Influences of Surface Coating, UV Irradiation and Magnetic Field on

Dec 8, 2014 - The influences of surface coating, UV irradiation, and magnetic field on the magnetophoretic separation were systematically examined. Af...
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Influences of Surface Coating, UV Irradiation and Magnetic Field on the Algae Removal Using Magnetite Nanoparticles Shijian Ge,† Michael Agbakpe,† Zhiyi Wu,‡ Liyuan Kuang,† Wen Zhang,*,† and Xianqin Wang‡ †

John A. Reif, Jr. Department of Civil and Environmental Engineering, New Jersey Institute of Technology, Newark, New Jersey 07102, United States ‡ Department of Chemical Biological and Pharmaceutical Engineering, New Jersey Institute of Technology, Newark, New Jersey 07102, United States S Supporting Information *

ABSTRACT: Magnetophoretic separation is a promising and sustainable technology for rapid algal separation or removal from water. This work demonstrated the application of magnetic magnetite nanoparticles (MNPs) coated with a cationic polymer, polyethylenimine (PEI), toward the separation of Scenedesmus dimorphus from the medium broth. The influences of surface coating, UV irradiation, and magnetic field on the magnetophoretic separation were systematically examined. After PEI coating, zeta potential of MNPs shifted from −7.9 ± 2.0 to +39.0 ± 3.1 mV at a pH of 7.0, which improved MNPs-algae interaction and helped reduce the dose demand of MNPs (e.g., from 0.2 to 0.1 g·g−1 while the harvesting efficiency (HE) of over 80% remained unchanged). The extended Derjaguin−Landau−Verwey−Overbeek theory predicted a strong attractive force between PEIcoated MNPs and algae, which supported the improved algal harvesting. Moreover, the HE was greater under the UV365 irradiation than that under the UV254, and increased with the irradiation intensity. Continuous application of the external magnetic field at high strength remarkably improved the algal harvesting. Finally, the reuse of MNPs for multiple cycles of algal harvesting was studied, which aimed at increasing the sustainability and lowering the cost.

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INTRODUCTION Microalgae are not only the promising feedstock for biodiesel production,1−3 but also a water contaminant that negatively affects water quality with uncontrolled growth (harmful algal bloom).4−6 Thus, efficient algal separation or removal from water is not only critical for biofuel production, but also important for safe drinking water supply. Due to the small size (typically 2−20 μm in diameter) and low density (e.g., 0.5−5 gdry weight·L−1) of algal cells in growth media,3,7 most conventional algal separation methods such as sedimentation by gravity, centrifugation, microstraining, chemical coagulation, precipitation, filtration, and flotation are often energy- or timeconsuming.8 Algal separation or removal from water represents a major technological and economical barrier for both algaebased biofuel and water treatment industries. Magnetophoretic separation using magnetic particles draws an increasing attention due to the high separation efficiency and low operational cost.9−13 As magnetic particles adhere to the © XXXX American Chemical Society

algal cells, the magnetically modified algal cells could be effectively concentrated into compact slurry in the external magnetic field and rapidly separated from the bulk liquid.14 Magnetic nanoparticles (NPs) are particularly preferred because of the high specific surface areas. However, bare or naked NPs are often insoluble in water and undergo agglomeration and precipitation, thus reducing the separation effectiveness.15 To stabilize these colloidal particles in aqueous dispersion, surface coating that enables electrostatic and/or steric repulsion and reduces the mutual attraction of dispersed NPs is necessary and important. A diverse range of materials have been used for NP surface coatings in different applications, including lipids,16 dendrimers,17 proteins,18 carbohydrates such Received: June 19, 2014 Revised: December 5, 2014 Accepted: December 8, 2014

