The impact of temperature on membrane fouling in algae harvesting

The impact of temperature on membrane fouling in algae harvesting

Algal Research 16 (2016) 458–464 Contents lists available at ScienceDirect Algal Research journal homepage: The impac...

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Algal Research 16 (2016) 458–464

Contents lists available at ScienceDirect

Algal Research journal homepage:

The impact of temperature on membrane fouling in algae harvesting Huaqiang Chu, Fangchao Zhao, Xiaobo Tan, Libin Yang, Xuefei Zhou, Jianfu Zhao, Yalei Zhang ⁎ State Key Laboratory of Pollution Control and Resource Reuse, Tongji University, Shanghai 200092, China

a r t i c l e

i n f o

Article history: Received 14 December 2015 Received in revised form 25 February 2016 Accepted 16 April 2016 Available online 23 April 2016 Keywords: Algae harvesting Temperature Flux Membrane fouling EOM

a b s t r a c t Temperature has a significant impact on both the secretion of extracellular organic matter (EOM) and the performance of membrane filtration, which influences the efficiency of algae harvesting by membrane technology. In this study, the performance of membranes for microalgae harvesting was investigated under different temperatures. The results showed that the critical flux (Jc) increased from 27.0 to 42.0 L/(m2·h) when the solution temperature increased from 15 to 35 °C. In continuous filtration tests, membranes at high temperature had a low flux decline. At 35 °C, the decrease rate of flux was 59.7%, whereas at 15 °C, the decrease rate of flux was 85.5%.The higher flux and lower membrane fouling at higher temperature were partly due to the decline of liquid viscosity, which further decreased the permeate drag force (FD). Lower FD retarded the deposition of particles on the membrane surface, which reduced the quantity of algae deposited on the membrane. At low temperatures, the high content of EOM was another possible cause of membrane fouling. At 15 °C, the algae solution contained a high concentration of total extracellular organic matter (TEOM), 263.2 mg/L; moreover, the specific EOM secretion rate (SEOM) decreased with a temperature increase from 15 to 35 °C. © 2016 Elsevier B.V. All rights reserved.

1. Introduction Biofuel can reduce global warming caused by fossil fuels and has very promising application prospects [1]. Microalgae are a good source for biofuel, but there are still substantial challenges in achieving efficient harvesting for commercial use. Membrane technology is a promising separation and filtration process due to its stable and clean effluent water [2]. Currently, a growing number of researchers have studied how to make better use of membranes for microalgae harvesting [3,4]. However, the primary problem of membrane technology is membrane fouling [5]. During filtration, algae cells and extracellular organic matter (EOM), can accumulate on the membrane surface, and some even enter into the pores of the membrane, resulting in a decrease of membrane permeability and an increase of filtering resistance [6]. Currently, EOM in either the bound or dissolved form is considered a significant cause of membrane fouling in the algae harvesting process [7]. Qu et al. [8] found that flux decline and irreversible membrane fouling were more serious when microalgae were combined with EOM. However, in our previous research, it was found that seasonal changes of temperature had a significant influence on algae growth in Abbreviations: EOM, extracellular organic matter; dEOM, dissolved extracellular organic matter; bEOM, bound extracellular organic matter; TEOM, total extracellular organic matter; SEOM, the specific EOM secretion rate; STEOM, the specific TEOM secretion rate; SdEOM, the specific dEOM secretion rate; SbEOM, the specific bEOM secretion rate; JC, critical flux; TMP, transmembrane pressure; IFM, improved flux-step method; JL, low flux; JH, high flux; JI, a fixed initial flux; ΔJ, the specific rate of change of flux; JC35, critical flux at 35 °C; FD, the permeate drag force; Rm, the membrane hydraulic resistance. ⁎ Corresponding author. E-mail address: [email protected] (Y. Zhang). 2211-9264/© 2016 Elsevier B.V. All rights reserved.

outdoor cultivation [9,10]. Temperature also has important effects on permeate flux and membrane fouling l. Particularly, for outdoorcultured microalgae, the effect of temperature on microalgae harvesting is more evident. Eziyi et al. [11] reported that the membrane flux was highly sensitive to temperature variations. Within a range of 33 to 36 °C, a 1 °C decline of liquid temperature can result in a decrease of approximately 1 L/(h·m2) of permeation flux [12]. However, the impact of temperature on the permeate flux is complicated when the algae solution contains a relatively high concentration of cells and EOM. Within a suitable temperature range, the higher the temperature, the faster the metabolism and the more EOM the microalgae releases [4,13]. It is possible that with an increase in temperature, the permeate flux of the membrane does not increase because of the aggravated membrane fouling at high levels of EOM in the feed. Although several researchers have studied the effect of temperature on membrane fouling, microalgae growth or secretion of EOM [11–14], there is little literature about membrane fouling in association with the performance of algae at different temperatures. Lee et al. [15] showed that high water temperature can reduce the viscosity of solution and thus increase the permeability of the membrane. However, how and why the viscosity influences the performance of the membrane has not been reported. Therefore, to determine the appropriate operation temperature to reduce membrane fouling and to understand how temperature influences the performance of microalgae harvesting by membrane filtration, it is necessary to investigate the effect of temperature on the performance of the membrane for microalgae filters. Tan et al. [9] reported that when temperature was above 40 °C or below 10 °C, the algae growth rate was very low. Therefore, in this study, 15, 20, 25, 30 and 35 °C use to study the changes of membrane fouling,

