Adsorption behavior of tetracycline onto Spirulina sp. (microalgae)-derived biochars produced at different temperatures

Journal Pre-proof Adsorption behavior of tetracycline onto Spirulina sp. (microalgae)-derived biochars produced at different temperatures

Yong-Keun Choi, Tae-Rim Choi, Ranjit Gurav, Shashi Kant Bhatia, Ye-Lim Park, Hyung Joo Kim, Eunsung Kan, Yung-Hun Yang PII:

S0048-9697(19)36278-3

DOI:

https://doi.org/10.1016/j.scitotenv.2019.136282

Reference:

STOTEN 136282

To appear in:

Science of the Total Environment

Received date:

28 October 2019

Revised date:

10 December 2019

Accepted date:

20 December 2019

Please cite this article as: Y.-K. Choi, T.-R. Choi, R. Gurav, et al., Adsorption behavior of tetracycline onto Spirulina sp. (microalgae)-derived biochars produced at different temperatures, Science of the Total Environment (2019), https://doi.org/10.1016/ j.scitotenv.2019.136282

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© 2019 Published by Elsevier.

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Adsorption behavior of tetracycline onto Spirulina sp. (microalgae)-derived biochars produced at different temperatures

Yong-Keun Choia, b, c, Tae-Rim Choia, Ranjit Gurava, Shashi Kant Bhatiaa, Ye-Lim Parka, Hyung Joo Kima, Eunsung Kanc, Yung-Hun Yang a, *

Department of Biological Engineering, Konkuk University, Seoul 05029, Republic of Korea

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The Academy of Applied Science and Technology, Konkuk University, Seoul 05029, Republic of

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a

Korea

Department of Biological and Agricultural Engineering & Texas A&M AgriLife Research Center,

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Texas A&M University, 1229 North US Highway 281, Stephenville, TX 76401, USA

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Dr. Yung-Hun Yang

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*Corresponding author

Department of Biological Engineering, Konkuk University Seoul 05029, Republic of Korea E-mail: [email protected]

Telephone: 82-02-450-3936 Fax: 82-02-3437-8360

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Abstract We evaluated the production of Spirulina sp. (microalgae)-derived biochars (SPAL-BCs) at different pyrolysis temperatures for the removal of an emerging water contaminant, tetracycline (TC). Physicochemical properties of SPAL-BCs were characterized and related with their capacity to adsorb TC. Increasing pyrolysis temperatures led to higher aromaticity, higher hydrophobicity, and higher specific surface area. In particular, SPAL-BC750 possessed

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the highest hydrophobicity, various strong crystallizations (i.e., calcite, hydroxyapatite, and

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rhenanite) and functional groups (i.e., CH2, C-N, C-O, and CO32-), which may be associated with high TC adsorption. SPAL-BC750 also presented the highest TC adsorption capacity

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(132.8 mg TC/g biochar) via batch experimentation because of hydrophobic, π-π interactions,

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functional groups, and metal complexation. The best fitting isotherm and kinetic models of

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TC adsorption by SPAL-BC750 were the Langmuir and pseudo-first order models, respectively. SPAL-BCs obtained as a by-product of pyrolysis may be an economical and

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potentially valuable adsorbent for aqueous antibiotic removal.

Keywords: Biochar, pyrolysis, Spirulina sp., tetracycline, hydrophobic interaction

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Introduction Microalgae are aqueous photosynthetic organisms that have attracted attention because

of their valuable potential in the development of pharmaceuticals and cosmetics, the production of biodiesels, and the bioremediation of heavy metals, nitrogen, and phosphates in wastewater (Choi et al., 2018a; Choi et al., 2017; Santos & Pires, 2018; Yu et al., 2017). Numerous researches have primarily focused on the development of microalgae cultivation

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technologies, the use of media, and extraction methods (Choi et al., 2018a; Choi et al., 2017;

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Jeon et al., 2013) to achieve high biodiesel production. However, not many researches have

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focused on the use of algal biomass with low lipid content or the use of residual biomass after

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lipid extraction. Although various recovery methods may be used, such as solvent or ionic liquid extraction, these methods are still burdened with high costs, low recovery rates and

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production yield, secondary pollution, and potential human health threats due to the use of

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various organic solvents (Jeon et al., 2013; Kim et al., 2012). Gasification and pyrolysis are alternative methods for biofuel production given that bio-gas, bio-oil, and biochar (BC) are

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produced simultaneously by these methods (Fahmy et al., 2018; Wang, 2014; Zhou et al., 2017). Moreover, as algal biomass can be used regardless of its lipid content, the use of algal biomass itself is important to expand upon its potential applications, such as for agricultural or bioremediation purposes (e.g., environmental adsorbents or agricultural soil amendments; (Vijayaraghavan & Ashokkumar, 2019; Zheng et al., 2017). Antibiotics, heavy metals, dyes, and other organic contaminants exist in potable and recreational water sources, and various problems and potential threats for human health have arisen owing to the presence of these substances (Cetecioglu et al., 2014; Crini & Lichtfouse, 2018; Fiyadh et al., 2019; Oladipo et al., 2018; Palansooriya et al., 2019). 3

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In particular, the presence of drug-resistant pathogens and genes, the presence of cyanobacteria by eutrophication, contamination of groundwater by run-off, and destruction of food webs have been reported to be associated with these substances (i.e., antibiotics, heavy metals, dyes, and other organic contaminants) (Cetecioglu et al., 2014; Choi et al., 2018b; Xiong et al., 2019; Zheng et al., 2017). Of these aforementioned problems, the accumulation of antibiotics in various water sources is particularly concerning.