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Environmental Science & Technology as starch,19 humic acid,20−22 and polymers such as polyethylene glycol (PEG),23 polyacrylamide,24 and poly(diallyldimethylammonium chloride) (PDDA).4,25 Particularly, due to the inherent negative surface charge of algae, positively charged coating will likely bring about the electrostatic attraction between polymer-coated magnetic NPs and facilitate the adhesion of magnetic NPs to algal cells. For example, Fe3O4 NPs coated with PDDA (a cationic polymer) have demonstrated excellent performance in the algal harvesting efficiency for Chlorella sp.26 Moreover, Hu et al. observed that Fe3O4 particles coated with a cationic polymer, polyethlenimine (PEI), could also effectively separate Chlorella ellipsoidea under a magnetic field.27 In spite of the recent advances, the large-scale application of magnetophoretic algal separation is yet hampered by many technological and economic challenges in increasing the algal separation efficiency while lowering the cost. In this study, magnetite (Fe3O4) NPs (MNPs) were used as the core because they are nontoxic, earth abundant, inexpensive, and reusable.28 Moreover, MNPs have been extensively used as model particles for magnetophoretic algal separation.27,29 PEI will be used as the coating, which is a biocompatible polymer produced at industrial scales for different applications such as detergents, adhesives, and water treatment agents. The following questions were addressed: (1) we experimentally assessed how the PEI coating prevents agglomeration of MNPs, increase the harvesting efficiency of a model biofuel-producing algae, Scenedesmus dimorphus (S. dimorphus), and reduces the dose demand of MNPs; (2) the colloidal interactions between PEI-coated MNPs and algae were analyzed with the extended Derjaguin−Landau−Verwey− Overbeek (EDLVO) theory; (3) recently, UV irradiation was found to play a role in algae biocoagulation, and algal harvesting efficiency could be enhanced,30 whether UV irradiation can be combined with magnetophoretic separation as a noninvasive way to improve the biocoagulation of the magnetically modified algal cells was explored; (4) the operational mode and strengths of a magnetic field on algal harvesting were documented; and (5) the reusability of PEI solution and MNPs was demonstrated to potentially decrease the operational cost and increase the sustainability of magnetophoretic algal separation processes.

measured by DLS on a Zetasizer nano ZS instrument (Malvern Instruments, U.K.). X-ray Diffraction (XRD) was recorded for the crystallography using a Philips PW3040 X-ray Diffractometer. The BET surface area was measured with the Micromeritics AutoChem II 2920 equipped with a thermal conductivity detector (TCD). The polymer coating amount or density (mg·m−2) was measured by TPD with a Micromeritics AutoChem II 2920 system. Surface compositions were assessed by Fourier Transform Infrared (FTIR) and Raman Spectrometers. FTIR was performed on a Nicolet ThermoElectron FTIR spectrometer combined with a MIRacle attenuated total reflectance (ATR) platform assembly and a Ge plate, while Raman was carried out with a Thermo Scientific DXR Raman microscope using an argon ion laser excitation (λ = 514.5 nm) at powers of 2−10 mW. The UV−vis absorption spectra were obtained using a Thermo scientific Evolution 201PC spectrophotometer. Algae and Cultivation Conditions. S. dimorphus was cultivated in 2-L Erlenmeyer flasks at room temperature (25 ± 1 °C) with 5% CO2 at a rate of 8.5 × 10−4 L-CO2·min−1·(Lmedium) −1.31,32 The light-dark cycle (12 h/12 h) was maintained at a photon flux of approximately 1200 lx (27.4 μmoles·m−2·s−1 or 4200 mWatt·m−2) measured by a spectroradiometer (Spectral Evolution, SR-1100). The modified Bold’s Basal Medium (MBBM) used to cultivate the algae has the compositions reported elsewhere.30 The initial solution pH, dissolved oxygen (DO), oxidation−reduction potential (ORP) of the culture medium was 7.0 ± 1.1, 18 ± 2 mg·L−1, and 170 ± 31 mV, respectively. The algal concentration (g·L−1) was characterized by the dry cell weight (DCW) with the initial and final concentration of approximately 0.2 g·L−1 and 1.8 g·L−1, respectively. Magnetophoretic Algal Separation Experiments. When algae reached their maximal concentration, magnetophoretic separation experiments begun in 25-mL glass specimen bottles, where the algal suspension in the MBBM medium was first mixed with MNPs for 30 s to allow the biocoagulation between MNPs and algal cells.11 Then, a permanent magnet was placed next to the bottle to separate the MNP-coated algal cells for 3.0 min, as shown in Supporting Information (SI) Figure S5. Three indicators were used to evaluate the separation performance, including the algal harvesting efficiency (HE), recovery capacity (RC), and recovery efficiency (RE) were calculated as follows:12,33

