cationic polyacrylamide

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Magnetic flocculation of algae-laden raw water and removal of extracellular organic matter by using composite flocculant of Fe3O4/ cationic polyacrylamide Jiangya Ma a, b, *, Wei Xia a, b, Xue Fu a, b, Lei Ding a, b, Yanli Kong a, b, Huiwen Zhang a, b, Kun Fu c a b c

School of Civil Engineering and Architecture, Anhui University of Technology, Maanshan, Anhui, 243002, China Engineering Research Center of Biomembrane Water Purification and Utilization Technology, Ministry of Education, Maanshan, Anhui, 243002, China College of Environmental Science and Engineering, Tongji University, Shanghai, 200092, China

a r t i c l e i n f o

a b s t r a c t

Article history: Received 5 August 2019 Received in revised form 20 October 2019 Accepted 11 November 2019 Available online xxx

Algae-laden water with low turbidity is a critical problem in eutrophic lakes of arid regions. Thus, how to effectively separate algae and turbidity is an urgent problem for drinking water production. In the current study, the magnetic flocculation performance of algae-laden raw water purification was investigated by using magnetic composite flocculant Fe3O4/cationic polyacrylamide (CPAM). The Chlamydomonas sp., turbidity and UV254 removal efficiency were evaluated at different Fe3O4: CPAM mass ratios, dosages and pH values. The recovery and reusability of Fe3O4/CPAM in flocculation was tested. Moreover, the saturation magnetization of flocculants and flocs and zeta potential of supernatant in magnetic separation was examined, and the flocculation mechanism of Chlamydomonas sp. was explored accordingly. In addition, the removal efficiency of bound extracellular organic matter (BEOM) and dissolved extracellular organic matter (DEOM) was compared by using Fe3O4/CPAM. The flocculation mechanism and interactions between Fe3O4/CPAM and extracellular organic matters were analyzed according to ultraviolet (UV) spectra, fluorescence three-dimensional excitation emission matrix spectra (EEM), gel permeation chromatography (GPC), and X-ray photo electronic spectroscopy (XPS). Results show that more than 97% of chlorophyll a (Chla), 87% of turbidity, and 65% of UV254 were removed at Fe3O4/CPAM dosage of 1.2 mg/L, Fe3O4: CPAM mass ratio of 1.5:1.0, and pH of 4.0e9.0. Charge neutralization was dominant at pH < 9.0, whereas adsorption through hydrogen bond played an important role at pH > 9.0. Humic acid-like substances and tryptophan-like proteins were the main components of DEOM, whereas fulvic acid-like substances, tryptophan-like proteins and few polysaccharides existed in BEOM. Fe3O4/CPAM exhibited excellent performance in binding with the functional groups in tryptophan-like proteins, such as amino, carboxyl and hydroxyl groups. © 2019 Elsevier Ltd. All rights reserved.

Handling editor: Baoshan Huang Keywords: Magnetic flocculation Algal removal Extracellular organic matter Cationic polyacrylamide Chlamydomonas sp

1. Introduction With the development of industries and agriculture worldwide, a large amount of nitrogen and phosphorus nutrients have been discharged into surface water, leading to frequent algal blooms in

* Corresponding author. School of Civil Engineering and Architecture, Anhui University of Technology, Maanshan, Anhui, 243002, China. E-mail addresses: [email protected], [email protected] (J. Ma), [email protected] (W. Xia), [email protected] (X. Fu), dinglei1978@163. com (L. Ding), [email protected] (Y. Kong), [email protected] (H. Zhang), [email protected] (K. Fu).

the summer season (Chen et al., 2019). Many eutrophic lakes and reservoirs in arid regions of China, including Chao Lake, Taihu Lake, are critical drinking water sources. The existence of algae in water sources can block rapid filtration tanks and cause membrane fouling in water treatment plants (Zhang et al., 2019b). These water sources are characterized by high concentrations of algae and low turbidity. Algal organic matters (AOM) produced during algal metabolism have adverse effects on human health. They are divided into two groups: intracellular organic matter (IOM) and extracellular organic matter (EOM) (Xu et al., 2018). IOM and EOM are difficult to remove from water through conventional water treatment technologies. Therefore, the effective separation of algae,

https://doi.org/10.1016/j.jclepro.2019.119276 0959-6526/© 2019 Elsevier Ltd. All rights reserved.

Please cite this article as: Ma, J et al., Magnetic flocculation of algae-laden raw water and removal of extracellular organic matter by using composite flocculant of Fe3O4/cationic polyacrylamide, Journal of Cleaner Production, https://doi.org/10.1016/j.jclepro.2019.119276

