]C 45 or C-C bonds. 46 The peaks for C]O 47 and C-N 48 were found at 287.6 eV and 286.6 eV respectively. The deconvoluted results of the high-resolution N 1s spectrum shown in Fig. 5(d) revealed that there were three types of N species in MFeBC, corresponding to graphitic-N (401.0 eV), pyrrolic-N (400 eV), and pyridinic-N (398 eV). 49 It has been reported that N can signicantly increase adsorption capacity and diffusivity of biochar by facilitating the capacity and rate performance of material anode. 50 In S 2p spectrum (Fig. 5(e)), 163.76 eV and 168.67 eV refer to C-S and RSO 3 À . 51 Therefore, two types of sulfur containing groups were added on the surface of MBC: one was C-S formed through dehydration condensation of -SH in thiourea and -COOH on the surface of biochar, the other were small amounts of RSO 3À formed during this process. Meanwhile, ve peaks were found in Fe 2p spectrum (Fig. 5(f)) including Fe 2+ 2p 3/2 peak at 710.06 eV, Fe 3+ 2p 3/2 peak at 711.716 eV, Fe 2+ 2p 1/2 peak at 723.79 eV, Fe 3+ 2p 1/2 peak at 725.34 eV, and a satellite peak at 717.4 eV were found and the results indicated that the Fe element in the MFeBC existed in the form of Fe 2+ and Fe 3+ simultaneously. 52 The elemental analysis showed that the magnetic and functional modication of BC were successfully modied by Fe 3 O 4 and thiourea.
3.1.6 Magnetic properties. The magnetic behaviors of FeBC and MFeBC were studied using the vibrating sample magnetometer (VSM) at 25 C. Fig. 6 presented the magnetic hysteresis curves of FeBC and MFeBC under an external magnetic eld ranging from À30 000 to +30 000 Oe. The saturation magnetization values of FeBC and MFeBC were 9.12 and 6.86 emu g À1 , respectively. The leaching of Fe during thiourea modication led to a slight decrease in saturation magnetization. Both materials have good superparamagnetism without coercive force and remanence. 53 Besides, biochar well dispersed in water can be rapidly attracted by ordinary magnets and make the suspensions clear (inset in Fig. 6), which indicated that Fe 3 O 4 has formed a good combination with biochar. This was consistent with the surface topography observed by SEM. These results further conrmed the excellent magnetic properties of the prepared magnetic biochar samples and could be fast separated and reused.

Different impacts
3.2.1 pH. Solution pH can affect ionization degrees, surface charges of biochar, and the speciation of TC. 54 The different initial pH (from 2.0 to 10.0) was adjusted using HCl (0.1 mol L À1 ) or NaOH (0.1 mol L À1 ) and the results were shown in Fig. 7. As the pH increased from 2.0 to 4.0, TC adsorption capacity increased. During 4.0 and 7.0, TC adsorption capacity was basically stable. However, TC capacity adsorption decreased rapidly as the pH further increased from 7.0 to 10.0. TC has three pK a values (3.3, 7.7 and 9.7). Under pH < 3.3, 3.3 < pH < 7.7, 7.7 < pH < 9.7 and pH > 9.7, the species were H 4 TC + , H 3 TC, H 2 TC À and HTC 2À , respectively. 55 Above 7.7, anion form was dominant and biochar surface was typically negatively charged. 56 Electrostatic repulsion led the adsorption capacity reduction. During the pH range of 4.0 to 7.0, neutral ion form (H 3 TC) was dominant and electrostatic interaction may not be the cause of the high TC adsorption. Suggesting that other adsorption mechanisms may be present, such as H-bonding, 57 P-P interaction 58 and pore-lling. 59 Overall, MFeBC had a higher TC adsorption effect in the pH range of 3.0-7.0.
3.2.2 Adsorbent dosage. Adsorbent dosage was a signicant inuence factor. The inuence of MFeBC doses (0.2-2.5 g L À1 ) was studied at 25 C and TC concentration of 50 mg L À1 . As shown in Fig. 8, the TC removal efficiency increased from 20.4% to 64.2% with the adsorbent dosage increased from 0.2 to 2.5 g L À1 . It was suggested that more MFeBC provided more accessible adsorption sites. In addition, the maximum adsorption capacity of 51.1 mg g À1 was obtained at the dosage of 0.2 g L À1 .