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MATERIALS AND METHODS MNPs Synthesis and Characterization. MNPs was prepared by the chemical coprecipitation method.12 Briefly, 0.99 g FeCl2·4H2O and 2.7 g FeCl3·6H2O were dissolved into a flask vessel containing 100 mL DI water with vigorous stirring under nitrogen atmosphere at 80 °C, and then 10 mL NH4OH (25 wt %) was added into the above solution. The mixture was stirred continuously for 30 min, and the color of the solution changed gradually from light brown to black. The resulting magnetite was separated from the mixture using a NdFeB permanent block magnet (K&J Magnetics, Inc., Pipersville, PA) and washed 4 times with DI water. The final MNPs were concentrated and dispersed in DI water for further use. The concentration of MNPs were represented by the concentration of the total iron (Fe) determined by Agilent 7500i Benchtop Inductively Coupled Plasma-Mass Spectrometer System (ICPMS). The morphology and sizes of the MNPs were determined by a Hitachi H-7500 transmission electron microscope (TEM). Hydrodynamic size distribution (PSD) and zeta potential were

HE(%) = [1 − (C t /C0)] × 100%

(1)

⎡ ⎛ C / C ⎞⎤ RE(%) = ⎢1 − ⎜ t 0 ⎟⎥ × 100% ⎢⎣ ⎝ C t′/C0′ ⎠⎥⎦

(2)

RC(g‐algae· g‐MNPs−1) =

(C 0 − C t )V m

(3)

where C0 and Ct are the algal concentrations before and after separation (g·L−1), C0′ and Ct′ are the algal concentrations without addition of MNPs in the control group (g·L−1), V is the volume (20 mL) of algal suspension, and m is the mass of MNPs added (g). The magnetophoretic separation was studied by varying the PEI coating on MNPs surface, the MNPs dose, the UV irradiation, and the external magnetic field strength with the details in the following. Effect of Surface Coating. 10% (w/w) PEI ((CH2 CH2NH)n, Mw ≈ 25 000 g·mol−1) was purchased from B

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Statistical Analysis. All experiments were carried out at room temperature of 25 ± 3 °C with triplicate sampling and testing. The presented results are mean values ± standard deviation from three independent experiments. The differences in HE, RE, and RC between test groups, and the control groups were tested for significance using one way analysis of variance (ANOVA) at a significant level of 0.05.

Sigma-Aldrich for surface coating of MNPs. The mass ratios (gPEI·g-MNPs−1) between PEI and MNPs varied from 0.1, 0.2, 0.4, 0.8, to 1.2 by adding different amounts of MNPs into a PEI solution of 200 mg·L−1 for the 20 min stabilization time. The mixture was moved to the magnet for 10 min to separate the PEI-coated MNPs, which were washed with DI water three times to remove loosely attached or the residual PEI. The PEI coating on MNPs was quickly indicated by the zeta potential changes using DLS. The exact surface adsorption quantity of PEI was evaluated by measuring the residual PEI concentration in the discarded solution (see details in the SI) and the TGA method. Subsequently, different amounts of naked or PEIcoated MNPs were applied to the suspension of S. dimorphus at approximately 1.0 g-DCW·L−1 to achieve the different mass ratios (0.05:1, 0.1:1, 0.2:1, 0.4:1, 0.8:1, and 1.2:1 g-MNPs·galgae−1), and PEI addition only was also done as the control. Effect of UV Irradiation. Two UV lamps at 254 and 365 nm with two different intensities (e.g., 1300 and 2600 μW· cm−2) were used to study the UV irraditon effects on the algal separation. The irradiation intensity was varied by adjusting the distance between the UV lamp and the surface of algal suspension. The naked and PEI-coated MNPs were applied at the optimal dose determined above. The control experiments without UV irradiation (but with addition of MNPs) were also performed. Effect of External Magnetic Field. The magnetic field was applied at both continuous and pulsed modes to study the role of magnetic field on the separation efficiency. In the continuous application, the magnet was placed at different distances away from the specimen bottle to achieve various magnetic strengths (e.g., 100 mT, 50 mT, and 20 mT). In the pulsed mode, the magnetic field was switched on and off for 1 min respectively for two times at the same magnetic strengths as used above. The magnetophoretic separation experiments for this study involved no UV irradiation. Assessment of MNPs Reuse. To collect MNPs from the concentrated algal biomass, the MNPs-algae slurry (approximately 1.7 g-algae·L−1 in 10 mL) were agitated for 5 min using the sonicator at 500 W (Sonic dismembrator 500, Fisher Scientific, U.S.) in the ice bath. MNPs were further separated from algal biomass by placing the 10-mL slurry close to the magnet for 2−3 min. A majority of MNPs was expected to detach from algae and attracted onto the bottom of the container by the magnet. The fluid slurry containing the majority of algae and a small fraction of MNPs was discarded (approximately 1.6 g-algae·L−1 in 9.8 mL). The collected MNPs were then washed at least three times with DI water, followed by the same magnetic separation for purification. The concentration of purified MNPs dispersed in DI water was quantified by ICP-MS to determine the recovery efficiency. Finally, the regenerated PEI-coated MNPs were reused in harvesting algae and algal harvesting efficiencies in terms of HE, RE, and RC were analyzed and compared with those obtained with freshly prepared MNPs. Colloidal Interactions. The EDLVO theory was used to compute the interaction energies for three types of interactions (e.g., MNPs−MNPs, MNPs−algae, and algae−algae). van der Waals attraction, electrostatic repulsion, magnetic, and steric and bridging forces contributed by adsorbed PEI polymer chains were considered. The relevant equations for computing the total interaction energies are provided and discussed in detail in SI Sections S4 and S5.

