Treatment of reverse osmosis concentrate using an algal-based MBR combined with ozone pretreatment

Treatment of reverse osmosis concentrate using an algal-based MBR combined with ozone pretreatment

Water Research 159 (2019) 164e175 Contents lists available at ScienceDirect Water Research journal homepage: www.elsevier.com/locate/watres Treatme...

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Water Research 159 (2019) 164e175

Contents lists available at ScienceDirect

Water Research journal homepage: www.elsevier.com/locate/watres

Treatment of reverse osmosis concentrate using an algal-based MBR combined with ozone pretreatment Hyoungmin Woo a, Hee Sung Yang b, Thomas C. Timmes c, Changseok Han d, Joo-Youn Nam e, Seokjong Byun f, Sungpyo Kim g, Hodon Ryu a, Hyun-Chul Kim h, * a

United States Environmental Protection Agency, Office Research and Development, 26 W. Martin Luther King Dr., Cincinnati, OH 45268, USA Department of Environmental Engineering, University of Seoul, Seoul 02504, Republic of Korea Department of Civil and Environmental Engineering, Virginia Military Institute, Lexington, VA 24450, USA d Department of Environmental Engineering, Inha University, Incheon 22212, Republic of Korea e Jeju Global Research Center, Korea Institute of Energy Research, Jeju-do 63357, Republic of Korea f Department of Research and Development, Jeollanamdo Environmental Industries Promotion Institute, Jeollanam-do 59205, Republic of Korea g Department of Environmental Engineering, College of Science and Technology, Korea University, Sejong 30019, Republic of Korea h Research Institute for Advanced Industrial Technology, College of Science and Technology, Korea University, Sejong 30019, Republic of Korea b c

a r t i c l e i n f o

a b s t r a c t

Article history: Received 5 February 2019 Received in revised form 9 April 2019 Accepted 1 May 2019 Available online 2 May 2019

Algal treatment was combined with ozone pretreatment for treatment of synthetic reverse osmosis concentrate (ROC) prior to microfiltration. The research mainly focused on minimizing the fouling of polyvinylidene-fluoride membranes and maximizing the restoration of membrane permeability. The algal treatment alone was only moderately effective for the mitigation of fouling in microfiltration, while a markedly improved performance was achieved when the algal treatment followed ozonation. The combination of ozonation and algal treatment reduced membrane permeability decline and significantly (p < 0.05) increased the reversibility of fouling after hydraulic washing. A longitudinal evaluation was also performed with a goal of achieving a robust removal of contaminants. Ozonation followed by algal treatment was very effective in attenuating both caffeine and carbamazepine, as well as removing organic matter and inorganic nutrients from ROC in a single bioreactor. In this study, an alkaline condition (~pH 12), produced by microalgae in the light without supplemental aeration was applied for insitu cleaning of fouled membranes. The result showed that the algal-induced cleaning successfully restored the permeability of organic-fouled membranes during the filtration of both raw and algaltreated ROC. This in-situ strategy offers a novel option for periodic cleaning of fouled membranes while maintaining operational simplicity, especially for existing submerged membrane filtration facilities. © 2019 Elsevier Ltd. All rights reserved.

Keywords: Reverse osmosis concentrate Ozonation Microalgae Microfiltration Fouling

1. Introduction Reverse osmosis (RO) technology is increasingly adopted for the tertiary treatment and indirect reuse of secondary effluent from municipal wastewater treatment plants. The concentrate, resulting from the filtration processes, remains a challenge to treat prior to discharge to the aquatic environment primarily due to the volume

* Corresponding author. E-mail addresses: [email protected] (H. Woo), [email protected] (H.S. Yang), [email protected] (T.C. Timmes), [email protected] (C. Han), [email protected] kier.re.kr (J.-Y. Nam), [email protected] (S. Byun), [email protected] (S. Kim), [email protected] (H. Ryu), [email protected] (H.-C. Kim). https://doi.org/10.1016/j.watres.2019.05.003 0043-1354/© 2019 Elsevier Ltd. All rights reserved.

and the quality of the direct discharge (Joo and Tansel, 2015; Subramani and Jacangelo, 2014). In South Korea, for instance, the concentrate can be further treated and discharged directly to surface water in compliance with the wastewater treatment plant discharge permit. Reverse osmosis concentrate (ROC) typically contains high concentrations of inorganic salts and organic compounds including persistent organic matter and a broad range of trace organic compounds (TOrCs), which are removed with varying success during secondary treatment (Knopp et al., 2016). Due to their recalcitrance to microbial degradation, various integrated treatment strategies combined with complementary technologies for removing the compounds have been considered and investigated to minimize the adverse impacts on the aquatic environment

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Nomenclature COD EEM EfOM EPS FTIR HPI HPO HRT MBR MF

chemical oxygen demand excitation-emission matrix wastewater effluent organic matter extracellular polymeric substances Fourier transform infrared hydrophilic hydrophobic hydraulic retention time membrane bioreactor microfiltration