Adsorption kinetics
Adsorption rate and adsorption capacity were the key parameters to evaluate the performance of adsorbents. Therefore, studying the adsorption kinetics was very necessary since they indicated reaction rate, providing the information on the factors affecting the reaction rate and revealed adsorption mechanisms. 60 Adsorption kinetic was researched at different temperature (25 C, 35 C, 45 C), under the condition of 0.025 g of MFeBC and 50 mL of TC (50 mg L À1 ). Fig. 9 showed the adsorption kinetics of TC in different temperature. Obviously, the adsorption of TC present two stages. The rst stage (0-30 min) was a rapid adsorption process due to the initial high TC concentration and multiple adsorption sites in biochar. 61 In the second stage (above 30 min), the adsorption capacity increased in a slower rate and nally reached an equilibrium state. At different temperatures, the adsorption kinetics curve has the same trend. From Fig. 9, the maximum adsorption capacity increased as the temperature increased. This indicated that the higher temperature was conducive to the adsorption reaction.
To predict the TC adsorption mechanism by MFeBC, the adsorption process was tested with the pseudo-rst-order (eqn (3)) and pseudo-second-order models (eqn (4)), respectively. Related parameters were listed in Table 1.
where q e and q t (mg g À1 ) correspond to the adsorption capacity at equilibrium and time t, respectively. k 1 (min À1 ) and k 2 (g mg À1 min À1 ) were the rate constants of the pseudo-rst-order and pseudo-second-order adsorption, respectively. As shown in Fig. 9, the pseudo-second-order kinetic model was more consistent with the actual adsorption data. The regression coefficients R 2 of the pseudo-second-order models (0.845, 0.885, 0.854) were higher than that of the pseudo-rst-order models (0.702, 0.752, 0.720). Thus, it can be concluded that chemisorption was dominant in the adsorption process.

Adsorption isotherms
As shown in Fig. 10, the adsorption capacity increased with the increase of the initial TC concentration. To provide a better description of the adsorption mechanism, two typical adsorption models, Langmuir (eqn (5)) and Freundlich (eqn (6)) isotherm models were applied to simulate the adsorption isotherms of TC onto MFeBC, respectively. Related parameters are listed in Table 2.
C e (mg L À1 ) was the equilibrium concentration, q e (mg g À1 ) was the TC adsorption capacity, K L (L mg À1 ) was the Langmuir constant, q m was the maximum adsorption capacity of the isotherm model, K F (L g À1 ) was the Freundlich constant and 1/n was the empirical constant associated with adsorption intensity. 62 Adsorption isotherm is important for describing how the adsorbate molecules are distributed between the liquid and solid phases under an equilibrium state. 63 The Langmuir isotherm assumed the adsorption occurs in the monolayer way with no interaction between the adsorbed molecular. 64 Freundlich isotherm assumed the multilayer and nonideal adsorption on the heterogeneous surface with a non-uniform distribution of adsorption activation energy. 65 Although the two typical isotherm models both t the data well, Freundlich model exhibited a little better than Langmuir model. This may be caused by the introduction of Fe 3 O 4 to the surface of biochar. In addition, the 1/n value (0.3649) dened as heterogeneity factor was less than 1 in Freundlich model. It was suggested that the interaction between adsorption sites and TC was via weak free energies, which was favorable to adsorption. This was consistent with other research. 66 Other modied adsorbents were presented in Table 3. In our study, an efficient adsorbent material was prepared by pyrolysis at 300 C for 1 h, greatly  reducing the energy consumption and the cost of sewage treatment for the practical application of the possibility. Besides, the separation factor (R L ) was always used to determine whether the adsorption was favorable or not. The R L was expressed as follows (eqn (7)): where C 0 was the highest initial TC concentration (mg L À1 ) in this research. The value of R L classied the nature of adsorption to be irreversible (R L ¼ 0), favorable (0 < R L < 1), linear (R L ¼ 1) or unfavorable (R L > 1). 67 In this study, the R L value was 0.0893, indicating that the adsorption was favorable.

Conclusions
An effective thiourea-functionalized magnetic biochar (MFeBC) was preparation via magnetization and functional modication for TC removal. N-S were successfully graed on the surface of biochar. The modied biochar displayed that the maximum TC adsorption capacity of 69.26 mg g À1 . The adsorbents could be fast separated. It was supposed that thiourea-introduced groups (sulfydryl and amidogen) and P-P interaction played a dominant role in TC adsorption process. The experimental results exhibited the adsorption data can be well tted by Freundlich model and pseudo-second-order model. Our study provided a promising adsorbent with high adsorption capacity and good separation performance for TC wastewater treatment.

Conflicts of interest
The authors declare that they have no known competing nancial interests or personal relationships that could have appeared to inuence the work reported in this paper.