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RESULTS AND DISCUSSION Physicochemical Surface Properties of MNPs. TEM images of the naked and PEI-coated MNPs are shown in Figure 1a,b, which indicates that the MNPs are spherical in shape with

Figure 1. TEM of the (A) naked MNPs, (B) PEI-coated MNPs, (C) naked MNPs with S. dimorphus, and (D) PEI-coated MNPs with S. dimorphus. Freshly made MNPs dispersed in solution were directly deposited onto the TEM grid.

a relatively uniform morphology and size. The large clusters or aggregates formed when MNPs were mixed with algae as shown in Figure 1c,d. The average diameter of naked MNPs was statistically determined to be of 8.8 ± 1.9 nm with the TEM counting technique (SI Figure S1), however, the hydrodynamic size distribution determined by DLS ranged roughly from 300 to 600 nm and were considerably larger than the TEM size distribution, which was a common observation reported previously.34−36 In general, it was the primary particle size of MNPs that was obtained from TEM; hence if particles do form aggregates or clusters in solution, this would result in the increased dimensions measured via DLS. Another possible reason for the difference was that the polymer coating and electric double layer (considerable for our highly charged particles) surrounding the particles were taken into account in the calculation of hydrodynamic diameters. Other physicochemical characterizations such as FTIR, XRD, Raman spectrum, and UV−vis are detailed in SI Figures S2 and S3. As shown in Figure 2a, the zeta potentials of S. dimorphus are negative at a wide pH range and approach approximately −40 mV at the neutral and alkalic pHs. By contrast, naked MNPs were positively charged at the pHs less than 6.0 and became C

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Figure 3. Harvesting efficiencies (HE) of S. dimorphus as a function of the mass ratio of MNPs to algae under room light. The initial algal concentation was 1.0 g·L−1. The magnetic field strength is 100 mT.