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The abuse of various antibiotics (e.g., tetracyclines, macrolides, β-lactams, and

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sulfonamides) in hospital settings, in the production of livestock, and in agricultural industries is significantly increasing; however, antibiotics remain difficult to remove from contaminated

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water sources (Cetecioglu et al., 2014; Xiong et al., 2019; Gurav et al., 2019). Various

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methodologies (e.g., adsorption by activated carbon, electrolysis, membrane separation,

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photocatalysis, coagulation, and biological degradation) have been employed for antibiotic removal (Dzomba et al., 2015; Lu et al., 2017; Peiris et al., 2017; Yang et al., 2016; Ye et al.,

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2019; Ye et al., 2017a; Ye et al., 2017b). However, these methodologies have various

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limitations, such as the high cost of materials, high energy consumption, and secondary pollution by additional use of chemicals for production of materials, complicated removal processes for antibiotic removal, and the development of economical methods that address these issues are needed (Daghrir & Drogui, 2013). Biochar as an eco-friendly and cost-effective adsorbent that can be employed for the removal of antibiotics from water sources. Currently, a few types of microalgae-derived biochar have been employed for the removal of organic contaminants including PNP (Zheng et al., 2017), heavy metals such as Co (II) (Bordoloi et al., 2017), tetracycline (Peng et al., 2014), and dyes such as Congo red (Nautiyal et al., 2016) (Table 1). According to previous studies, microalgae-derived biochar may be a viable material due to microalgae possess high 4

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nutrients (e.g., nitrogen and phosphorus), protein, carbohydrates, and lipids (Peng et al., 2014; Wang, 2014; Zheng et al., 2017). Microalgae intended for use as feedstock for biochar production can also be harvested from lakes with algal blooms or cultured using wastewater intended for N and P removal (e.g., dairy effluents; (Wang et al., 2018b). As previously mentioned, microalgae-derived biochar by-products may be harvested from gasification or pyrolysis processes that use microalgae with low lipid content or from microalgal residues

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that would have usually been deemed worthless materials and discarded after their lipids had

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been extracted. Therefore, microalgae-derived biochar may be an economical adsorbent for the antibiotic removal from water sources. To the best of our knowledge, there have been no

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pyrolysis at different temperature.

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studies related to TC adsorption using Spirulina sp. microalgae-derived biochar produced by

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The present study focuses on the adsorption of the target antibiotic TC from wastewater using microalgae-derived biochar. To the best of our knowledge, Spirulina sp.-

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derived biochar produced by pyrolysis has rarely been used to study TC adsorption. Thus, the

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objectives of the present study were to (1) investigate the physical and chemical characteristics of the Spirulina sp.-derived biochar (SPAL-BC), (2) evaluate the correlation between physiochemical characteristics and the TC adsorption capacity of SPAL-BCs, and (3) determine the mechanism for TC adsorption based on the results of isotherm and kinetic models. 2 2.1

Materials and Methods Adsorbate and SPAL-BC production Tetracycline (C22H23N2O8) that was purchased from Sigma-Aldrich (USA) was used as

the adsorbate. TC solutions were prepared for the adsorption experiments with purified grade 5

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water (i.e., HPLC water). Spirulina sp. powder was used for the production of biochar and was purchased from Naturalmom (Seoul, Republic of Korea). The Spirulina sp. powder used as the feedstock was dried overnight at 80 °C to remove moisture before pyrolysis. The Spirulina sp. powder was pyrolyzed at peak temperatures of either 350, 550, or 750 °C for 2 h under nitrogen flow in a furnace (OTF-1200X, MTI Co., Richmond, CA). The SPAL-BCs produced at the different

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pyrolysis temperatures were added to distilled water (DI) for cooling and washing. The SPAL-

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BCs were washed several times to eliminate surface ash and impurities, and named according to their formation temperature (i.e., SPAL-BC350, SPAL-BC550, and SPAL-BC750). The

SPAL-BC characterization

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2.2

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SPAL-BCs were then crushed and filtered through 140 µm mesh.

The lignocellulosic properties of the Spirulina sp. cells as a feedstock were evaluated

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via thermogravimetric analysis (TGA, 209 F3, Netzsch, Germany). The lignin, cellulose, and hemicellulose content of the Spirulina sp. cells was estimated based on previous research (Lee

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et al., 2009). The content of extractives was calculated by the differences in the total amount of lignin, cellulose, and hemicellulose. An elemental analyzer (FLASH EA 1112, Thermo Scientific, Waltham, MA) was used to estimate the content of N, O, C, and H. The pH at the point of zero charge (pHpzc) and the content of ash, fixed carbon (FC), and volatile carbon (VC) were analyzed following previously described methods (Choi & Kan, 2019). The surface morphologies of SPAL-BCs were analyzed using a scanning electron microscope (SEM, TM4000 Plus, Hitachi Co., Tokyo, Japan) and the specific surface area (SSA) of the SPAL-BCs was evaluated based on the Brunauer-Emmett-Teller (BET) method (TriStarⅡ, Micromeritics, USA). The crystallographic structures of the SPAL-BCs from 2° to 6