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turbidity, and AOM has become an urgent problem in tap water treatment. Several techniques have been developed for algal removal, including centrifugation (Qiu et al., 2018), gravitational settling (Wang et al., 2014), air flotation (Nguyen et al., 2019), membrane filtration (Zhang et al., 2019a), oxidation (Diao et al., 2019), flocculation (Chen et al., 2019), and ultraviolet radiation (Lundgreen et al., 2019). Among them, flocculation is the most essential method in drinking water production. If a suitable flocculant can be developed, we can conveniently separate algae through effective flocculation without adding any other complicated treatment units (Ma et al., 2017). Aluminum and iron based flocculants can be used to remove algae and turbidity from water, and they can achieve algal removal efficiency of 85%e95% (Xu et al., 2018). However, the application of iron based flocculants for drinking water production is limited by their increased chromaticity, resulting from iron residuals. By contrast, aluminum based flocculants, such as polyaluminum chloride (PAC), are widely used for source water treatment (Lin and Ika, 2019). However, the compactness of flocs produced by PAC is insufficient for complete algal sedimentation, leading to flocs resuspension and decreased algal separation efficiency (Zhu et al., 2018). As a result, increased dosages of PAC are needed for enhanced flocculation toward low turbidity water. Thus, organic flocculants are inappropriate for purifying algae-laden water with low turbidity. Compared with inorganic flocculants, organic flocculants such as cationic polyacrylamide (CPAM) exhibit excellent flocculation performance in water treatment because of the low dosage needed, high positive charge density, and favorable adsorption and bridging effect (An et al., 2019; Liu et al., 2018). Nevertheless, the resuspension of flocs generated by CPAM still remains unresolved. Magnetic flocculation, a newly emerging technology, has been extensively used for solid-liquid separation in water treatment under an external magnetic field. Magnetic flocculation technology has several advantages, including effective capture, rapid settling, easy recovery and recyclability (Tang et al., 2019). Ferroferric oxide (Fe3O4), a magnetic seed, is used in combination with CPAM for colloidal pollutant separation. The generated flocs of magnetic flocculation cannot be broken and dispersed into water because of the powerful magnetic suction between flocs and external magnet, thereby solving the issue of flocs resuspension. The algal cell integrity remains intact during flocculation, avoiding the release of IOM into water. However, EOM can be released into water during the algal growth period, which accelerates membrane fouling, production of obnoxious disinfection by-products, and foul odor in drinking water (Tang et al., 2017). EOM is divided into two groups, namely bound extracellular organic matter (BEOM) and dissolved extracellular organic matter (DEOM) (Ma et al., 2019; Qu et al., 2012; Yang et al., 2019). The flocculation performance and mechanism of BEOM and DEOM are still unclear. In addition to algal and turbidity removal, control of EOM is also important during flocculation. In recent years, flocculation of Microcystis aeruginosa (Chen et al., 2018; Guo et al., 2017), Cylindrospermopsis raciborskii (Li et al., 2018), Chlorella ellipsoidea (Gerchman et al., 2017; Kothari et al., 2017) and Melosira sp. (Henderson et al., 2010) was closely investigated in raw water treatment. Studies found that 69%e98% of Microcystis aeruginosa can be removed by using 3.5e6.2 mg/L ampholytic modified chitosan flocculant CPCTS-g-P (CTADMDAAC), which was synthesized from photo polymerization (Chen et al., 2018). Furthermore, 51% of UV254, and 38% of DOC in AOM of Microcystis aeruginosa were separated by aluminum sulfate at high Al dosages (Guo et al., 2017). For Cylindrospermopsis raciborskii raw water, 73%e91% of chlorophyll a (Chla) was removed by using polyaluminum ferric chloride coagulant at dosage of

5.0e10 mg/L. Algal cells could be damaged at high dosages (>10 mg/L), resulting in the release of algal toxins and secondary pollution of raw water (Li et al., 2018). However, more than 90% of Chlorella vulgaris were effectively harvested using CPAM at 5.0 mg/L and pH of 10 (Gerchman et al., 2017). Moreover, 46%e71% algal organic matter of Melosira sp. could be eliminated by aluminum sulfate coagulant, which was higher than that by using ferric chloride coagulant (Henderson et al., 2010). Chlamydomonas sp. is one of the most common green algal species in algal boom of lakes or reservoirs. However, it has not been studied in flocculation. In this study, the removal efficiency of Chlamydomonas sp. and turbidity was investigated by magnetic flocculation using composite flocculant Fe3O4 coating with CPAM (Fe3O4/CPAM). The removal performance of DEOM and BEOM was compared, and the interactions between Fe3O4/CPAM and DEOM or BEOM were analyzed in according with UV spectra, fluorescence threedimensional excitation emission matrix spectra (EEM), gel permeation chromatography (GPC), and X-ray photo electronic spectroscopy (XPS). Furthermore, the recovery performance of Fe3O4/CPAM and the morphology and magnetization of flocs were also determined. Finally, the flocculation mechanism of Chlamydomonas sp. for drinking water treatment was comprehensively summarized and discussed. 2. Materials and methods 2.1. Raw materials The magnetic composite flocculant Fe3O4/CPAM was prepared in a laboratory in accordance with our previously reported method (Ma et al., 2018) (Fig. S1). The chemical structures of Fe3O4/CPAM and monomers are exhibited in Scheme 1. CPAM was synthesized by copolymerization of acrylamide (AM) and methacryloxyethyl trimethyl ammoniumchloride (DMC) through low-pressure UV initiation. AM and DMC have unsaturated double bonds, which are desirable for the formation of long chains in copolymerization. Furthermore, DMC, a cationic monomer, contains positive charged groups of quaternary ammonium eNþ(CH3)3. This positive structure was favorable for flocculation through charge neutralization. The mass ratio of Fe3O4 and CPAM was 1.5:1.0 ([h] CPAM ¼ 0.88 L/g), and the cationic degree of composite flocculant was 40%. The saturation magnetization, remanence, and coercive magnetization of Fe3O4/CPAM were 59, 0.92, and 2.2 emu/g, respectively. The microalgae used in flocculation (Chlamydomonas sp.) were purchased from the Institute of Hydrobiology, Chinese Academy of Sciences (Wuhan, China). The chemicals used in culture media were of analytical grade (>96 wt %), which were provided by Sinopharm Group Co.Ltd (Beijing, China) without exception. Deionized water was used in all experiments to prepare solutions through dissolution or dilution. 2.2. Algae cultivation and test water Chlamydomonas sp. was grown in the prepared culture media with the following compositions (Tan et al., 2019): NaHCO3 (0.013 g/L), Na2SiO3$9H2O (0.028 g/L), NaHCO3 (0.013 g/L), NaNO3(0.085 g/L), K2HPO4(0.0087 g/L), CaCl2$2H2O(0.037 g/L), MgSO4$7H2O(0.037 g/L), vitamin Thiamine$HCl (0.10 mg/L), and EDTA trace element solution with the following concentration was added to 1 L of the above solution: FeCl3$6H2O (3.2 g/L), CuSO4$5H2O (0.010 g/L), ZnSO4$7H2O (0.022 g/L), CoCl2$6H2O (0.010 g/L), MnCl2$4H2O (0.018 g/L), Na2MoO4$2H2O (0.0060 g/L), and H3BO3(1.0 g/L). The culture media was sterilized for 20 min at 121  C in an autoclave and vaccinated with Chlamydomonas sp. after completely cooling to room temperature. The algal culture

Please cite this article as: Ma, J et al., Magnetic flocculation of algae-laden raw water and removal of extracellular organic matter by using composite flocculant of Fe3O4/cationic polyacrylamide, Journal of Cleaner Production, https://doi.org/10.1016/j.jclepro.2019.119276