respectively. By contrast, the biocoagulation with only PEI addition into the algal suspension at a dose of 0.6 g·L−1 (the maximal relevant PEI concentration achieved with the application of PEI-coated MNPs into the algal suspension) was not substantially improved (results not shown), indicative of the critical roles (e.g., increasing available surface areas for interactions) of MNPs in this biocoagulation process. Obviously, the PEI coating enhanced the binding between MNPs and algal cells, and thus improved the magnetophoretic separation. More importantly, with PEI coating, the dose demand to achieve the same high HE was significantly reduced (half of that for naked MNPs). It was reported that the surface modification of magnetic NPs with special block copolymers could manipulate the surface properties such as surface charge, hydrophobicity and even addition of chelating/complexation moieties.21,37 In this study, the improved magnetophoretic separation of S. dimorphus cells can be mainly attributed to the positive surface charge brought by PEI coating, resulting in the promotion of the attachment of MNPs with the negatively charged algae cells. Furthermore, the TEM images in Figure 1 clearly displayed the surface layer of PEI polymers, which could capture algae cells via the netting or bridging mechanism.38,39 Effects of UV Irradiation. Figure 4 compares three indicators (HE, RE, and RC) of algal separation performance with addition of naked or PEI-coated MNPs under UV irradiation. Compared with the control group (no UV irradiation), all the HEs under UV irradiation significantly increased for both naked and PEI-coated MNPs. Particularly, the highest HE for naked MNPs was 85.0 ± 0.1% under UV365 irradiation at 2600 μW·cm−2, followed by 82.9 ± 0.1% under UV254 irradiation at 2600 μW·cm−2, 81.6 ± 0.1% under UV365 irradiation at 1300 μW·cm−2, and 80.0 ± 0.1% under UV254 irradiation at 1300 μW·cm−2, which was consistent with data for PEI-coated MNPs. Apparently, higher UV light intensity led to better magnetophoretic algal separation. Moreover, the UV365 irradiation tended to be more effective than UV254, probably because the MNPs-algae mixture likely adsorbed more light energy at larger wavelengths, as evidenced by the UV−vis spectra in SI Figure S3d. The increase of RE and RC in the presence of UV followed the similar patterns with HE. For instance, the RC values for PEI-coated MNPs under UV365 irradiation at 2600 μW·cm−2 reached 5.6 ± 0.1 g-algae·g−1MNPs, which was much greater by 13.7% than that of naked MNPs, and those RC values under other UV irradiation conditions (by 4.76% for UV365 irradiation at 1300 μW·cm−2, 3.25% for UV254 irradiation at 2600 μW·cm−2, and 8.06% for UV254 irradiation at 1300 μW·cm−2.). The obtained RC values,

Figure 2. (a) Zeta potentials of naked, PEI-coated MNPs (at a mass ratio of 0.4), and S. dimorphus in algal medium at differetn pHs. (b) zeta potential changes of MNPs with the PEI coating at different mass ratios in DI water at pH = 7.0.

negatively charged at the pHs above 7.0. Moreover, the zeta potentials of algae or MNPs remained the same when they were dispersed in MBBM culture medium, which had a solution pH of 7.0 and the ionic strength of approximately 0.0134 M. As expected, the cationic PEI coating clearly imposed the dramatically positive charge on MNPs. Particularly, the zeta potentials of S. dimorphus and naked MNPs in the medium (pH = 7.0 ± 0.3) were −38.5 ± 3.8 and −7.9 ± 2.0 mV, respectively, whereas the PEI-coated MNPs at a PEI-to-MNP mass ratio of 0.4 had 35.1 ± 2.5 mV, implying that the PEI-coated MNPs were more likely to attach to algae cells owing to the electrostatic attraction compared to naked MNPs. Figure 2b shows that with the increase of PEI coating, the zeta potentials of PEI-coated MNPs gradually became more and more positive from −8.0 ± 2.4 to 35.1 ± 2.5 mV, which is the maximum level when the mass ratio reached 0.4 or greater. Thus, for the following experiments, the PEI coating on MNPs was prepared at the mass ratio of 0.4 g-PEI g-MNPs−1. As discussed in SI Section S3, the adsorbed quantity of PEI on MNPs was 0.35 gPEI·g−1-MNPs, which is slightly lower than 0.4 g-PEI·gMNPs−1 (the nominal mass ratio). In addition to the positive surface charge, the PEI coating substantially increased the colloidal stability and prevented the agglomeration of MNPs in dispersion. Without PEI coating, MNPs aggregated rapidly as the mean hydrodynamic diameter of MNPs gradually increased from 100 nm to 1 μm (SI Figure S1) and black precipitates were observed at the bottom of the container. The PEI-coated MNPs, however, showed significantly enhanced stability against aggregation, as evidenced by a constant mean hydrodynamic diameter of around 60 nm during the experimental period. Effects of Surface Coating. Figure 3 indicates that the HE of S. dimorphus cells increased with the increase of the mass ratio between the both naked or PEI-coated MNPs and algae. The maximal levels of HE achieved by naked MNPs and PEIcoated MNPs were approximately 80.3 ± 1.4% and 82.7 ± 1.0%, when the mass ratio exceeded 0.2 and 0.1 g·g−1, D