that are associated with the direct surface discharge of ROC. These strategies generally focused on reducing the organic pollutant loading into the environment from wastewater treatment facilities rez (Jamil et al., 2015; Lee et al., 2009a, 2009b; Liu et al., 2012; Pe et al., 2010; Radjenovic et al., 2011; Umar et al., 2016b), which typically include biological stabilization, physicochemical solute separation, and photocatalytic or electrochemical advanced oxidation. Likewise, Zhou et al. (2011) investigated several oxidation processes at a bench-scale level and demonstrated their effectiveness in increasing both the removal of organic contaminants and the biodegradability of organic residues. A similar conclusion using highly saline ROC was also drawn by Umar et al. (2016a). These previous observations indicate that the combination of bioremediation and physiochemical treatment is desirable for further removal of biodegradable fractions and inorganic nutrients prior to surface water discharge, despite the possible production of more complex and toxic by-products in some cases from chemical oxidation. To date, the authors have screened diverse algal species to determine their adaptability in the context of phycoremediation, selected the best candidate based on several criteria, and applied to the treatment of a wide range of refractory wastewaters (Kim et al., 2014d). In the latest work, the authors have demonstrated that the treatment of synthetic ROC with Scenedesmus quadricauda is highly feasible to remove inorganic nutrients, reduce enteric bacteria, and degrade TOrCs (Maeng et al., 2018b). Similarly, other studies corroborated the effectiveness of algal-mediated treatment on the removal of inorganic nutrients, organic components, metallic ions, and emerging contaminants from a wide range of wastewaters including actual ROC (Rawat et al., 2016; Wang et al., 2016). The separation of biosolids is essential prior to the direct discharge of algal treated ROC to meet the regulatory standard or to further minimize the volume of concentrate prior to disposal. Membrane processing is one of the most common techniques used in liquid/ solid separation for a wide range of wastewaters. Particularly, the membrane bioreactor (MBR) is a highly-promising technology for the treatment of organic-rich wastewater and is beneficially combined with photobioreactors for microalgae cultivation and wastewater treatment (Liao et al., 2018). The membrane photobioreactor (MPBR) remove organic carbon in MBR in parallel to reduce nutrients in photobioreactor. While the submerged MPBRs have focused on the cultivation of algal biomass with a primary goal of harvesting a high density of feedstocks for the production of bioenergy and value-added materials, limited attention has been given to the treatability of wastewater and the associated impacts on membrane fouling (Luo et al., 2017). The use of membranes is typically limited by fouling which decreases permeability and in extreme cases can result in a loss of membrane integrity (membrane failure).

MPBR OD680 PES PVDF RO ROC SEM SMP SRT TN TOrCs TP

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membrane photobioreactor optical density at 680 nm polyethersulfone polyvinylidene fluoride reverse osmosis reverse osmosis concentrate scanning electron microscopy soluble microbial products solids retention time total nitrogen trace organic compounds total phosphorus

The mechanisms of fouling in MPBRs are similar to those observed in conventional MBRs (Low et al., 2016). Fouling can be caused by biological growth, by the deposition of inorganic precipitates or particles on or within the membrane pores, or by the physicochemical attachment of organic matter (Kim and Dempsey, 2013). It is generally agreed that the impact of algal cells on membrane fouling is lower than that of algal-derived organic matter (Qu et al., 2012). Organic matter secreted by algal cells working at MPBRs can be categorized as wastewater effluent organic matter (EfOM) with similarities to extracellular polymeric substances (EPS) and soluble microbial products (SMP) found in MBRs with respect to their characteristics and fouling behaviors. Various organic constituents of wastewater effluent have been suggested as important causes of fouling in low-pressure membrane filtration. Humic-like substances (polymerized organic matter) (Ayache et al., 2013; Kim and Dempsey, 2012; Shon et al., 2006), protein-like substances (Fan et al., 2008; Wang et al., 2011), and hydrophilic polysaccharide-like substances (Zhu et al., 2010) have been implicated as dominant organic foulants in EfOM. The fractional composition of the EfOM can be affected by both the characteristics of the influent wastewater and the performance of the reclamation processes. Humic-like substances are usually derived from transformations of organic matter in biological treatment processes. Dextran has been frequently used as a model surrogate for polysaccharide-like substances present in secondary effluent (Contreras et al., 2009). In this study, we focus on the membrane fouling by EfOM commonly referred as EPS and SMP derived from biological activities in wastewater treatment. Many attempts have been made to either minimize fouling or maximize the restoration of membrane permeability, which include surface hydrophilization of membranes, optimization of operational parameters, manipulation of algal biomass properties, and physicochemical cleaning of fouled membranes (Liao et al., 2018). Pretreatment of feed water ahead of algal treatment is also applicable for improved membrane filtration performance. This study utilized ozone for that purpose. Ozonation also tends to increase the hydrophilicity and biodegradability of organic matter, and only small portions of the organics can be completely mineralized (Kim et al., 2014c). Pretreatment of feed water using oxidation techniques was found to effectively reduce membrane fouling and cake resistance during algal filtration (Heng et al., 2008; Hung and Liu, 2006; Zhang et al., 2015), while the combination of algalbased MBR and ozone pretreatment is very scarce and is still in their infancy. Despite considerable research efforts and major advances in technology, membrane fouling can only be decelerated, as it will eventually happen, and requires physicochemical cleaning to restore flux. A systematic cleaning approach has not been established and thus further efforts are needed to develop the most costeffective cleaning protocol and restoration approaches for different