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80° were evaluated using X-ray diffraction (XRD, Rigaku SmartLab, Rigaku Co., Tokyo, Japan). Fourier transform infrared spectroscopy (FTIR) using an FT/IR-4600 spectrometer (Jasco, Japan) was used to observe the functional groups on the surface of the SPAL-BCs from 400 to 4000 cm-1. X-ray photoelectron spectroscopy (XPS, K-Alpha, Thermo Scientific, U.S.) was used to observe the surface composition of the SPAL-BC750 before and after TC adsorption. The Ca, Mg, Fe, N, P, and K content of the Spirulina sp. feedstock and the SPAL-

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BCs was measured by inductively coupled plasma optical emission spectroscopy (ICP-OES,

TC adsorption experiments with SPAL-BCs

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2.3

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iCAP7400 DUO, Thermo Fisher Scientific, Waltham, MA).

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A TC stock solution with a concentration of 100 mg/L (pH 6) was prepared by

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dissolving TC in distilled water. TC adsorption capacities of SPAL350-BC, SPAL550-BC, and SPAL750-BC were measured by shaking 0.05 L of the TC solution (100 mg/L) containing

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0.005 g of the SPAL-BCs at 20 °C for 5 d. The same procedures were followed for the kinetic adsorption experiments with time intervals. The TC adsorption kinetic models (i.e., elovich,

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pseudo-first order, pseudo-second order, two-compartment, liquid film diffusion, and intraparticle diffusion model) were used to interpret the data as shown in the supporting information. The pH of the TC solution (pH 3-9) was adjusted using 0.1 M NaOH or HCl to evaluate the effects of the solution pH on TC adsorption. For the isotherm adsorption experiments, the initial concentration of the TC solution was diluted from the stock solution and ranged from 10 to 100 mg/L. The isotherm experiments were carried out at 20 °C by shaking (200 rpm) for 5 d. At the end of the adsorption reaction, the TC solutions were centrifuged at 1000хg and filtered through a 0.45 µm membrane syringe filter. The TC adsorption isotherm models (i.e., Temkin, Langmuir, and Freundlich) were used to interpret 7

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the data as shown in the supporting information. Additionally, the influence of the reaction temperature on TC adsorption was evaluated at 20, 30, and 40 oC. This experiment was conducted under the same conditions as the aforementioned batch experiment. 2.4

Desorption and regeneration of SPAL-BC750

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Desorption efficiency of TC onto SPAL-BC750 and regeneration of SPAL-BC750 were performed to evaluate reuse ability. First, the TC (0.05 L, 100 mg/L) adsorption onto

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0.005g of SPAL-BC750 was carried out for 24h and then, the adsorbed TC on SPAL-BC750

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was desorbed by 0.1 N NaOH at 20 oC for 24h (Choi & Kan, 2019; Peng et al., 2014; Song et

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al., 2019). For the analysis of regeneration, the adsorption and desorption were conducted 4

Data analysis

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2.5

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cycles. The collected liquid samples were measured using HPLC as described in section 2.5.

The concentration of TC was analyzed before and after the adsorption experiments

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using an HPLC (Shimadzu LC-2030C, Shimadzu Co., Kyoto, Japan) system equipped with a photo-diode array (PDA) detector at a wavelength of 355 nm. An Aeris Peptide 3.6 µm XBC18 column (Phenomenex Inc., Torrance, CA) was employed, and the TC was eluted at a flow rate of 0.6 mL/min with a mixture of 67% pure water containing 0.1% formic acid and 33% methanol as the mobile phase under isocratic runs (Choi & Kan, 2019). 2.6

Statistical analysis The data acquired in the present study were analyzed by Minitab 16 Statistical

Software (Minitab Inc, State College, PA). The relationship between the pyrolysis temperature (350, 550, and 750 °C) and the physicochemical properties (i.e., element content, 8

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O/C, H/C, (N+O)/C, mineral content, and surface area) of the SPAL-BCs was evaluated by Pearson correlation analysis. Pearson correlation analysis was also used to evaluate the relationship between the physicochemical properties of the SPAL-BCs and the TC adsorption capacity of the SPAL-BCs. Statistical significance was set as p < 0.001, 0.01, or 0.05. 3

SPAL-BC physicochemical characteristics

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3.1

Results and Discussion

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Thermogravimetric curve as shown in (Fig. 1a) shows that the weight of the Spirulina

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sp. feedstock decreased as the temperature of the Thermogravimetric analysis (TGA) increased. A weight loss of 10% was detected from 0 to 200 °C, which corresponded to the

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loss of moisture in the form of vapor and the decomposition of the majority of the

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hemicellulose as well as some cellulose. A dramatic weight loss of 50% was observed near 220 °C, implying that some cellulose, lignin, and extracts were decomposed between 200 to

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400 °C. Above 400 °C, microalgae weight continued to decrease owing to the decomposition