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Figure 4. Comparisons of harvesting efficiency (HE, %), recovery efficiency (RE, %) and recovery capacity (RC, g-algae·g−1 MNPs) of S. dimorphus under various irradiation for the naked (a) and PEI-coated MNPs (b). Two UV-light intensities (2600 μW·cm−2 and 1300 μW· cm−2) were tested, denoted as UV-A and UV-B, respectively. The MNP dose was 0.2 for naked MNPs and 0.15 g·g−1 for PEI-coated MNPs) with the initial algal concentration of 1.0 g·L−1. The magnetic field strength is 100 mT. *denotes significant difference in comparison with the control values (p < 0.05).

Figure 5. Comparisons of computed HE, RE, and RC of S. dimorphus under different conditions. Control group: naked or PEI-coated MNPs and S. dimorphus; M1, M2, and M3 refer to the application of the continuous magnetic fields of 100 mT, 50 mT, and 20 mT, respectively. M4, M5, and M6 are the application of the pulsating magneitc fields at the above three intensities with 1 min on and off. The MNP dose was 0.2 for naked MNPs and 0.15 g·g−1 for PEI-coated MNPs) with the initial algal concentration of 1.0 g·L−1. No UV irradiation was provided. *denotes significance in comparison to control values (p < 0.05).

particularly, were comparable with the reported values elsewhere (e.g., 5−93 g-algae·g−1-MNPs for different interacting MNPs and algae12,26,27). However, the MNPs or algal suspensions alone were observed to be stable under the same UV irradiation (no enhanced agglomeration or precipitation), indicating that UV irradiation did not affect homoaggregation of MNPs or algal cells. The enhanced performance of magnetophoretic algal separation in the presence of MNPs and UV irradiation might be attributed to the changes in surface characteristics on algae cells. First, surface attachment of MNPs may lead to the changes to surface charge and other physicochemical properties of algae.40 This is supported by the zeta potential shift from −38.5 ± 3.8 to −0.1 ± 0.6 mV for algae after mixing with PEIcoated MNPs. Second, as magnetite (F3O4) NPs are a semiconductor material with the band gap of 2.2−2.3 eV, which is less than the photoenergy (3.3−4.9 eV) of UV365 or UV254. Thus, the photoexcitation could occur under UV irradiation, leading to the generation of reactive oxygen species (ROS) on the surface MNPs.41,42 ROS such as superoxide anion, hydroxyl radicals, or singlet oxygen could nonselectively oxidize organic materials and subsequently alter the cell surface properties.41,42 Consequently, the MNP-algae or algae−algae interactions would be changed. Additionally, extracellular organic matter (EOM) such as proteins, polysaccharides, nucleic acids, and lipids released from algae cells might react with ROS. A high EOM level usually resulted in a lower bioflocculation rate of algae compared to that in the absence of EOM.43,44 The photooxidation or chemical oxidation of EOM in the aqueous medium by ROS may also be one of the potential drivers for enhanced algal harvesting efficiency under UV irradiation. Effects of External Magnetic Field. The influences of magnetic field strength and application modes (continuous or intermittent) on algal separation are indicated in Figure 5 by the values of HE, RE, and RC for both naked and PEI-coated MNPs added into the S. dimorphus suspension. In the control groups (without placing the permanent magnet), the HE, RE