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types of membrane materials (Liao et al., 2018). The objective of this research was to investigate an algal-based MBR combined with ozone pretreatment to achieve the following goals during the treatment of saline ROC: (1) mitigated flux decline and enhanced permeability recovery; (2) operational simplicity in the cleaning of fouled membranes; (3) robust removal of COD, TN, and TP in a single continuous-flow bioreactor; (4) a better understanding of how mixotrophic algal species work on wastewater remediation and membrane cleaning in the light. S. quadricauda has been employed for consistent removal of contaminants in a single compartment system with continuing light. Thus, the main hypothesis to be tested was that ozone pretreatment could mitigate membrane fouling and so increase process efficiency when treating ROC with the microalga in the light. This study also investigated a novel alternative method to restore the permeability of organicfouled membranes using an in-situ cleaning strategy forgoing the use of caustic chemicals. We evaluated the applicability of using ozone and microalgae for treatment of saline ROC prior to microfiltration (MF). This evaluation emphasized achieving the robust removal of organic matter, inorganic nutrients, and TOrCs while concurrently reducing fouling of polyvinylidene fluoride (PVDF) MF membranes. Ozone alone may be effective in decreasing fouling in MF, but this hypothesis was not explored in this study as ozonation is not a stand-alone technique for removing nutrients. The membrane performance was quantified by determining the permeability decline and the fouling reversibility (flux recovery) after cleanings. Various advanced analytical tools were employed to determine the viability of algal cells as bioagents during ROC treatment, to investigate the fate of organic compounds through the treatment of ROC, and to characterize the physicochemical properties of foulants retained on the surface of membranes. 2. Materials and methods Experiments were conducted in three phases: (1) HPO and HPI PVDF MF membranes were examined to investigate the reversibility of organic fouling after chemical and algal-induced cleanings; (2) HPI PVDF MF was selected for additional tests including the effects of ozonation and subsequent algal treatment on MF performance (flux decline in filtration and permeability recovery after cleaning); (3) an algal-based MBR was constructed and then combined with ozone pretreatment for evaluation of contaminant removal and hydraulic resistance to filtration during continuous treatment of ROC. 2.1. Synthetic ROC All chemicals used in this study were of analytical grade and were supplied by Sigma-Aldrich (St. Louis, MO, USA). Synthetic ROC was prepared as previously described (Supporting Information Table S1 and Fig. S1) (Maeng et al., 2018b) and the pH ranged between 7.3 and 7.5 (Orion Star A215, Thermo Scientific, USA). Unless specified otherwise, all experiments used synthetic ROC prepared by blending 30% humic acid and 70% dextran (15e25 kDa) based on the findings reported by Vakondios et al. (2014). The organic concentration was approximated as chemical oxygen demand (COD). The COD, total nitrogen (TN), and total phosphorus (TP) in the synthetic ROC ranged from 97 to 120 mg L1, 29e34 mg L1, and 10e13 mg L1, respectively. Dichromate, persulfate digestion, and acid persulfate digestion methods were employed to measure the COD, TN, and TP in the water samples using a DR/5000 spectrophotometer (Hach, USA). The water samples were manually filtered with hydrophilic 0.22 mm polyethersulfone (PES) microfilters prior to measuring the water quality parameters (Kim, 2015). Each measurement was carried out at least in triplicate, and the average

and standard deviation values were reported. The final concentrations of organic and inorganic components in the synthetic ROC were selected based on the previously reported observations with an actual ROC from municipal wastewater treatment plants (Badruzzaman et al., 2009; Hurwitz et al., 2014; Lee et al., 2009a; Umar et al., 2016b; Zhou et al., 2011). In some experiments, caffeine and carbamazepine were added to the synthetic ROC. A diluted mixture of both chemicals was prepared using their stock solutions and spiked into the ROC. The concentrations of caffeine and carbamazepine determined in the prepared ROC were 44.9 ± 2.2 mg L1 and 56.7 ± 1.5 mg L1, respectively. TOrCs have been detected at concentrations higher than 80 mg L1 in actual ROC (Urtiaga et al., 2013) and therefore our initial TOrC levels were deemed appropriate for these experiments. The physicochemical properties of these selected compounds have been reported in detail elsewhere (Kim et al., 2015). Carbamazepine and caffeine were analyzed using an Agilent 1200 highperformance liquid chromatograph, and mass spectrometry detection was performed on an Agilent 6460 triple-quadrupole mass spectrometer equipped with a dual jet stream electrospray ionization source (Supporting Information Fig. S2). The details have been described in our previous work (Maeng et al., 2018b). 2.2. Strain and cultivation The S. quadricauda strain (AG 10003) was obtained from the Korea Collection for Type Culture in the Korea Research Institute of Bioscience and Biotechnology (Jeongeup, South Korea). The stock culture of S. quadricauda was grown in 2 L flasks containing 1.5 L of sterilized BG-11 medium (Rippka et al., 1979) in air enriched with 5% CO2 under continuous white fluorescent light illumination (75 mmol photons m2 s1) at 25  C (Kim et al., 2016). The light intensity was determined using an MQ-500 quantum meter (Apogee Instruments, Inc., USA). The cell growth was monitored using fluorescence-based flow cytometry. The analysis was immediately carried out using a Partec CyFlow® Cube6 flow cytometer € rlitz, Germany) equipped with a 20 mW blue (Partec GmbH, Go diode-pumped solid-state laser emitting at 488 nm. All collected fluorescence data were processed using the FCS4 Express Cytometry software (De Novo Software, Glendale, CA). Additional details on the procedures for counting intact cells and determining cell viability have been described in our previous publication (Maeng et al., 2018a). The cellular density was also monitored by determining the optical density (OD) of algal suspension. The cellular suspension was scanned in the wavelengths from 400 nm to 800 nm using a DR/5000 spectrophotometer, and the OD at 680 nm showed a good correlation (R2 ¼ 0.9972) with cell counting (Supporting Information Fig. S3) (Moheimani et al., 2013). 2.3. Treatment of ROC prior to microfiltration 2.3.1. Algal treatment Batch experiments with the closed system were conducted to determine the filterability of algal-treated ROC in MF. The algal cells in the exponential growth phase were collected via centrifugation (1620 g, 10 min), washed by mineral bottled water, and inoculated at four different cell concentrations (0.4, 0.8, 1.2, and 1.6 cm1 as OD680) into flasks containing 800 mL of synthetic ROC. The flasks were incubated under continuous light illumination with the intensity of 150 mmol photons m2 s1 at 25  C while shaking at 130 rpm for 24 h (Kim et al., 2014b). The flasks were aerated with a gas mixture of 95% air and 5% CO2 at a flow rate of 40e50 mL min1 (Raeesossadati et al., 2015). The flasks were then allowed to settle for 1 h and supernatant was filtered using 1.2 mm glass-fiber filters (GF/ C, Whatman, USA). The filtrate was used in dead-end filtration tests