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Scheme. 1. The chemical structures of Fe3O4/CPAM and monomers.

was incubated at 25  C with 2700 lx illumination and 12/12 h light/ dark period in a RGX-3500 artificial photochemical incubator (Shanghai Kuntian Experimental Instruments Co., Ltd, China). The Chlamydomonas sp. cultures were harvested in the late exponential growth stage for further preparation of algae-laden water. Experimental raw water was collected from Chao Lake (Hefei, China), which is the most important drinking water source for Chaohu City and several surrounding towns. The obtained raw water samples were first filtered through 0.45 mm glass fiber membranes to remove large suspended matter and phytoplankton. Subsequently, a predetermined amount of Chlamydomonas was added into the filtered raw water under stirring to prepare algaeladen raw water. The water quality characteristics of test water were as follows: pH of 7.8e8.5, turbidity of 20e36 NTU, algal cell density of 1.2107e1.5107 cell/mL, UV254 of 0.090e0.12 cm1, and Chla of 0.25e0.28 mg/L.

stirred at 300 rpm for 15 min, followed by slowly stirred at 50 rpm for 25 min (Figs. S2eS3). Subsequently, the beaker was placed on a quadrate permanent magnet (10 cm L  10 cm W  1 cm H) for gravity and magnetism settling in 5e10 min. Finally, the supernatants at the depth 2 cm below the water surface were collected for further measurement. The magnetic media Fe3O4 was recovered with following process for further using in preparation of magnetic flocculant of Fe3O4/CPAM. In the first step, the flocs collected from magnetic separation were soaked in sodium hydroxide solution (NaOH, 0.1 M) for 1 h. Then, the solution was rapidly stirred at 1000 rpm for 10 min. The supernatant was poured out and keep the Fe3O4 particles by using quadrate permanent magnet. Add deionized water, and repeat rapid stirring and magnetic separation for three times. The clean Fe3O4 particles were combined with CPAM according to the method reported in our previous work, obtaining recovered magnetic flocculant Fe3O4/CPAM for reusing in flocculation.

2.3. DEOM and BEOM extraction DEOM and BEOM were extracted from algae cells through centrifuge separation approach by using a TG-16 high-speed centrifuge (Xinbao Experimental Instrument Company, China) with following two steps (Tang et al., 2017). Firstly, a certain amount of algae cells were centrifuged at 4000 rpm for 15 min. Afterward, the supernatant was filtered through a 0.45 mm filtering membrane for separating residual algae cells from filtrate. The extracted filtrate was described as DEOM solution. Secondly, add predetermined volume 0.60% NaCl into the obtained residual algae cells under magnetic stirring. Then, the mixture was heated in a HH-US water bath (Spring Instrument Co., Ltd, China) at 50  C for 20 min, followed by centrifugation at 10000 rpm for 15 min. The supernatant was filtered through a 0.45 mm filtering membrane, obtaining the BEOM solution. 2.4. Magnetic flocculation The magnetic flocculation was conducted using a ZR4-6 program controlled mixing apparatus (Zhongrun Company, China). The experiments were performed in a 1 L beaker, and the operating procedure was set as follows: after adding a predesigned amount of flocculants Fe3O4/CPAM into the beaker, the tested water was rapidly

2.5. Analytical and characterization methods Several water quality parameters in flocculation processes were tested according to following analyzing methods. The algae content in our experiments were determined by Chla, which was measured by a 722s UVevis spectrophotometer (Inesa Analytical Instrument Co., Ltd, China) (Fig. S4). The turbidity of tested water before and after flocculation was detected by a 2100Q portable turbidimeter (HACH, USA), whereas the zeta potential was recorded by a ZS90 nano potential instrument (Malvern, UK). Moreover, a Model 7307 vibrating sample magnetometer (VSM, USA) was used to compare magnetization hysteresis loop of flocculants and flocs. A TOC-L total organic carbon analyzer (Shimadzu, Japan) was employed to measure TOC of BEOM and DEOM solution. In order to explore flocculation mechanism of algae extracellular organic substances by using magnetic flocculant Fe3O4/CPAM, various chemical structure or components qualitative characterizations were performed for BEOM and DEOM in flocculation. The ultraviolet spectra and molecular weight distribution of EOM solution were analyzed by the UV3600 ultraviolet spectrophotometer (Shimadzu, Japan) and the PrepLinc gel permeation chromatograph (GPC, J2Scientific, USA), respectively. A FE-4P-TCSPC fluorescence spectrophotometer (Horiba Jobin Yvon, France) were used to record

Please cite this article as: Ma, J et al., Magnetic flocculation of algae-laden raw water and removal of extracellular organic matter by using composite flocculant of Fe3O4/cationic polyacrylamide, Journal of Cleaner Production, https://doi.org/10.1016/j.jclepro.2019.119276

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the three dimensional excitation emission matrices (EEM) spectra of EOM during lex/em ¼ 200e450/200-550 nm to evaluate the changes of chemical composition in BEOM and DEOM during flocculation process. To reveal the interactions of EOM and flocculant Fe3O4/CPAM, an ESCALAB 250Xi X-ray photoelectron spectrometer (Thermo Fisher Scientific, USA) was used to accomplish series survey scan the photoelectron spectra of flocs of BEOM and DEOM. Furthermore, series high resolution XPS scans of C and Fe elements of flocs were also examined for further analysis.