and RC reached only approximately 51.9%, 43.4% and 3.1 galgae·g−1-MNPs, respectively, for naked MNPs, whereas for PEI-coated MNPs they were 59.9%, 53.3%, and 3.5 g-algae·g−1MNPs, respectively. By contrast, in the presence of the external magnetic field, the separation performance was improved and the efficiencies almost linearly increased with the exposed magnetic field strength from 20 to 100 mT. Under the continuous magnetic field of 100 mT, the greatest harvesting efficiencies were obtained with PEI-coated MNPs (97.3 ± 2.1% of HE, 96.8 ± 2.5% of RE, and 5.8 ± 0.1 g-algae·g−1-MNPs, respectively). However, the alternating or pulsating magnetic field exposure led to slightly lower separation efficiencies compared with the case of the continuous magnetic fields. In addition, the magnetic field alone without addition of MNPs could hardly separate the algal cells due to the minimal magnetic susceptibility between algae and the culture medium (results not shown).26 Interaction Energy Analysis Using EDLVO Theory. Figure 6 compares the total interaction energies for the naked and PEI-coated MNPs indicated that no energy barrier existed between naked MNPs, whereas a pronounced energy barrier was present between PEI-coated MNPs. The interaction energy barrier on PEI-coated MNPs was clearly attributed to the electrostatic and polymer steric repulsion. For naked MNPs, the attractive forces of van der Waals and magnetic forces were greater than the electrostatic repulsive force, which resulted in a net interparticle attraction and negative interaction energy. Our DLS measurement showed that naked MNPs tend to aggregate faster in water suspension than PEI-coated MNPs, which agreed with the EDLVO prediction. Likewise, a significant energy barrier was present between algal cells themselves as shown in the inset, implying that algal suspension could be rather stable and do not undergo spontaneous biocoagulation with themselves.45 This prediction was also in agreement with our observation of no apparent homoaggregation or sedimentation for algal suspension for the experimental period of time. E

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ASSOCIATED CONTENT

S Supporting Information *

Additional information including characterizations and analysis using TEM, XRD, TPD, FTIR, Raman, UV−vis, and EDLVO, Tables S1−S3, and Figures S1−S6. This material is available free of charge via the Internet at http://pubs.acs.org.

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AUTHOR INFORMATION

Corresponding Author

*Phone: 1-973-596-5520; fax: 1-973-596-5790; e-mail: [email protected]. Notes

The authors declare no competing financial interest.

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Figure 6. Total interaction energy as a function of the separation distance between different interacting entities: (a) Naked MNPs-tonaked MNPs, (b) PEI-coated MNPs-to- PEI-coated MNPs, (c) Naked-MNPs-to-algae, and (d) PEI-coated MNPs-to-algae, with the inset of (e) Algae-to-algae. The simulated interaction occurred in algal medium with pH of 7.0 and the ionic strength of approximately 0.0134 M.

ACKNOWLEDGMENTS This study was supported by the Research Startup Fund at NJIT and National Science Foundation Grant CBET-1235166.

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There appeared to be no energy barrier between algae and naked or PEI-coated MNPs. However, the primary minimum for the ineraction between algae and PEI-coated MNPs was more negative than that between algae and naked MNPs. Clearly, with the PEI coating, there was a greater energy release from the adsorption of PEI-coated MNPs on algae and thus a higher harvesting efficiency was achieved in the presence of PEI coating. Challenges and Sustainability in Large-Scale Applications. The presented magnetophoretic separation technology provides a rapid and high efficient way for algal harvesting or removal in biomass engineering or environmental applications. But whether this technology can be developed in a sustainable and “green” manner and whether it can be implemented in industrial scales or worldwide deserves more research. Of the numerous critical challenges that must be overcome, increasing the economic viability or lowering the operational and manufacturing cost of MNPs is important for securing the sustainability of this technology and reducing our resource consumption. Our strategies are reducing the dose demand of MNPs by a cationic polymer coating as well as the reuse of MNPs, which is discussed in SI Section S7. Cost effective use of magnetic particles will not only improve the process economic viability, but also mitigate the negative impacts on the downstream lipid extraction or the natural environment. Nevertheless, to date, a few studies attempted to develop green methods that avoid the use of hazardous chemicals (e.g., acid or base) in the recovery of MNPs.11,14,46 In addition to the low MNPs dose demand and the reuse of MNPs, the magnetophoretic separation can also prove to be more sustainable, if earth abundant or renewable materials are employed.9−13 Our results indicated that UV irradiation could appreciably increase the magnetophoretic algal harvesting efficiency. Since the sunlight consists of UV radiation at a comparable order of magnitude (∼5 mW·cm−2) as we used in the experiment, the solar irradiation as a renewable energy source will be not only integral for algae growth, but also potentially useful for large scale algal harvesting in magnetophoretic algal separation processes. F

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DOI: 10.1021/es5049573 Environ. Sci. Technol. XXXX, XXX, XXX−XXX