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(as described in section 2.4). Based on membrane permeability and light availability, an optimal algal concentration (OD680 ¼ 0.80 ± 0.05 cm1) was selected for further algal treatment. 2.3.2. Ozone pretreatment Three different doses of O3 (0, 1, and 2 mg-O3 mg-C1) were examined for the treatment of ROC prior to algal treatment. The apparatus and method of ozonation have been reported in detail elsewhere (Kim et al., 2014c). Under the identical cultivation conditions as described above, ozonated ROC was treated with fresh algal biomass at initial OD680 of 0.80 ± 0.05 cm1 for 24 h. For raw ROC, the algal treatment continued for up to 48 h. The algal biomass was removed immediately after the algal treatment, and the liquid sample was used in dead-end filtration tests. The final pH ranged between 7.8 and 8.2 for all experiments. Unless otherwise stated, the temperature of synthetic ROC was kept at room temperature (z25  C). The fluorescence spectra of organic matter in raw and treated ROC were collected using a Shimadzu RF-5301PC fluorescence spectrometer with a 150 W xenon lamp source. All liquid samples were filtered (0.22 mm) and diluted with a carbon-free electrolyte solution to a concentration of 1 mg C L1 prior to the spectroscopic analysis. The spectra were concatenated into an excitationemission matrix (EEM). The analytical conditions have been reported in detail elsewhere (Kim et al., 2016). 2.4. Dead-end filtration and characterization 2.4.1. Membranes Flat-sheet hydrophilic (HPI) PVDF MF membranes (GVWP04700, Durapore, MilliporeSigma, USA) were used for all dead-end filtration tests. In some experiments, hydrophobic (HPO) PVDF MF membranes (GVHP04700) were used for comparative examination in parallel with the HPI PVDF MF membranes. PVDF has been comprehensively used as a porous membrane material in many public and industrial fields due to its excellent resistant capabilities to harsh environments for acids, alkaline, oxidants, and halogens (Kim et al., 2014a). The specifications of the examined membranes are shown in Table 1. 2.4.2. Dead-end filtration Flat-sheet membranes with a diameter of 44.5 mm were obtained by cutting MF membranes with subsequent adaptation to the filtration module. Membranes were wetted in methanol and were soaked in deionized water overnight before use. A dead-end filtration system was used to determine the flux decline as a function of specific permeate volume. The pre-wetted membrane was placed in a 50 mL commercial filtration cell (Amicon Cat. # UFSC05001, MilliporeSigma, USA), providing an effective filtration area of 13.4 cm2. The sample solution from an 800 mL pressure vessel (Amicon Cat. # 6028, MilliporeSigma, USA) was passed

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through the membrane under nitrogen gas at a constant feed pressure of 60 kPa, resulting in an initial pure water permeate flux of 2760 ± 77 L m2 h1 (HPI MF) or 3097 ± 106 L m2 h1 (HPO MF). These high fluxes were selected to accelerate membrane fouling. Likewise, relatively large cumulative volumes were also processed in the filtration experiments. The permeate flux (by permeate mass) was continuously recorded. The membrane filtration continued until at least 400 mL of permeate was collected (equivalent to ~300 L m2) or the flux decreased to 10% of the initial flux under the given pressure, whichever came first. For some experiments, the MF membrane was removed at the end of each membrane filtration test, hydraulically washed with deionized water to remove any cake layer, and replaced in the filter assembly for measurement of permeability recovery. The percent permeability recovery of fouled membranes after cleaning was determined based on the variance from the pure water permeability measured for each fresh membrane before the filtration test. 2.4.3. Cleaning strategies Both HPI and HPO PVDF MF membranes were intentionally fouled by filtering a given amount of untreated ROC. Subsequent cleaning was performed by soaking the fouled membrane sheets in flasks containing either 800 mL of either diluted NaOH solutions (pH 9, 10, 11, and 12) or algal suspension (OD680 ¼ 0.80 ± 0.05 cm1). The goal of this experiment was to evaluate the feasibility of using an alternative cleaning strategy for recovery of membrane permeability. The membrane sheets in NaOH solutions were gently agitated for 48 h, while the flask containing algal suspension and membrane sheets was incubated in the light under non-aerated conditions for 48 h and the pH of the mixed liquor was monitored. The submerged membrane sheets in the flask were drawn out one at a time at intervals (6, 12, 18, 24, and 48 h) during the incubation. A pure water flux test was conducted to determine the permeability of the membrane sheets after cleaning for a given period. For some experiments, the fouled membranes were prepared by filtering a given amount of algal-treated ROC which was collected after the treatment of ROC with microalgae using aeration (5% CO2) in the light for 24 h. Likewise, subsequent algal-induced cleaning was applied to the fouled membranes for 48 h, and the restoration of permeability was determined by conducting a pure water flux test every 24 h. 2.4.4. Membrane characterization The organic matter retained on membranes after filtration and subsequent cleaning was characterized using Fourier transform infrared (FTIR) spectroscopy. Spectral data were collected on a Nicolet iS10 FT-IR spectrometer (Thermo Scientific, USA) equipped with a Smart iTR attenuated total reflection accessory. The FTIR spectra were obtained between 4000 and 600 cm1 over 16 scans with a resolution of 0.5 cm1 and then normalized to the highest absorbance. The morphological features of the top side of both

Table 1 Characteristics of the flat-sheet MF membranes examined in the batch experiments. Parameter

Hydrophilic (HPI) MF

Hydrophobic (HPO) MF

Catalogue No./trade name Material Surface property Nominal pore size (mm) Thickness (mm) Porosity (%) Pure water permeability (L m2 h1 kPa1) Water contact angle ( ) Protein binding capacity (mg cm2) Surface charge at pH 7 (mV)