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of most of the cellulose, some lignin, and some extracts. At the end of the TGA, only 15% of the initial weight remained. Microalgae were composed of 2.02% hemicellulose, 7.65% cellulose, 14.30% lignin, and 76.02% extracts. According to these results, most hemicellulose, most cellulose, and some extracts were decomposed as temperature increased. In contrast, the minerals (i.e., N, P, K, and Ca) in the SPAL-BCs were condensed at higher temperatures as is summarized in Table 2. The physiochemical characteristics of the Spirulina sp. feedstock and the SPAL-BCs are displayed in Table 3. The C (44.70%), H (7.09%), and O (31.54%) content of the Spirulina sp. feedstock differed from that of the SPAL-BCs, which possessed higher C (61.6366.60%), lower H (6.62-1.30%), and lower O (18.71-12.25%) content. In particular, the 9

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content of H and O of the SPAL-BCs decreased with decreasing pyrolytic temperature. The lower content of H and O of SPAL-BC750 compared to that of the other SPAL-BCs resulted in the lowest O/C and H/C, indicating high hydrophobicity and aromaticity (Ahmad et al., 2012; Choi & Kan, 2019). In contrast, the ash content of the SPAL-BCs increased with increasing pyrolytic temperature due to the condensing of various minerals (e.g., N, P, K, and Ca). The lower specific surface area (0.31-2.63 m2/g) of the SPAL-BCs appeared compared to

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that of other studies (2.12-167 m2/g; (Nautiyal et al., 2016; Zheng et al., 2017). Nevertheless,

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the specific surface area of the SPAL-BCs slightly increased with the increase of pyrolytic temperature. As shown in Table 3, the slightly higher pHpzc values of the SPAL-BCs

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appeared at higher temperatures owing to the condensation of alkaline minerals. These results

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(i.e., lower O/C and H/C ratios, higher specific surface area, and higher pHpzc values at

Sadaka et al., 2014).

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higher temperatures) are similar to those of biochar from previous studies (Choi & Kan, 2019;

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The surface morphology of the Spirulina sp. feedstock and the SPAL-BCs is shown in

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Fig. 1b. It can be observed that the SPAL-BCs possessed developed structures, while the surface of the Spirulina sp. feedstock was smooth. In particular, SPAL-BC750 had a more developed pore structure compared to the other SPAL-BCs (Fig. 1b). XRD and FTIR analyses were conducted to identify the effect of pyrolytic temperature on the metal composition and functional groups on the surface of the SPAL-BCs as shown in the Fig. 2 and Fig. 3. SiO2, CaCO3, Ca3(PO4)2, and CaNaPO4 were detected on the surface of the SPAL-BCs. In particular, peaks at 26.4, 29.5, 31.3, and 41.6° in the SPAL-BC750 XRD patterns were assigned to SiO2, CaCO3, Ca3(PO4)2, and CaNaPO4, respectively (Choi & Kan, 2019; Orlov et al., 2019; Prezas et al., 2017). In contrast, SPAL-BC350 did not possess any peaks whereas SPAL-BC550 possessed weak peaks.

XRD patterns revealed the abundant calcium on the surface of 10

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SPAL-BC750. It is known that complexation between the cations (e.g., Ca2+ and Mg2+) and TC as reported by Anton-Herrero et al. and Owings (Antón-Herrero et al., 2018; Owings, 1973). Thus, Ca on the surface of SPAL-BC750 may be associated with TC adsorption. Moreover, according to XPS results, the loss of Ca in SPAL-BC750 after TC adsorption demonstrated that metal complexation would favorably make. These results suggest that strong CaCO3, Ca3(PO4)2, and CaNaPO4 may influence TC adsorption in biochar (Li et al.,

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2017) (Fig. 2).

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The FTIR spectrums of the Spirulina sp. feedstock and the SPAL-BCs showed broad bands (Fig. 3a and b). As presented in Fig. 3a and b, the strong spectrum of the Spirulina sp.

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feedstock decreased with the formation of biochar. These results suggest that most functional

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groups with an -OH band (3200-3400 cm-1), CH2 and CH3 stretching (2930 cm-1), aromatic

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conjugated C=O and C=C bonds (1640 cm-1), N-H bending and C-N stretching (1520 cm-1), C-H bending (1430 cm-1), C=O carboxylate ion stretching (1375 cm-1), C-OH phenolics (1270

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cm-1), C-O single bonds (1150 cm-1), C-O stretching (1049 cm-1), and CO32-, (875 cm-1)

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vanished with the increase of pyrolysis temperature, as has been reported in previous literatures (Domingues et al., 2017; Islam et al., 2016; Zhang et al., 2014). The SPAL-BC750 spectrum after TC adsorption was present in Fig. 3b. The peaks of CH stretching in CH2 and CH3, N-H bending and C-N stretching, C-O stretching, and CO32- decreased, whereas C-H bending (1430 cm-1), C=O carboxylate ion stretching (1375 cm-1), aromatic stretching (1236 cm-1), C-O stretching (1061 cm-1), and C-H (826 cm-1) of the TC compound were observed. These results indicate that lower peaks were associated with TC adsorption and that TC was successfully incorporated onto the surface of SPAL-BC750. To further estimate the composition of biochars before and after adsorption reaction, XPS was used in this study. There was the presence of C1s, O1s, N1s, Ca2p, Na, and P by survey scan of SPAL-BC750 11

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(Fig. 4) (Zeng et al., 2019). Like XRD results, it can be confirmed that CaCO3, Ca3(PO4)2, and CaNaPO4 in SPAL-BC750 are mainly present. Additionally, the peaks including C1s, N1s, Ca2p, Na, and P were slightly decreased after the reaction (Fig. 4a). As shown in Fig. 4b, c, and d, the decrease of π-π, C-N, and CaCO3 appeared owing to π-π interaction and metal complexation and the increase of NH2 could be associated with NH2 of TC compound after the reaction (Lai et al., 2019; Tang et al., 2018). These results demonstrated that C1s, N1s,

TC adsorption capacity and the effects of pH and temperature

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Ca2p, Na, and P as active sites influenced on TC adsorption.