3. Results and discussion 3.1. Removal of Chla and turbidity 3.1.1. Comparison of Fe3O4/CPAM and CPAM The flocculation performance of turbidity and Chla removal by using Fe3O4/CPAM was compared with that of CPAM. Fig. 1(a) depicts the experimental comparison results with different flocculant dosages. Obviously, more than 86% of turbidity and 90% of Chla were successfully removed during flocculation, indicating that Fe3O4/CPAM and CPAM exhibited excellent performance in flocculation of algae-laden water. Using Fe3O4/CPAM, the turbidity and Chla removal rate increased first with the increase of dosage from 0.60 mg/L to 1.2 mg/L, and decreased with the further increase of dosage within 1.2e3.6 mg/L (Fig. S5). The maximum turbidity and Chla removal rate achieved at Fe3O4/CPAM dosage of 1.2 mg/L were 87% and 97%, whereas the optimal turbidity and Chla removal rate

achieved at CPAM dosage of 1.8 mg/L and 3.0 mg/L were 84% and 90%, respectively. The results indicated that CPAM required an increased dosage, and only obtained lower turbidity and Chla removal efficiency compared with Fe3O4/CPAM. As the CPAM dosage was insufficient for flocculation (Fig. S6), the collision probability between microalgae and CAPM would be reduced. This led to decreased turbidity and Chla removal rate. Thus, a higher CPAM dosage was needed for promoting collision and adsorption probability. Conversely, due to the introduction of Fe3O4 nanoparticles into CPAM flocculants, the magnetostatic attractiveness and van der Waals force improved the formation and subsequent agglomeration of small microalgaeeflocculants precipitates, resulting in increased separation efficiency of suspended particles and microalgal cells at lower Fe3O4/CPAM dosage (Zhao et al., 2015; Zhou et al., 2018b). However, the slight decline of the removal rate caused by increased Fe3O4/CPAM dosage might be attributed to the electrostatic barrier from CPAM polymer chain coating on the Fe3O4 nanoparticles surface, thereby inhibiting magnetostatic attraction at the core of flocs (Yeap and Tia, 2019). Hence, the introduction of Fe3O4 nanoparticles into CPAM flocculants was beneficial for efficient flocculation in algae-laden turbid water treatment.

3.1.2. Effect of Fe3O4: CPAM mass ratio To obtain excellent flocculation performance, the effect of Fe3O4: CPAM mass ratio on turbidity, Chla and UV254 removal rate was comprehensively investigated. A series of magnetic composite flocculants was prepared under different Fe3O4: CPAM mass ratios,

Fig. 1. Magnetic flocculation property for algae-laden raw water treatment: (a) Comparison of Fe3O4/CPAM and CPAM, effect of mass ratio of Fe3O4: CPAM on (b) turbidity removal rate, (c) Chla removal rate, and (a) UV254 removal rate.

Please cite this article as: Ma, J et al., Magnetic flocculation of algae-laden raw water and removal of extracellular organic matter by using composite flocculant of Fe3O4/cationic polyacrylamide, Journal of Cleaner Production, https://doi.org/10.1016/j.jclepro.2019.119276

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including 0.5:1, 1:1, 1.5:1, 2:1 and 3:1. The experimental results are presented in Fig. 1(bed). As shown in Fig. 1(b), a turbidity removal rate of 78%e88% was achieved by using Fe3O4/CPAM with mass ratio of 1.5:1, which was higher than that of other flocculants with different mass ratios at various dosages. As exhibited in Fig. 1(c), the Chla removal rate showed large differences when using Fe3O4/ CPAM with different mass ratio. The maximum Chla removal rate was achieved at 98% by using 1.2 mg/L Fe3O4/CPAM with mass ratio of 1.5:1. However, only 14% and 19% of Chla were removed by flocculants Fe3O4/CPAM at dosage of 0.60 mg/L and mass ratios of 0.5:1 and 2:1, respectively, displaying poor flocculation performance in algae-laden water treatment. Approximately 96% of Chla was separated from water when using 3.6 mg/L Fe3O4/CPAM with mass ratio of 3:1. This finding indicated that a higher dosage was needed for algal removal, which would increase the cost. If the percentage of CPAM is lower than that of Fe3O4, the charge neutralization and bridging effect of CPAM will not completely destabilize colloidal particles and algal cells. Moreover, the settling process of flocs was extremely rapid due to the gravity of excessive Fe3O4, which was insufficient for adequate collision and agglomeration between Fe3O4/CPAM and algal cells. However, excessive CPAM percentage in flocculants would cause a “cage effect” between flocculants and algal cells, forming mutual exclusion between small aggregates and further preventing flocs growth. In addition, abundant natural organic matters (NOM), such as humic substances, exist in natural raw water. Thus, the UV254 removal rate was also investigated in the magnetic flocculation of algae-laden raw water. As illustrated in Fig. 1(d), Fe3O4/CPAM with mass ratios of 1:1 and 1.5:1 achieved 79% and 70% UV254 removal efficiency in flocculation at dosage of 3.6 mg/L and 2.4 mg/L, respectively. By contrast, Fe3O4/CPAM with mass ratios of 0.5:1 and 2:1 did not effectively separate UV254 from algae-laden raw water. Obviously, increased flocculant dosage was required in flocculation for UV254 removal. Organic matters have negative charges, always interact with microalgal cells, and further change the surface charge of Chlamydomonas sp. After being adsorbed on microalgal cells, the electrostatic stabilization of NOMealgal particles was enhanced because of the highly negatively charged absorbed layer, leading to the increase of flocculant dosage to neutralize the negative changes (Jiang et al., 2010). On the other hand, the steric stabilization of Fe3O4 was strengthened when NOM was absorbed on the surface of excessive Fe3O4 nanoparticles, inhibiting algal and UV254 removal through further aggregation. Consequently, 1.2 mg/L Fe3O4/CPAM with mass ratio of 1.5:1 was favorable for flocculation of algaeladen raw water.