GVWP04700 / Durapore® PVDF Hydrophilic 0.22 125 70 46±1 74±3 4 21

GVHP04700 / Durapore® PVDF Hydrophobic 0.22 125 75 52±2 117±2 150 18

Reference

Fan et al. (2001) Xiao et al. (2014) Fan et al. (2001) Fan et al. (2001)

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clean and fouled membranes were also observed using scanning electron microscopy (SEM) (NOVA nanoSEM 200, FEI, The Netherlands). 2.5. Submerged membrane bioreactor A bench-scale submerged MBR with a working volume of 8.4 L was operated over a month at a hydraulic retention time (HRT) of 25e29 h (Fig. 1) (Luo et al., 2017). The OD680 of algal biomass ranged between 0.8 and 1.1 cm1 (equivalent to 595e789 mg L1 as cellular dry weight) under continuous illumination (150e300 mmol photons m2 s1) and solids retention time (SRT) was maintained at 7 d during the course of algal MBR experiments. The aeration with 5e10% (v/v) CO2 was continuously applied with a flow rate of 70e80 mL min1 at the bottom of the MBR where a flat-sheet hydrophilic PVDF membrane module was submerged. Filtration runs were conducted at a constant flux of 5 L m2 h1 using a peristaltic pump for the permeate side of the membrane module with a nominal pore size of 0.1 mm (Shanghai SINAP Membrane Tech Co. Ltd., China), providing an effective filtration area of 0.1 m2. In addition to the MBR study, all the submerged MPBR studies were intentionally performed at relatively low fluxes ranging between 2.6 and 15 L m2 h1 as a strategy to decrease the extent of membrane fouling (Luo et al., 2017). Permeate flux was controlled and the transmembrane pressure was continuously recorded. Light intensity shown as the photon flux per unit area was converted to the volume-based photon flux density (mmol photons m3 s1) using the projected area and the working volume of the MBR reactor (rectangular tank), in order to compare this with the light intensity applied to cylindrical reactors used for the batch algal treatment.

was steeper for HPO MF (Supporting Information Fig. S4). More severe fouling in HPO MF was associated with hydrophobic interactions between organic molecules and membrane materials, especially when Ca2þ was added to organic-rich water. Several previous studies have reported that permeability decreased sharply with increasing Ca2þ concentration from 0.5 to 10 mM (Yuan and Zydney, 1999a, 1999b). Ca-induced formation of intermolecular bridges among organic foulant molecules retained on the surface of the membrane can also result in an incomplete restoration of membrane permeability after cleaning. Fig. 2 shows that the

3. Results and discussion 3.1. Fouling reversibility and novel cleaning strategy PVDF MF membranes with different surface wettability (HPI and HPO) were compared in terms of the reversibility of fouling after cleaning. The wettability of membrane can be judged by measuring the contact angle of water on the surface of the membrane (Table 1). The fouling tendency for HPO MF has been found to be higher than HPI MF in short-term tests (Fan et al., 2001; Kim et al., 2006a), which coincided with our observations with organic-rich synthetic wastewater in this study. The relative permeability of both membranes decreased with permeate volume, but the decline

Fig. 2. The recovery of membrane permeability following hydraulic wash and chemical cleaning of fouled membranes using caustic solutions (pH 9e12). Prior to each of the cleanings, HPI MF (a) and HPO MF (b) membranes were intentionally fouled by filtering ROC under the given conditions of filtration. The filtration of ROC continued until the permeability of ROC reached 11 ± 5% of the initial permeability. A pure water flux test was conducted to determine the restoration of membrane permeability after each cleaning.

Fig. 1. Experimental set-up for treatment of synthetic ROC using MBR with S. quadricauda microalga.

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reversibility of fouling for HPO MF (26 ± 5%) after the hydraulic wash was much lower than HPI MF (52 ± 6%), indicating the formation of denser and thicker cake layer on the surface of the HPO MF membrane faced to wastewater. Separate chemical cleanings with different pH levels of caustic solutions were performed to remove foulants retained on the surface of the membranes or its pore walls after filtration of ROC. Their effectiveness on the restoration of membrane permeability was found to correlate with the surface wettability of the membranes, i.e., HPI MF was less susceptible to irreversible fouling than HPO MF. The permeability recovery for HPI MF with chemical cleaning for 12 h or longer was always higher than HPO MF, except for the highest pH of 12 used in the experiment. The permeability of HPI MF was restored by 81 ± 5% after the first 12 h of the chemical cleaning at the solution pH ranging from 9 to 11 and further notable changes of the permeability was not found for the next 36 h. However, much lower recovery was achieved by cleaning at a more basic pH of 12 and even decreased gradually from 45 ± 8% to 27 ± 4% with the lapse of cleaning time from 6 h to 48 h. This performance was even lower than that achieved by hydraulic washing for 24 h, likely due to a deformation of the hydrophilic properties of membrane surface under highly alkaline conditions (Rabuni et al., 2013, 2015). In contrast, 68 ± 5% of the initial permeability was restored for HPO MF after the first 24-h cleaning, and no changes were found for the following 24 h with a range of pH values from 9 to 12 examined in the experiment. It is worthwhile to note that the permeability recovery increased with increasing pH from 9 to 12 for the first 18 h of chemical cleaning, and such pH-dependent cleaning process was similar to typical desorption kinetics of compounds from adsorbents (Avena and Koopal, 1998). Additionally, we evaluated the feasibility of the use of a novel alternative cleaning strategy to restore the permeability of membranes fouled in the filtration of ROC. The result of algal-induced cleaning for HPI and HPO MF membranes is displayed in Fig. 3,