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TC adsorption capacity of the SPAL-BCs is described in Fig. 5a. The TC adsorption

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capacity of the SPAL-BCs ranged from 14.9 mg TC/g BC to 132.8 mg TC/g BC. Among the

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SPAL-BCs, the highest TC adsorption capacity (132.8 mg TC/g BC) was observed in SPALBC750. These results imply that the pyrolysis temperature influenced the capacity of the

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biochar to adsorb TC. Additionally, as the reaction temperature for adsorption increased from 20 to 40 °C, the capacity for TC adsorption increased from 132 to 522 mg TC/g BC (Fig. 5b).

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This result suggests that higher temperatures were favorable and enhanced the adsorption of TC by SPAL-BC750. This phenomenon could be attributed to an endothermic process. As seen in Fig. 5c, the pH of the aqueous solution (pH 3-9) influenced the TC adsorption of SPAL-BC750 owing to the physiochemical characteristics of SPAL-BC750 and the ionization process of the TC molecule based on the pKa of TC. The capacity of TC adsorption increased as the solution pH increased from pH 3 to pH 9 (98 to 278 mg TC/g BC, respectively). Lower pH (pH 3 and 4) appeared to have an inhibitory effect on TC adsorption in SPAL-BC750, while a different effect was observed at higher pH (pH 8 and 9). TC adsorption onto SPAL-BC750 was found to be pH-dependent and alkali condition was 12

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favorable between TC and SPAL-750. At low pH (< 3.3), the surface of SPAL-BC750 (pHpzc = 8.3) was positively charged, and TC dominated the positive charge (H 3TC+). This result suggests that electrostatic repulsion was present between SPAL-BC750 and TC. SPAL-BC750 was positively charged, whereas TC (H3TC0) was non-charged between pH 3.3 and pH 7.7. As mentioned in section 3.1, there were the decrease of π-π and C-N, indicating TC adsorption onto SPAL-BC750 at solution pH 6. This result implies that hydrophobic

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interactions, π-π interactions, and functional groups mainly favor TC adsorption. Moreover,

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the TC adsorption capacity of SPAL-BC750 increased with the increase of the solution pH (pH 3.3 to 7.7). In particular, the increase in the TC adsorption capacity of SPAL-BC750 was

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appeared to be similar to the trend associated with the increase in TC (H3TC-). Although the

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main mechanism was not an electrostatic interaction or repulsion at these pH values,

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electrostatic interactions may occur as a separate sub-mechanism. The positive charge of SPAL-BC750 and the negative charge of TC at pH values between 7.7 and 8.3 allowed for

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electrostatic interactions that resulted in a higher TC adsorption capacity (276 mg TC/g BC).

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Despite the higher TC adsorption capacity at pH 9, both SPAL-BC750 and TC were negatively charged, suggesting that electrostatic repulsion was present. Although this phenomenon was not obvious, electrostatic interactions owing to a change in pH by SPALBC750 (pHpzc = 8.3) and the dominant forms of negatively charged TC (H3TC- and H3TC2-) may have been present. 3.3

Statistical evaluation Pearson correlations between the independent (i.e., elemental content, mineral content,

and surface area) and dependent variables (i.e., pyrolysis temperature and adsorption capacity) were analyzed using Minitab software and the results are summarized in Table 4. A negative 13

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relationship between the pyrolysis temperature and most minerals (i.e., Ca, Mg, N, P, K, and Fe) was found. In contrast, the pyrolysis temperature was positively related with TC adsorption capacity (Qe), ash content, surface area, and the H/C. As mentioned in section 3.1, TC adsorption capacity (Qe) revealed a positive relationship with pyrolytic temperature because SPAL-BCs possessed higher C, lower H, lower O, higher ash content, and higher surface area with increasing pyrolytic temperature. These results may imply that various

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functional groups of SPAL-BC350 and SPAL-BC550 produced at low temperature were

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mainly associated with TC adsorption, whereas higher hydrophobicity, higher aromaticity and higher surface area of SPAL-BC750 related with TC adsorption. Particularly, the H/C ratio

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was observed to have a stronger relationship (r = -1.000, p-value: 0.019) with pyrolytic

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temperature. The findings of the present study imply that the H/C ratio, which indicates

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higher hydrophobicity and strong aromaticity, significantly decreased with increasing pyrolysis temperature. Moreover, surface area as well as the H/C ratio except the ash content

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was correlated with the adsorption capacity (Table 4). The TC adsorption capacity presented a

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positive relationship (p-value < 0.05) with increasing surface area and a decreasing H/C ratio. These results imply that increased TC adsorption is likely due to higher pyrolysis temperatures, higher surface areas, and lower H/C ratios. 3.4

Adsorption isotherms for TC onto SPAL-BC750 The adsorption isotherms were used to investigate the relationship between SPAL-