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3.1.3. Effect of pH and zeta potential analysis In flocculation, pH is the most important factor for surface charge of colloids in water. Thus, the effect of pH on turbidity, Chla and UV254 removal rate, and zeta potential was studied. As evident from Fig. 2(a), their removal rates apparently increased with the increase of pH from 3.0 to 5.0 and then slightly decreased with the further increase of pH from 5.0 to 10. Moreover, 87%e90% of turbidity, 94%e96% of Chla, and 67%e75% of UV254 were removed at pH of 4.0e8.0. Obviously, Fe3O4/CPAM showed effective flocculation in a wide pH value, indicating that the composite magnetic flocculants have excellent ability to adapt to pH changes in the water environment. As exhibited in Fig. 2(b), the zeta potential of raw algae-laden water was 15 mVe5.8 mV. The results suggested that Chlamydomonas sp. was completely negatively charged at various pH values, which was attributed to the ionization of anionic functional groups, such as carboxyl (eCOOH), hydroxyl (-OH), amino (eNH2), and phosphate groups (ePO34 ), etc. In addition, the zeta potential of Fe3O4/CPAM was positive (1.4e26 mV) within pH of 3.0e9.0, and the isoelectric point of flocculants was observed at pH of 8.6. As the pH increased from 9.0 to 10, the zeta potential of Fe3O4/CPAM drastically decreased from 1.4 mV to 26 mV. Fe3O4 was negatively charged at various pH values because of the hydroxyl group existing on its surface (Zhao et al., 2015). However, the acylamino group (O]CeNH2) in CPAM neutralized these negative charges in composite reaction with Fe3O4 through ion exchange, increasing the zeta potential (Prochazkova et al., 2013). Furthermore, most positive charge of Fe3O4/CPAM is derived from the quaternary ammonium functional group eNþ(CH3)3, which can resist the influence of pH on surface charge (Liu et al., 2016). However, in alkali environment, the amine groups in CPAM were deprotonated to form eNH-, decreasing the zeta potential (Jia et al., 2016). The zeta potential of supernatant after flocculation was improved at various pH values, and displayed a positive charge (0.90e15 mV) at pH < 5.0. The isoelectric point of the supernatant appeared at pH 5.0, corresponding to maximum turbidity, Chla and UV254 removal rate in Fig. 2(a) due to the minimum stability of colloidal particles and microalgal cells. At pH < 8.6, Fe3O4/CPAM and microalgal cells carried opposite charges, resulting in the occurrence of charge neutralization and double-layer compression in flocculation (Zhou et al., 2018a; Rashid et al., 2019). However, at pH < 3.0, the excessive positive charge on the surface of microalgae prohibited the collision and agglomeration with positively charged Fe3O4/CPAM. Conversely, the zeta potential of Fe3O4/CPAM was lower than that of microalgal cells at pH > 9.0, and both were negatively charged. The electrostatic

Fig. 2. The effect of pH on flocculation: (a) turbidity, Chla and UV254 removal rate, (b) zeta potential.

Please cite this article as: Ma, J et al., Magnetic flocculation of algae-laden raw water and removal of extracellular organic matter by using composite flocculant of Fe3O4/cationic polyacrylamide, Journal of Cleaner Production, https://doi.org/10.1016/j.jclepro.2019.119276

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attraction originated from charge neutralization was changed into electrostatic repulsion. Nevertheless, the zeta potential of supernatant after flocculation was increased at pH > 9.0. We speculated that the strong adsorption derived from hydrogen bonds between eCeNH- in Fe3O4/CPAM and eCOOH, and eOH in microalgal cells was dominant in flocculation, decreasing the negative charges in Fe3O4/CPAM (Jia et al., 2016). Overall, Fe3O4/CPAM exhibited a desirable flocculation performance for microalgal and turbidity removal at a wide pH value (4.0e10), although different flocculation mechanism dominant at various pH environments. Furthermore, the results indicated that Fe3O4/CPAM has an excellent pH resistance in flocculation of algae-laden turbid water. 3.1.4. Effect of magnetic field and recycling The effect of the external magnetic field was evaluated in algaeladen water flocculation at different settling times. The flocculation performance and magnetization of first used and reused Fe3O4/ CPAM were also assessed in magnetic flocculation. As exhibited in Fig. 3(a), the turbidity removal rate with or without external magnetic field rapidly increased with the increase of settling time from 1 min to 9 min, and then slowly increased with the further increase of settling time from 9 min to 24 min. Turbidity removal rates of 95% and 92% were achieved using Fe3O4/CPAM under external magnetic field and without magnetic field at a settling time of 9 min, respectively. Moreover, the differential was kept within 15 min. This finding indicated that when using Fe3O4/CPAM, the flocs presented excellent settling property, and the average particle sizes of settled flocs generated at pH of 5.0, 7.0, and 9.0 were 16.7, 13.6, and 17.8 mm, respectively (Figs. S7e9). In addition, a small portion of flocs with a small particle size settled through magnetic attraction force under external magnetic field and could not settle without a magnetic field. These small flocs remained suspended in solution and required a much longer time for sedimentation (Wang et al., 2014). No obvious increase of Chla removal rate (93%e97%) was observed for flocculation under magnetic field with increased settling time. However, the Chla removal rate without magnetic field increased from 85% to 94% in 24 min. This phenomenon revealed that the external magnetic field was advantageous to further remove algal cells in flocs settling through sweeping and enmeshment effect. As shown in Fig. 3(b), the first used Fe3O4/CPAM presented a slightly different flocculation performance compared with reused Fe3O4/CPAM, although it was satisfactory in reusing flocculation. The maximum turbidity and Chla removal rates of 88% and 98%