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showing a gradual increase in pH as a result of algal photosynthesis in ROC and consequent restoration of the membrane permeability with the lapse of time. The permeability recovery for HPI MF increased from 38% to 82% as the pH of ROC increased from 9.3 ± 0.1 to 10.6 ± 0.8 (6 he24 h), but the trends were reversed at pH 11.3 ± 0.7 (48 h). This result was consistent with a deteriorated recovery of membrane permeability after cleaning at a pH higher than 11 as described above (Fig. 2a). The maximum recovery, which was achieved by the algal-induced cleaning of HPI MF for 24 h, was comparable to that observed after chemical cleaning at pH in the range of 9e11 for an identical amount of time. Likewise, a notable flux restoration was observed for HPO MF with the lapse of time for algal-induced cleaning. However, the permeability of HPO MF recovered by 57 ± 14% after the cleaning for up to 48 h, and this was lower than that observed for HPI MF after the first 24 h cleaning (82 ± 13%). This might be attributed to strong binding of cell debris and/or EPS to the hydrophobic surface of HPO MF during the in-situ cleaning with microalgae for a day or longer in the light with nonaerated conditions. In support of this explanation, Table 1 shows that HPO MF has a considerably higher binding capacity for protein than HPI MF. Similar results were observed in the separate batch tests for algal-induced in-situ cleaning of membranes fouled by filtering algal-treated ROC (Fig. 4). A higher recovery was observed for HPI MF which produced twice the amount of permeate volume. The first 24-h cleaning with microalgae restored the permeability of HPI MF by 87 ± 5%, which was much greater than that observed for HPO MF (27 ± 4%). The pH of algal suspension increased for the next 24 h. This resulted in a further increase in the permeability recovery of HPO MF (by up to 47 ± 5%), while the opposite result was observed for HPI MF as described above (Fig. 3). This is the first time that microalgae are shown to influence the restoration of permeability in the filtration via naturally occurred photosynthesis. This is significant, as this process does not require drainage of wastewater/ biomass and the use of additional caustic chemicals. It is worthwhile to note that a negligible change in the viability of algal cells was found after the first 24 h of algal-induced cleaning under the given conditions (Supporting Information Fig. S5). It indicates that ROC treatment could be continued after the in-situ cleaning without a loss of algal biomass as bioagents for wastewater remediation. 3.2. Ozonation followed by algal treatment prior to microfiltration

Fig. 3. The variations in pH and permeability recovery during algal-induced cleaning of fouled membranes. Prior to each of the cleaning, HPI MF (a) and HPO MF (b) membranes were intentionally fouled by filtering ROC under the given conditions of filtration.

HPI MF showed high reversibility of fouling after cleaning and was thus selected for additional tests. ROC was treated using S. quadricauda with four different algal concentrations at OD680 values in the range of 0.4e1.6 cm1 and their filterability through HPI MF was plotted in comparison with untreated ROC in Fig. 5a. Although the relative permeability at the end of the tests tended to be lower with an increase of algal concentration, all the treatment using microalgae alleviated the permeability decline of HPI MF compared to when filtering untreated ROC. Light availability was considered to determine a proper density of algal biomass for wastewater treatment. Results of our preliminary test indicate that CO2 fixation deteriorates for denser cultures (>0.85 cm1 as OD680) due to mutual shading of algal cells (Supporting Information Fig. S6). An OD680 of 0.8 cm1 roughly means that 84% of the light illumination is absorbed within a path length of 1 cm1 and cells deeper in the culture receive less or no light. Light and CO2 metabolism interact in defining the limits of light availability for the growth of algae (Borowitzka and Moheimani, 2013). Fig. 5b shows the effects of ozone pretreatment combined with algal treatment (OD680 ¼ 0.80 ± 0.05 cm1) on the performance of HPI MF with respect to permeability and fouling reversibility.

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Fig. 4. Decline in the permeability during the filtration of algal-treated ROC using two different PVDF membranes, the permeability recovery of the fouled membranes after subsequent in-situ cleaning with microalgae, and the surface images of fresh (I-1 & O-1), fouled (I-2 & O-2), and cleaned (I-3 & O-3) membranes.

Ozonation followed by algal treatment substantially decreased fouling in MF, showing a much slower decline in the membrane permeability compared to when filtering ROC after algal treatment alone, and the permeability decline tended to be slower with increasing ozone dosage. It has been reported that the ozone pretreatment of organic-rich water decreases the adsorption tendency of organic matter onto the membrane materials, resulting in a significant (beneficial) increase in the membrane permeability (Van Geluwe et al., 2011). The fluorescence EEM spectra of organic components in ROC show a typical feature of humic substances that has been implicated as the primary cause of short-term fouling in low-pressure membrane filtrations (Fig. 5c) (Kim and Dempsey, 2010, 2012). The fluorescence intensity attenuated by 25% after algal treatment alone, while 75e82% decrease in the initial intensity was achieved by coupling ozone pretreatment with the algal treatment. The decrease in fluorescence intensity of organic matter

reflects the degradation or sometimes mineralization of the corresponding fluorophores or functional groups that are present in the chemical structure of the fluorescent organic matter (Mostofa et al., 2013a, 2013b). 2222The reversibility of fouling (equivalent to the restoration of permeability) after hydraulic cleaning was 88e91% when ozone pretreatment was combined with algal treatment, which was higher compared to when using microalgae as the sole pretreatment for microfiltration of ROC (64 ± 6%). This result was consistent with observed variations in the FTIR spectra of the surface of fouled membranes after cleaning. Fig. 6 shows the FTIR spectra of clean and fouled HPI MF. Most of the changes in absorbance occurred at 1690e1510, 1100e1030, and 670‒630 cm1, corresponding to the increased occurrence of N-containing organic compounds and polysaccharide-like substances. The absorbance bands were interpreted using information from our prior work characterizing

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Fig. 5. Flux decline during the filtration of raw and algal-treated ROC using HPI MF membranes (a) and the effects of pre-ozonation combined with algal treatment on the performance of HPI MF (b) and the fluorescent characteristics of organic matter (c). Inset shows the membrane permeability restored by hydraulic cleaning. ROC was treated using microalgae with different cell concentrations (OD680 ¼ 0.4e1.6 cm1) in the light under aerated conditions (5% CO2) for 24 h. Ozonation was examined for pretreatment of ROC ahead of algal treatment at an OD680 of 0.8 cm1.