BC750 and TC at equilibrium via Temkin, Langmuir, and Freundlich models. The three isotherm models for TC adsorption in SPAL-BC750 are described in Fig. 6. When compared to Freundlich and Temkin modes, the Langmuir model presented a higher correlation coefficient (R2 = 0.961). Based on these results, the Langmuir model indicated that monolayer 14

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homogeneous adsorption was the best-fit model, which was similar to the results reported by Peng et al. (2014) and Zhou et al. (2017). In contrast, many previous studies have report that the Freundlich model was successfully fitted to TC adsorption data from biochar produced from rice straw-BCs , swine manure-BCs , and sewage sludge-BCs (Wang et al., 2018a; Yang et al., 2016). Moreover, the maximum TC adsorption capacity of SPAL-BC750 was 147.9 mg TC/g BC, which was much higher than that of rice straw-BC and swine manure-BC (8.1-14.2

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mg TC/g BC; (Wang et al., 2018a); holm oak-BC and an oak, eucalyptus and pine mixture-BC

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(11.9-15.2 mg TC/g BC; (Antón-Herrero et al., 2018); and a sewage sludge-BC (15.2 mg TC/g BC; (Yang et al., 2016) (Table 5). According to various studies, the TC adsorption

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capacity (87.8-816.7 mg TC/g BC) of activated biochar and carbons treated with H3PO4,

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NaOH, ferric activation and iron-coating, zinc-coating, Fe3O4-coating, and g-MoS2-decorating

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may be notably higher because of the higher associated surface areas (126-1515 m2 /g); (Chen et al., 2018; Jang et al., 2018; Oladipo & Ifebajo, 2018; Torres-Pérez et al., 2012; Yang et al.,

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2016; Zeng et al., 2019; Zhou et al., 2017) (Table 5). Therefore, these results imply that

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SPAL-BC750 possessed considerable TC adsorption ability that surpassed that of other activated biochars. Additionally, Fig. 7 shows correlation analysis results between specific surface areas and the TC adsorption capacity from the results of various studies. Overall, a lower correlation (e.g., R2 = 0.528) was revealed between specific surface areas and the TC adsorption capacity. The results indicate that the TC adsorption of the biochar or activated carbon may be influenced by various mechanisms, including electrostatic interactions, high surface areas, the presence of functional groups, hydrophobicity, π-π interactions, and metal precipitation as has been previously present (Peng et al., 2014; Wang et al., 2018a; Zhou et al., 2017). Although SPAL-BC750 had the lowest surface area compared with other biochar and activated carbon from previous literatures (Table 5), the TC adsorption of SPAL-BC750 was 15

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most likely induced by hydrophobic properties and the presence of various functional groups. Thus, SPAL-BC750 is a noteworthy and potential adsorbent for the TC removal, an emerging contaminant, given that SPAL-BC750 may be produced from microalgal biomass harvested from lakes or cultured from wastewater. Without any functionalization or activation, SPALBC750 possessed a higher adsorption capacity of TC compared to that of the other biochars that were produced under similar pyrolysis conditions. These properties indicate that

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microalgae-derived biochars possess multiple advantages, such as reduced production costs

Adsorption kinetics for TC onto SPAL-BC750

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3.5

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and the potential for use in environmental management (Wang & Wang, 2019).

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Kinetic models were applied to evaluate the mechanism and rate-limiting step of TC

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adsorption. As shown in Fig. 8a, TC adsorption was rapid during the first 4 h and then reached equilibrium. This result suggests that TC progressively saturated and occupied active sites on

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the surface of SPAL-BC750. With regard to the evaluated kinetic models, high R2 values (> 0.97) were observed in the pseudo first order, two compartment, and liquid film diffusion

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models (Fig. 8a, 8b, 8c, and 8d). In particular, the pseudo first order model resulted in an R2 value of 0.978, indicating that physical sorption was well modeled in this study. This result suggests the presence of hydrophobic interactions as physical sorption was mainly present between TC and SPAL-BC750. Additionally, high R2 values of 0.978 and 0.976 were observed with the two compartment and liquid film diffusion models, respectively. These results indicate that a two-domain process and TC adsorption from liquid solutions occurred (Fig. 8b and 8d; (Li et al., 2009; Tan et al., 2016). 3.6

Desorption and regeneration of SPAL-BC750

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As for desorption experiment, SPAL-BC750 was desorbed by 0.1N NaOH solution in this study owing to an importance of reusability of adsorbent (Peng et al., 2014). The results in Fig 9a showed that SPAL-BC750 has high desorption efficiency (over 60%) for TC, although desorption efficiency (over 93% and 89%) reported by Peng et. al. and Song et. al. was higher (Peng et al., 2014; Song et al., 2019). The high desorption of SPAL-BC750 could be related to weak correlation with TC adsorption during alkaline desorption. Moreover, TC

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desorption of SPAL-BC750 reached equilibrium within 360 min and TC adsorption and

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desorption of SPAL-BC750 was interestingly rapid. Additionally, multiple cycles process of adsorption-desorption regeneration of SPAL-BC750 was performed. TC desorption rate in

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three cycles could reach 61%, 65%, and 60%, respectively. However, the desorption rate was

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about 40% lower (37%) in the fourth run of regeneration of SPAL-BC750. These results

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might be ascribed various reasons including loss or block of active sites (Li et al., 2019). Eventually, the regeneration effect of SPAL-BC750 was proved that it had the prospect of

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reuse in the environmental field.