were obtained by first used Fe3O4/CPAM at 1.2 mg/L dosage, whereas removal rates of 84% and 91% were achieved by reused Fe3O4/CPAM at 3.0 mg/L dosage, respectively. The decrease of turbidity and Chla removal efficiency by reused Fe3O4/CPAM at low dosage was attributed to the occupation of charge neutralization and adsorption sites on the surface of Fe3O4/CPAM because of the incomplete separation of flocculants and microalgal cells during Fe3O4/CPAM recovery. The result was in accordance with magnetization analysis in Fig. 4(a). The saturation magnetization of first used Fe3O4/CPAM was 63 emu/g. However, the saturation magnetization of recycled Fe3O4 nanoparticles and reused Fe3O4/CPAM was 56 and 54 emu/g, respectively. The decrease of magnetization during recovery suggested that a certain loss and incomplete desorption were inevitable. The magnetization difference for recovered Fe3O4 and reused Fe3O4/CPAM was ascribed to the coating of CPAM on the surface of Fe3O4 nanoparticles, which indirectly indicated the successful composite of CPAM and Fe3O4 (Li et al., 2017). As depicted in Fig. 4(b), the saturation magnetization of flocs generated at pH of 5.0, 7.0 and 9.0 was 60, 56, and 52 emu/g, respectively. The adhesion and agglomeration of colloidal particles and microalgal cells caused the decrease of flocs magnetization. Obviously, flocs magnetization at acidic conditions was larger than that at alkaline conditions, indicating that the charge neutralization was dominant in flocculation at acidic condition and had no influence on demagnetization in flocculation. However, adsorption through hydrogen bond at alkaline conditions enabled flocs to become wrapped by microalgal cells, decreasing flocs magnetization (Ma et al., 2018). Importantly, all analysis results demonstrated that the magnetization of first used or reused Fe3O4/CPAM and flocs were sufficient for rapid separation in flocculation. 3.2. Removal of DEOM and BEOM 3.2.1. UV spectrum analysis Fig. 5 exhibited the UV spectra of supernatant liquor of DEOM and BEOM solutions at various Fe3O4/CPAM dosages. The UV absorption spectrum of a substance is determined by the characteristics of chromophores and aid-chromophores in its molecules. For DEOM flocculation, maximum absorption peaks of 3.48, 3.29, 3.08, 3.18, 3.29, and 3.18 were observed at 209, 208, 210, 206, 209, and 207 nm wavelengths at Fe3O4/CPAM dosages of 0, 0.60, 1.2, 1.8, 2.4, and 3.0, respectively. The peaks near 205e210 nm were possibly attributed to the chromophores of the amino group (eNH2) and unsaturated conjugated systems (pep* transition), such as

Fig. 3. Flocculation performance of Fe3O4/CPAM: (a) the effect of magnetic field on turbidity and Chla removal rate in flocs settling, and (b) comparison of flocculants first use and recovery.

Please cite this article as: Ma, J et al., Magnetic flocculation of algae-laden raw water and removal of extracellular organic matter by using composite flocculant of Fe3O4/cationic polyacrylamide, Journal of Cleaner Production, https://doi.org/10.1016/j.jclepro.2019.119276

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Fig. 4. Magnetization curves: (a) comparison of first used Fe3O4/CPAM, recycled Fe3O4 and reused Fe3O4/CPAM; (b) the effect of pH on flocs magnetization.

Fig. 5. UV spectra: (a) DEOM, and (b) BEOM after flocculation at different Fe3O4/CPAM dosages.

carbonyl group eC]O and aromatic ring. This finding indicated that various types of amino acids and proteins existed in DEOM (Yan et al., 2019). The pep* transition existence resulted from the existence of p bond in unsaturated conjugated systems. Furthermore, as shown by wavelength changes, the pep* absorption was red-shifted because of the presence of certain aid-chromophore groups. The intensity of these absorption peaks decreased at different degrees after flocculation because of the interaction between these components and Fe3O4/CPAM. Moreover, the dosage of 1.2 mg/L was the most effective in DEOM flocculation. As displayed in Fig. 5(b), an obvious absorption peak was observed at 254 nm wavelength for BEOM, which was ascribed to humic substances (Guo et al., 2017). Compared with raw BEOM solution, the DEOM solution showed slightly decreased intensity of absorption peaks at 254 nm after flocculation, and the minimum value was observed at dosage of 1.2 mg/L. Thus, DEOM and BEOM have different chemical compositions, and Fe3O4/CPAM with dosage of 1.2 mg/L was favorable in flocculation through various interactions. 3.2.2. EEM analysis Fluorescence EEM, a rapid and sensitive technique used to characterize organic compounds, was employed to analyze the changes of fluorescent algal extracellular organic matters after magnetic flocculation (Hou et al., 2018). As illustrated in Fig. 6(a),

two evident peaks were observed at lex/em ¼ 270e300/ 300e360 nm and lex/em ¼ 325e400/400e480 nm for raw DEOM solution, which were related to tryptophan-like proteins and humic-like substances, respectively (Zhang et al., 2018). Tryptophan-like proteins are associated with microbial activity and biological productivity in microalgal growth (Chu et al., 2015). The results demonstrated that tryptophan-like proteins and humic acid-like substances existed in DEOM. The fluorescence peak at lex/ em ¼ 270e300/300e360 nm was also found in raw BEOM solution, as shown in Fig. 7(a). In addition, another peak appeared at lex/ em ¼ 350e475/300e400, which was derived from soluble microbial by-product-like and humic acid-like substances (Li et al., 2018). Compared with DEOM, BEOM presented lower fluorescent intensities for these peaks, indicating lower concentration of organic matters. The result was consistent with the TOC analysis result in Fig. S10. Proteins are important components of microalgal cells and can be released during the metabolism process of Chlamydomonas sp. cells (Qu et., 2012). Thus, the proteins in DEOM and BEOM can be detected. Furthermore, as shown in Fig. 6(bef) and Fig. 7(bef), the fluorescent intensities of all peaks were reduced in DEOM and BEOM spectra after flocculation with various Fe3O4/CPAM dosages. The tryptophan-like proteins were almost undetectable in DEOM and BEOM solution after flocculation at Fe3O4/CPAM dosage of 1.2e1.8 mg/L. This finding suggested that protein-like substances in

Please cite this article as: Ma, J et al., Magnetic flocculation of algae-laden raw water and removal of extracellular organic matter by using composite flocculant of Fe3O4/cationic polyacrylamide, Journal of Cleaner Production, https://doi.org/10.1016/j.jclepro.2019.119276

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Fig. 6. Fluorescence EEM spectra of DEOM before and after flocculation at various Fe3O4/CPAM dosages: (a) dosage ¼ 0 mg/L, (b) dosage ¼ 0.60 mg/L, (c) dosage ¼ 1.2 mg/L, (d) dosage ¼ 1.8 mg/L, (e) dosage ¼ 2.4 mg/L, and (f) dosage ¼ 3.0 mg/L.