foulants in the low-pressure membrane filtration of natural organic matter and wastewater effluent organic matter (Kim, 2016; Kim and Dempsey, 2008; Kim et al., 2006b). The band at 1645 cm1 was attributed to the C]O stretching of amide groups (amide I band); this vibration was coupled with the NeH bending and C]N stretching vibrations (amide II band) that weakly appeared at around 1535 cm1. The general features of the amide bands were observed for slightly fouled two membranes (1 and 2 mg-O3 mg-C1), but not for moderately fouled membrane (0 mg-O3 mg-C1) probably due to an increased absorbance band at around ~1600 cm1 which was attributed to the C]C stretching of the aromatic ring structure. The moderately fouled membrane also showed remarkable bands at 1100‒1030 cm1 and 670‒630 cm1 which were associated with the CeO stretching of polysaccharide-like substances and deformations of COOH and/or O]CeN, respectively. Although FTIR is only able to detect the functional groups at a finite depth of the surface of membranes, the absorbance in these FTIR regions was apparently increased by organic matter retained in membranes and was higher for the moderately fouled membrane than that observed for the slightly fouled membranes. In this study, the use of constant pressure experimental procedures for membrane filtration resulted in high initial fluxes (2760 ± 77 L m2 h1) that could be super-critical, i.e., where transport of materials to the membrane surface so dramatically exceeds the back-transport processes (Kim, 2016; Kim and Dempsey, 2008). Therefore, in this case, fouling with humic-like and polysaccharide-like substances could be limited on the top of the membranes instead of being transferred to the pores deeper inside the membranes due to immediately applying super-critical conditions.

Increasing cultivation time can result in increased removal of contaminants by providing additional time and opportunity for biochemical reactions (Maeng et al., 2018b). This would, in turn, also significantly affect the performance of the membrane when filtering algal-treated ROC. In this study, increasing cultivation time from 24 h to 48 h resulted in a steeper decrease in membrane permeability during dead-end filtration (Supporting Information Fig. S7). Moreover, the 48-h cultivation deteriorated the reversibility of fouling after hydraulic cleaning, indicating that more irreversible cake layer formed with the filtration of algal-treated ROC. These observations coincided with the concurrent observations with fluorescence and FTIR spectroscopies in characterizing organic matter. FTIR spectra showed more intense absorbance bands at wavenumbers of 1690e1510 and 1100‒1030 cm1, as the algal treatment of ROC was allowed to continue for an additional 24 h. A fingerprint of tryptophan-like substances was observed after the treatment of ROC with microalgae for 48 h. Algal-derived organic matter contains polymeric organic components such as polysaccharides and proteins (Henderson et al., 2008), which have high molecular weight and hydrophobic characteristics (Liao et al., 2018). Tryptophan-like biopolymers are typically associated with microbial activities among the fluorescent organic constituents and have been implicated as major foulants in submerged MPBRs for microalgae cultivation and wastewater treatment (Luo et al., 2017). 3.3. Treatment of ROC using algal MBR Results of batch experiments showed that treatment of ROC with microalgae alleviated fouling to some extent in MF and its

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Fig. 6. ATR-FTIR absorbance spectra for the top-side of HPI PVDF membranes after dead-end filtration and subsequent hydraulic cleaning. Lines (bottom to top) represent a clean, slightly fouled (2‒1 mg-O3 mg-C1), and moderately fouled (0 mg-O3 mg-C1) membranes. The extent of fouling was determined based on the restoration of membrane permeability after hydraulic cleaning. Spectra were normalized to the highest peak at a wavenumber of 875 cm1.

Fig. 7. The variations in hydraulic resistance to filtration (a) and water quality (b) during algal treatment of ozonated ROC using MBR with a flat-sheet hydrophilic 0.1 mm PVDF membrane module. The MBR was operated at a constant flux of 5 L m2 h1 under ordinary conditions of pH (8.5 ± 0.3) and temperature (20 ± 1  C).

combination with ozone pretreatment achieved better performance, e.g., slower decline in permeability and increased reversibility of fouling. In this study, a longer-term evaluation was performed with a goal of achieving a robust removal of contaminants. A submerged MBR with hydrophilic PVDF MF was constructed and operated using microalgae as bioagents which are certainly more promising for removal of nutrients from wastewater. The hydraulic resistance to filtration was determined using tap water (with no added algae) for the first 2 days of operation, which never exceeded 3.2  1012 m1, and a negligible change in the resistance to filtration was found during the course of MBR experiments using ozonated ROC (1 mg-O3 mg-C1) with added algal biomass (Fig. 7a). Removal of TN was the biggest challenge at the initial stage of the MBR operation using a single illumination (150 mmol photons m2 s1) on the front of the reactor. The light intensity was mended by placing the light source closer to the reactor and providing an additional illumination on the backside of the reactor. Between the 11th and 21st day of the experiment, the light intensity was stepwise increased to 300 mmol photons m2 s1 per each side, which resulted in a dramatic decrease in TN and consistently achieved 89 ± 2% removal of TN for the last ten days of operation. A similar trend was observed for TP, showing 94 ± 2% removal of TP was achieved by supplying more light energy to microalgae in the reactor and was continued until the end of the experiment. Fig. 7b shows that the algal assimilation of nitrate was more lightdependent when compared to the uptake of phosphate by the microalgae, which was consistent with our previously reported observations with the same algal strain (Kim et al., 2014c). Microalgae assimilate the inorganic nitrogen present in wastewater and