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Further works are needed to evaluate TC adsorption onto SPAL-BC750 for real wastewater and effective regeneration methods (e.g., chemical, thermal, and microwave) of contaminant-saturated SPAL-BC750. In addition, further and more detailed thermodynamic modeling of TC adsorption by SPAL-BCs in aqueous solutions is required. 4

Conclusion The increase in pyrolysis temperature led to lower H/C and O/C ratios, higher

specific surface area, and higher pHpzc values. In particular, SPAL-BC750 possessed the highest hydrophobicity as well as strong calcite (CaCO3,), hydroxyapatite (Ca3(PO4)2), and rhenanite (CaNaPO4) crystallizations and functional groups (CH2, C-N, C-O, and CO32-), 17

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which may be associated with TC adsorption. SPAL-BC750 showed the highest TC adsorption capacity (132.8 mg TC/g BC) in the batch experiments owing to hydrophobic and electrostatic interactions, functional groups, and metal complexation. The best fitting TC adsorption isotherm and kinetic models for SPAL-BC750 were the Langmuir and pseudo-first order models, respectively. Acknowledgement

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This research was supported by Basic Science Research Program through the National

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Research Foundation of Korea (NRF) funded by the Ministry of Education (NRF2019R1I1A1A01054638 and NRF-2019M3E6A1103979). This study was carried out with the

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support of ―R&D Program for Forest Science Technology (Project No. 2019157B10-1921-

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0101) provided by Korea Forest Service (Korea Forestry Promotion Institute).

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References

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Declaration of interests

☒ The authors declare that they have no known competing financial interests or personal

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relationships that could have appeared to influence the work reported in this paper.

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Figure legends: Fig. 1. Thermogravimetric curve (A) of Spirulina sp. (microalgae) feedstock under N2 supply and SEM images (B) of Spirulina sp. (microalgae) feedstock, SPAL-BC350, SPAL-BC550, and SPAL-BC750. Fig. 2. XRD patterns of SPAL-BCs (●: SiO2, ▲: CaCO3, ■: CaKPO4, ♦: CaNaPO4).

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Fig. 3. FT-IR spectrum of (A) SPAL-BCs and (B) SPAL-BC750 before and after TC adsorption (CO32-, (875 cm-1), C-O stretching (1049 cm-1), C-O single bond (1150 cm-1), C-OH phenolic (1270 cm-1), C=O stretch of carboxylate ions (1375 cm-1), C-H bending (1430 cm-1), N-H bending and C-N stretching (1520 cm-1), aromatic conjugated C=O, C=C (1640 cm-1), CH stretching of CH2 and CH3 (2930 cm-1), -OH (3200-3400 cm-1)).

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Fig. 4. XPS spectrum of survey (A), C1s (B), Ca2p (C), and N1s (D) of SPAL-BC750 before and after TC adsorption.

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Fig. 5. Adsorption capacity (A) of SPAL-BCs for TC under batch experiment, effect of reaction temperature (B) on TC adsorption onto SPAL-BC750, and pH-dependent TC species and effects of solution pH (C) on the adsorption of TC onto SPAL-BC750. Conditions: 50 mL, 100 mg/L TC, 0.005 g BC, pH = 6, 20 °C, 5 d.

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Fig. 6. Adsorption isotherms of TC onto SPAL-BC750 by Langmuir, Freundlich, and Temkin isotherm models. Conditions: 50 mL, 10-100 mg/L TC, 0.005g BC, pH = 6, 20 °C, 5 d.

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Fig. 7. Correlation between specific surface area of BCs (biochars) and activated carbon and TC adsorption capacity (Qmax).

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Fig. 8. The adsorption kinetics of TC onto SPAL-BC750 by fitting (A) pseudo-first order, pseudo-second order, and elovich model, (B) two compartment model, (C) intraparticle diffusion model, and (D) liquid film diffusion model. Conditions: 50 mL, 100 mg/L TC, 0.005 g BC, pH = 6, 20 oC, 1 d. Fig. 9. Desorption efficiency of TC onto SPAL-BC750 and regeneration of SPALBC750.

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Fig. 1.

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Fig. 2.

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Fig. 3.

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Fig. 4.

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Fig. 5.

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160 140

100

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80

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60

Freundlich (Kf= 56.88, nf= 4.682, R2= 0.891)

40

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Langmuir (KL= 0.181, Qm=147.9, R2= 0.961)

20

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Temkin (bT= 113.5, KT= 4.385, R2= 0.935) 20

40

60

80

100

Ce (mg/L)

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Fig. 6.

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Qe (mg/g)

120

33

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Fig. 8.

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Fig. 9.

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Table 1. Contaminants adsorption using various microalgae-derived biochars as adsorbent Microalgae

Contaminants

Pyrolysis conditions

Chlorella sp.

p-nitrophenols

600oC, 0.5h

Specific surface area (m 6.163

Chlamydomonas sp.

2.122

Coelastrum sp.

15.032 Co (II)

500oC, -

-

Spirulina platensis

Congo red

450oC, 2h

167

Blue-green microalgae

Tetracycline

Spirulina sp.