DEOM and BEOM were effectively removed by magnetic flocculation. Fe3O4/CPAM exhibited excellent performance in binding with the functional groups in tryptophan-like proteins, such as amino, carboxyl and hydroxyl groups (Zhang et al., 2018). Moreover, the fluorescent intensity of humic acid-like substances was greatly reduced in BEOM at a dosage of 0.60e1.2 mg/L, rather than in DEOM after flocculation. Obviously, humic acid-like substances were difficult to remove from DEOM and algae-laden water by

using magnetic flocculants of Fe3O4/CPAM (Fig. S11). However, organic matter was still detected in BEOM after flocculation at Fe3O4/CPAM dosage of 1.0e1.6 mg/L (Fig. S10). The result indicated that a small amount of non fluorescent polysaccharides were present in the BEOM solution. Overall, the lowest fluorescent intensities of these substances in DEOM and BEOM were found at dosage of 1.2 mg/L, which was in accordance with the aforementioned analysis results.

Please cite this article as: Ma, J et al., Magnetic flocculation of algae-laden raw water and removal of extracellular organic matter by using composite flocculant of Fe3O4/cationic polyacrylamide, Journal of Cleaner Production, https://doi.org/10.1016/j.jclepro.2019.119276

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Fig. 7. Fluorescence EEM spectra of BEOM before and after flocculation at various Fe3O4/CPAM dosages: (a) dosage ¼ 0 mg/L, (b) dosage ¼ 0.60 mg/L, (c) dosage ¼ 1.2 mg/L, (d) dosage ¼ 1.8 mg/L, (e) dosage ¼ 2.4 mg/L, and (f) dosage ¼ 3.0 mg/L.

3.2.3. Molecular weight (MW) distribution MW distributions of DEOM and BEOM solution before and after flocculation were characterized after magnetic flocculation at different Fe3O4/CPAM dosages. As presented in Fig. 8(a), three peaks of MW were observed at approximately 201, 15429, and 56896 Da for raw DEOM solution, which originated from tryptophan, macromolecular humic acid and protein-like substances, respectively (Xu et al., 2018; Zhang et al., 2018). Thus, the DEOM of

Chlamydomonas sp. mainly contains a few macromolecular humic acids substances and small molecular amino acids tryptophan. Obviously, the MW at 201 Da was not detected after flocculation by using Fe3O4/CPAM, which indicated that tryptophan was effectively removed in flocculation. The positively charged Fe3O4/CPAM might easily bind with negatively-charged aromatic compounds with conjugate double-bonds, such as tryptophan (Guo et al., 2017). However, the peak intensity of humic acid substances was not

Please cite this article as: Ma, J et al., Magnetic flocculation of algae-laden raw water and removal of extracellular organic matter by using composite flocculant of Fe3O4/cationic polyacrylamide, Journal of Cleaner Production, https://doi.org/10.1016/j.jclepro.2019.119276

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Fig. 8. Molecular weight distribution: (a) DEOM, and (b) BEOM before and after flocculation under various Fe3O4/CPAM dosages.

remarkably reduced after flocculation. It revealed that Fe3O4/CPAM had a poor flocculation performance in removing humic acid substances from DEOM. This result agrees well with the aforementioned EEM analysis result. As illustrated in Fig. 8 (b), no organic maters with MW > 1000 kDa were detected, whereas a notable peak was found at 508 Da. A small amount of fulvic acids may be present in BEOM (Chu et al., 2015). The peak intensity was slightly

deceased after flocculation at various Fe3O4/CPAM dosages. The result demonstrated that humic acid-like substances in BEOM were more easily removed by magnetic flocculation compared with those in DEOM, although they were still not removed completely. Overall, Fe3O4/CPAM was favorable for flocculation of small molecular substances. The complexes formed by macromolecular humic acid substances and proteins via hydrogen bond would inhibit

Fig. 9. XPS profiles: (a) survey spectra of flocs, deconvoluted spectra for C1s of (b) algae-laden flocs, (c) DEOM flocs, and (d) BEOM flocs.

Please cite this article as: Ma, J et al., Magnetic flocculation of algae-laden raw water and removal of extracellular organic matter by using composite flocculant of Fe3O4/cationic polyacrylamide, Journal of Cleaner Production, https://doi.org/10.1016/j.jclepro.2019.119276

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the flocculation performance (Tang et al., 2017). 3.2.4. XPS analysis The wide scan XPS spectra of flocs formed in magnetic flocculation were recorded to further investigate the interaction between Fe3O4/CPAM and microalgae, DEOM and BEOM. As shown in Fig. 9(a), the survey spectra of algae-laden, DEOM and BEOM flocs exhibited signals relevant to C 1s, N 1s, O 1s and Fe 2p, which were observed at binding energies of 294.1, 392.4, 539.0 and 731.2 eV, respectively. Furthermore, binding energies of 710.5 and 724.0 eV were ascribed to binding energy peaks of Fe 2p3/2 and Fe 2p1/2, respectively. In the Fe 2p XPS spectra, the fully oxidized states of Fe3þ and Fe2þ were one of the distinguishing characteristics of Fe3O4, which represented Fe2O3 and FeO, respectively (Tahir et al., 2018). Thus, Fe 2p found in flocs indicated that Fe3O4/CPAM combined with algal cells, DEOM, and BEOM in flocculation. Fig. 9(bed) displays the deconvoluted spectral signals relevant to C 1s of flocs. Three peaks had binding energies at 284.8, 286.2, and 288.1 eV in three flocs samples, which were assigned to aromatic CeC/CeH, CeN and C]O, respectively (Fig. S12) (Li et al., 2019; M & S, 2016; Tang et al., 2017). The CeC and CeH signals appeared at similar binding energies with comparable intensities. These functional groups were the most significant components in tryptophan-like protein substances, which were probably influenced by the p bond formed in attached algae. This suggested that Fe3O4/CPAM easily flocculated tryptophan-like protein substances in algal cells. The changes in the relative content of each peak indicated that functional groups formed complexes with contaminants, in which the O from eOH and C]O, and N from eNH2 donate electrons to metal ions. Thus, the electron density at the two adjacent carbon atoms decreased. As shown in Table 1, the proportion of Fe 2p in DEOM was 25%, higher than that in BEOM (19%). Moreover, the proportion of C 1s in DEOM was the lowest in three flocs samples. The results indicated that increased Fe3O4/CPAM dosage is needed in DEOM flocculation with low carbon removal efficiency. In other words, DEOM was difficult to be removed in magnetic flocculation. This conclusion was in agreement with the results of EEM analysis and provided further evidence for the interaction between Fe3O4/ CPAM and microalgal cells and EOM. 4. Conclusions In this study, magnetic composite was used in flocculation of algae-laden raw water with low turbidity to remove Chla, turbidity, and UV254. The flocculation efficiency of DEOM and BEOM in Chlamydomonas sp. algal cells was investigated, and the UV spectra, EEM, GPC, and XPS were used to analyze the flocculation mechanism. The results shows that more than 97% of Chla, 87% of turbidity, and 65% of UV254 were removed by using Fe3O4/CPAM dosage of 1.2 mg/L, Fe3O4: CPAM mass ratio of 1.5:1, and pH of 4.0e9.0. Moreover, 84% of Chla and 90% of turbidity were removed by using recovered Fe3O4/CPAM at a dosage of 3.0 mg/L. The external magnetic field facilitated the rapid separation of flocs from water and improved the turbidity and Chla removal efficiency.