convert it to various organic nitrogen species required for cell synthesis, while efficient P removal does generally not require additional algal biomass production above that needed for N assimilation and excess amounts of orthophosphate taken up by microalgae are stored in the cell (Dyhrman, 2016; Raven and Giordano, 2016). Mixed liquor suspended solids (MLSS) in the reactor ranged between 595 and 789 mg L1 during MBR operation at a SRT of 7 d, which was about 3e4 times lower than typical MLSS ranges for activated sludge treatment at the same SRT. In addition to reducing solid wastes from the bioreactor, the operation of MBR with a low level of biosolids is desirable for algal treatment of wastewater to prevent mutual interference in the light availability (i.e., self-shading effect) that can result in a substantial decrease in the nutrient removal (Kim et al., 2014c). Along with the removal of inorganic nutrients with microalgae, the removal of carbonaceous organic matter can also be achieved by S. quadricauda, unless the organic carbon source for heterotrophic (in the dark) or mixotrophic (in the light) algal growth is a limiting factor. Fig. 7b shows that S. quadricauda engaged in mixotrophic growth under aerated conditions with 5e10% (v/v) CO2 and was effective in removing organic matter, especially when using a lower intensity of illumination. The trophic shift of microalgae from photoautotrophy to mixotrophy could be promoted with decreasing light energy delivered to the algal cells, and vice versa. The MBR was operated with microalgae under continuous illumination of low to a high intensity which accounted for about 27%e 107% of light intensity used in the batch experiments. The removal of COD was much higher than that of TN, but the trend was reversed at the 18th day of operation. Increasing the light intensity in the middle of the experiment resulted in a decreased removal of

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COD, but achieved 40e70% removal of COD until the end of the operation. Ozonation alone was ineffective in completely oxidizing organic components (Supporting Information Fig. S8), however this inefficiency could contribute to improving the bioavailability of organic matter for the microalgae. Biological treatment following ozonation is a well-known strategy for effective removal of recalcitrant dissolved organic matter from a wide range of wastewater, but this study did not focus on a common issue of possible changes in the biodegradability of organic compounds. Simultaneous removal of COD, TN, and TP from wastewater in a single reactor suggests that the phycoremediation with S. quadricauda proposed in this study may offer simplicity in reactor design, configuration, and operation, in contrast to conventional biological nutrient removal processes that are comprised of nitrification/denitrification and luxury P uptake under strictly controlled operating conditions. This study also investigated the fate of caffeine and carbamazepine during the continuous flow treatment of ozonated ROC using the MBR with microalgae. They were selected from ten TOrCs examined in our previous work (Maeng et al., 2018b), showing wide variations in the treatability with bioremediation for which S. quadricauda achieved the highest removal of caffeine, but hardly removed carbamazepine. In this study, ozonation attenuated caffeine by 52 ± 2% and subsequent algal treatment further removed by 93 ± 5% (Fig. 8). A similar trend regarding the treatability of caffeine with bioremediation following ozonation was also observed in our previous study (Kim et al., 2017), and a high biodegradability of caffeine has been reported in other previous studies (Ahmed et al., 2017; Garcia-Rodríguez et al., 2014). Likewise, ozonation followed by algal treatment achieved >94% removal of carbamazepine, but almost all of this attenuation was completed by the ozonation, and a negligible change in the level of residual carbamazepine was found during algal treatment under the given conditions. Carbamazepine is known to be recalcitrant toward biological degradation as shown in previous reports (Kim et al., 2015; Maeng et al., 2018b), correlated to the non-polar hydrophobicity of the compound.

4. Conclusions This study applied ozonation and algal treatment for treatment of ROC prior to MF. The algal treatment as a standalone process alleviated fouling to some extent in MF, while a markedly improved performance was achieved when ozonation was combined with algal treatment. The ozone pretreatment combined with algal

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treatment significantly mitigated flux decline and increased the reversibility of fouling in MF. This combination suggests improved degradation of recalcitrant organic matter, along with removing nutrients during algal growth under light illumination with aeration (5e10% CO2). In particular, this combination is highly recommended to minimize the level of TOrCs with the wide diversity of treatability, e.g., caffeine (relatively resistant to ozone oxidation, but easily biodegradable under aerobic conditions) and carbamazepine (contrarily, hardly biodegradable). Spectroscopic diagnosis of membrane fouling indicated that increasing the algal cultivation time for treatment of ROC promoted the deformation and/or production of undesirable organic matter for MF, which was strongly associated with both accelerated flux decline and deteriorated permeability recovery. Longer-term studies should be performed to determine the long-term fouling effects of algogenic organic matter, especially fluorescent proteinaceous fractions that can be produced in algal growth. In this study, we also demonstrated the possible applicability of using algal-induced pH adjustment for in-situ cleaning of fouled membranes. The algal-mediated in-situ cleaning successfully restored the permeability of fouled membranes. In addition to the concurrent removal of organic and inorganic components in a single biological process, this in-situ cleaning offers operational simplicity and adaptability to existing membrane facilities that currently perform periodic chemical cleaning. This is the first time that S. quadricauda is shown to play dual roles of anti-foulants and bioagents in the remediation of refractory wastewater. The natural cleaning process identified in this study uses living algal components that are capable of reproduction and nutrient uptake. Acknowledgments This research was supported by the National Research Foundation of Korea (NRF) grant funded by the Korea government (MSIT) (No. 2018R1A2A2A05022776). This work has been subjected to the U.S. Environmental Protection Agency's administrative review and has been approved for external publication. Any opinions expressed in this paper are those of the authors and do not necessarily reflect the views of the agency; therefore, no official endorsement should be inferred. Any mention of trade names or commercial products does not constitute endorsement or recommendation for use. Appendix A. Supplementary data Supplementary data to this article can be found online at https://doi.org/10.1016/j.watres.2019.05.003. References

Fig. 8. The attenuation of selected TOrCs through ozonation followed by algal treatment during MBR operation (n ¼ 17).

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