Tetracycline

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Scenedesmus dimorphus

-

350oC, 2h,

0.31

550oC, 2h

1.55

750oC, 2h

2.63

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Hydrothermal process

Table 2. Mineral compositions of various sources Mineral composition (%)

rious sources N

P

K

Ca

Mg

F

pirulina sp.

10.10

1.38

1.18

0.15

0.32

0.0

PAL-BC350

11.77

1.24

0.78

0.29

0.26

0.0

PAL-BC550

11.09

1.29

1.45

0.39

0.25

0.1

PAL-BC750

9.42

1.64

1.72

0.58

0.22

0.0

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Table 3. Physiochemical characteristics of Spirulina sp. (feedstock), SPAL-BC350, SPAL-BC550 and SPAL-BC750 Ultimate analysis (%)

C

SPAL-BC350 SPAL-BC550 SPAL-BC750

O/C

H/C

(N+O)/C

(mol/mol)

(mol/mol)

(mol/mol)

H

O

N

7.09

31.54

10.10

0.529

1.903

61.63

6.62

18.71

11.77

0.228

65.43

3.73

14.22

11.09

66.60

1.30

12.25

9.42

44.70

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Spirulina sp.

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Materials

Proximate an

VC

FC

0.723

85.16

8.2

1.289

0.391

56.47

42.2

0.163

0.684

0.308

29.55

64.9

0.138

0.138

0.259

19.59

69.9

SSA: Specific surface area pHpzc: pH at point of zero charge

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Table 4. Pearson correlation analysis (coefficients (r) and significance level) between pyrolysis temperature and physicochemical properties, and between physicochemical properties and adsorption capacity (Qe) of TC Factors

Temperature (°C) r

Significance level

p value

r

Signi

0.998

*

0.043

-

Ash (%)

0.999

*

0.026

0.994

Volatile Carbon (%)

-0.967

NS

0.165

-0.982

Fixed Carbon (%)

0.939

NS

0.224

0.960

Surface area (m2/g)

0.999

*

0.025

1.000

O/C (mol/mol)

-0.969

NS

0.160

-0.983

H/C (mol/mol)

-1.000

*

0.019

-0.999

N (%)

-0.972

NS

0.152

-0.953

P (%)

0.975

NS

0.144

0.957

K (%)

0.970

NS

0.156

0.984

Ca (%)

0.986

NS

0.107

0.972

Mg (%)

-0.922

NS

0.254

-0.893

NS

0.904

-0.082

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TC Qe (mg/g)

Fe (%)

-0.150

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*, **, and *** are significance level of <0.05, <0.01 and <0.001; NS= not significant.

Table 5. Comparison of various biochars for TC removal Carbonaceous materials

Desorption efficiency (%)

Reaction time (h)

Kinetic model

Rice straw biochar

NA

24

pseudo second order

Swine manure biochar

NA

36

pseudo second order

Isotherm model Langmuir and Freundlich Langmuir and Freundlich

Tetracycline concentration (mg/L)

Dosage (g/L)

pH

16

3

Ambient

16

3

Ambient

Holm oak pruning biochar

NA

24

-

Langmuir

50

5

2

Oak, eucalyptus and pine pruning mixture biochar

NA

24

-

Langmuir

50

5

2

Sewage sludge biochar

NA

-

pseudo second order

Freundlich

100

2

6

Pinus taeda biochar

NA

72

elovich

Freundlich

100

0.1

6

NA

72

elovich

Freundlich

100

0.1

6

NA

-

pseudo second order

Langmuir

150

-

6

Pinus taeda biochar (NaOH activated) Sawdust biochar (Iron and zinc coated)

39

Sur (

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Spirulina sp. (microalgae) biochar

NA

24

-

Freundlich

100

1

8

3

NA

24

pseudo second order

Freundlich

20

0.4

6

1

NA

-

pseudo second order

Freundlich

100

2

6

1

NA

216

pseudo second order

Langmuir

120

0.4

9

3

NA

216

pseudo second order

Langmuir

120

0.4

9

NA

120

-

Freundlich

200

0.5

4

NA

120

-

Freundlich

200

0.5

4

NA

120

-

Freundlich

200

0.5

4

61

120

pseudo first order

Langmuir

100

0.1

6

of

Chicken bone-based biochar (Fe3O4 coated) Rice straw biochar (g-MoS2 decorated) Sewage sludge biochar (Ferric activated) Rice straw biochar (H3PO4 activated) Swine manure biochar (H3PO4 activated) Beet pulp biochar (Steam activated) Commercial activated carbon (Steam activated coconut shell) Commercial activated carbon (H3PO4 activated wood)

Jo ur

na

lP

re

-p

ro

NA= not analyzed.

40

Journal Pre-proof

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of

Graphical Abstract

41

Journal Pre-proof

Highlights 

Microalgae (Spirulina sp.) was successfully applied for biochar production



High pyrolysis temperatures led to low O/C and H/C and high SSA and pHpzc values



SPAL-BC750 had the highest hydrophobicity, crystallizations, and functional groups SPAL-BC750 had the highest TC adsorption capacity (132.8 mg TC/g biochar)



SPAL-BCs are economical and potentially valuable adsorbents

Jo ur

na

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re

-p

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of



42

Figure 1

Figure 2

Figure 3

Figure 4

Figure 5

Figure 6

Figure 7

Figure 8

Figure 9