Table 1 Chemical composition from the XPS analysis of the algae-laden flocs, DEOM flocs, and BEOM flocs. Samples

Algae-laden water flocs DEOM flocs BEOM flocs

Element (at. %) O 1s

C 1s

N 1s

Fe 2p

43.73 49.40 44.16

32.72 22.28 32.43

5.8 3.16 3.81

17.75 25.16 19.6

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Fe3O4/CPAM presented excellent flocculation performance at a wide pH value (4.0e9.0) because of the dominant role of charge neutralization in acidic conditions and adsorption through hydrogen bond in alkaline condition. The experimental results demonstrated that BEOM contains small molecular fulvic acid-like substances, tryptophan-like proteins, and few polysaccharides (MW < 1.0 kDa), whereas DEOM contains macromolecular humic acid-like substances (MW > 10 kDa) and tryptophan-like proteins. Tryptophan-like protein substances in DEOM and BEOM were effectively removed by using Fe3O4/CPAM through the interaction with amino, carboxyl, and hydroxyl groups. Conversely, humic acid-like substances from DEOM were difficult to remove in flocculation compared with those in BEOM. Declaration of competing interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. Acknowledgement The work was financially supported by the National Natural Science Foundation of China (Project Nos. 51878001 and 51408004), and the University Natural Science Research Key Project of Anhui Province (Project No. KJ2018A0044). Appendix A. Supplementary data Supplementary data to this article can be found online at https://doi.org/10.1016/j.jclepro.2019.119276. References An, Y.Y., Zheng, H.L., Zheng, X.Y., Sun, Q., Zhou, Y.H., 2019. Use of a floating adsorbent to remove dyes from water: a novel efficient surface separation method. J. Hazard Mater. 375, 138e148. M, D., S, B., 2016. Synthesis, characterization and application of acryloyl chitosan anchored copolymer towards algae flocculation. Carbohydr. Polym. 152, 459e467. Chen, L., Liu, C., Sun, Y., Sun, W., Xu, Y., Zheng, H., 2018. Synthesis and characterization of ampholytic flocculant CPCTS-g-P (CTA-DMDAAC) and its flocculation properties for microcystis aeruginosa removal. Processes 6 (5), 1e4. Chen, L., Sun, Y., Sun, W., Shah, K.J., Xu, Y., Zheng, H., 2019. Efficient cationic flocculant MHCS-g-P(AM-DAC) synthesized by UV-induced polymerization for algae removal. Separ. Purif. Technol. 210, 10e19. Chu, H., Yu, H., Tan, X., Zhang, Y., Zhou, X., Yang, L., Li, D., 2015. Extraction procedure optimization and the characteristics of dissolved extracellular organic matter (dEOM) and bound extracellular organic matter (bEOM) from Chlorella pyrenoidosa. Colloids Surf., B 125, 238e246. Diao, Z.H., Pu, S.Y., Qian, W., Liang, S., Kong, L.J., Xia, D.H., Lei, Z.X., Du, J.J., Liu, H., Yang, J.W., 2019. Photocatalytic removal of phenanthrene and algae by a novel Ca-Ag3PO4 composite under visible light: reactivity and coexisting effect. Chemosphere 221, 511e518. Gerchman, Y., Vasker, B., Tavasi, M., Mishael, Y., Kinel-Tahan, Y., Yehoshua, Y., 2017. Effective harvesting of microalgae: comparison of different polymeric flocculants. Bioresour. Technol. 228, 141e146. Guo, T., Yang, Y., Liu, R., Li, X., 2017. Enhanced removal of intracellular organic matters (IOM) from Microcystic aeruginosa by aluminum coagulation. Separ. Purif. Technol. 189, 279e287. Henderson, R.K., Parsons, S.A., Jefferson, B., 2010. The impact of differing cell and algogenic organic matter (AOM) characteristics on the coagulation and flotation of algae. Water Res. 44 (12), 3617e3624. Hou, J., Yang, Z., Wang, P., Wang, C., Yang, Y., Wang, X., 2018. Changes in Microcystis aeruginosa cell integrity and variation in microcystin-LR and proteins during Tanfloc flocculation and floc storage. Sci. Total Environ. 626, 264e273. Jia, S.Y., Yang, Z., Ren, K.X., Tian, Z.Q., Dong, C., Ma, R.X., Yu, G., Yang, W.B., 2016. Removal of antibiotics from water in the coexistence of suspended particles and natural organic matters using amino-acid-modified-chitosan flocculants: a combined experimental and theoretical study. J. Hazard Mater. 317, 593e601. Jiang, C., Wang, R., Ma, W., 2010. The effect of magnetic nanoparticles on Microcystis aeruginosa removal by a composite coagulant. Colloids Surf., A 369 (1e3), 260e267. Kothari, R., Pathak, V.V., Pandey, A., Ahmad, S., Srivastava, C., Tyagi, V.V., 2017.

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Please cite this article as: Ma, J et al., Magnetic flocculation of algae-laden raw water and removal of extracellular organic matter by using composite flocculant of Fe3O4/cationic polyacrylamide, Journal of Cleaner Production, https://doi.org/10.1016/j.jclepro.2019.119276