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permeate flux, algae growth and EOM concentration. First, at different temperatures, the critical fluxes were measured; meanwhile, the calculation of the permeate drag force at different temperatures was used to explain why high temperature could reduce membrane fouling. Second, we studied the changes of the concentration of algae and EOM under different temperatures. Finally, to further verify the effects of temperature on the variation in flux and membrane fouling, a continuous filtration experiment was conducted. Through this study, we hope to provide some valuable information to further the understanding of why and how temperature influences the performance of the membrane and membrane fouling in algae harvesting; in addition, we also hope to provide a reference for algae harvesting by membrane technology. 2. Materials and methods 2.1. Cultivation of microalgae Chlorella pyrenoidosa (C. pyrenoidosa, FACHB-9) was obtained from the Institute of Hydrobiology at the Chinese Academy of Sciences in China. C. pyrenoidosa was cultured in Basal medium prepared in sterile distilled water. The Basal medium consisted of KNO3 (1250 mg/L), KH2PO4 (1250 mg/L), MgSO•47H2O (1000 mg/L), EDTA (500 mg/L), H3BO3 (114.2 mg/L), CaCl•22H2O (111 mg/L), FeSO•47H2O (49.8 mg/L), ZnSO•47H2O (88.2 mg/L), MnCl•34H2O (14.2 mg/L), MoO3 (7.1 mg/L), CuSO•45H2O (15.7 mg/L), Co(NO3)•36H2O (4.9 mg/L) and glucose (1000 mg/L). The pH of the culture solution was adjusted to 6.1 using NaOH before being inoculated with algae. The algae was inoculated in 3 L conical flasks containing 2 L of autoclaved Basal medium and placed in an incubator (GZX-300BS-III, CIMO Medical Instrument, Shanghai, China). All experiments were conducted in three parallel cultures. The initial concentration of algae was 0.08 g/L. The temperatures of the incubators were maintained at 15 ± 0.5, 20 ± 0.5, 25 ± 0.5, 30 ± 0.5 and 35 ± 0.5 °C, respectively. The culture conditions were as follows: light/dark = 14 h/10 h, light intensity = 127 μmol/m2·s. For the continuous filtration experiments, algae were cultivated in transparent plastic buckets, with 20 L placed in the incubator under different temperature conditions. 2.2. Extraction and analysis of extracellular organic matter (EOM) The extracellular organic matter (EOM) was divided into boundEOM (bEOM) and dissolved-EOM (dEOM). Algae solution (5 mL) was first centrifuged at 4000 rpm for 15 min in a centrifuge (CT15RT, Shanghai, China), and the supernatant was filtered through a 0.45 μm filter to obtain the dEOM. For the bEOM extraction, the residual algae (added to 5 mL using distilled water) was centrifuged at 10,000 rpm for 15 min and subsequently filtered through a 0.45 μm filter to obtain the bEOM [8,16]. C. pyrenoidosa was cultured for 11 days, and the biomass and EOM (including dEOM and bEOM) were collected for daily analysis. The concentration of C. pyrenoidosa was measured using the OD680 method. Polysaccharides and proteins were the main compositions in EOM (accounting for 90% of EOM) and had a significant influence on membrane fouling [17,18]. Polysaccharides and proteins in dEOM were named dpolysaccharides and d-proteins, respectively; polysaccharides and proteins in bEOM were named b-polysaccharides and b-proteins, respectively. The contents of the proteins and polysaccharides were measured using the anthrone-sulfuric acid method and the modified Lowry method, respectively [19]. To determine the capacity of EOM release by C. pyrenoidosa at different temperatures, a specific EOM secretion rate (SEOM) was used, as in Eq. (1):


CEOM Calgae



where SEOM is the specific EOM secretion rate (mg/g), CEOM is the concentration of EOM (mg/L), and Calgae is the concentration of C. pyrenoidosa (g/L).

2.3. Reactor set-up The filtration experiments were all conducted in a lab-scale filtration tank, as illustrated in Fig. 1. The filtration tank had a working volume of 2.5 L. A micro-porous pipe was located on the bottom to reduce membrane fouling. The volume of aeration was 30 m3.h−1.m− 2. In this study, a hydrophilic PVDF membrane (pore size of 0.1 μm) was used. The membrane had an effective filtration area of 0.02 m2. The filtrate was pumped by a peristaltic pump (BT100-LJ, Kejian, China). The flow velocity was automatically recorded by an electronic balance connected to a computer. A vacuum meter was installed on the module measuring the transmembrane pressure (TMP).

2.4. Filtration experiments 2.4.1. Critical flux test Critical flux (JC) is a quantitative parameter for the filterability of a membrane, which is generally regarded as the flux above which the membrane fouling rate will be aggravated [20,21]. Practically, a higher flux will cause serious membrane fouling and a sharp decline in flux, but a lower flux affects the working efficiency of the membrane. Selecting an appropriate flux under the critical flux, namely, an appropriate sub-critical flux, will prolong the service life of a membrane and reduce the cleaning frequency. In addition, the critical flux can also be employed to compare the fouling propensities between membranes. Thus, it was essential to measure the critical fluxes under different temperature conditions. The values of critical flux were determined by an improved flux-step method (IFM) [22]. The algae used in the IFM tests were all cultured at 25 °C and had similar concentrations of 0.3 mg/L. During each test, one other algae sample was placed at the same temperature to verify if there was a difference in the content of the algae and EOM after several hours, and it was found that there was a small difference in every group. Thus, in IFM, the performances of the membranes were considered to be affected only by temperature. The permeate was measured and recorded using an electric balance and a computer and was subsequently recycled into the filtration tank to keep the cell concentration constant. In IFM, a stepwise increasing flux (JH) was applied and an intermediate decrease in flux to a low flux (JL) was employed after each JH [22,23]. In IFM, no fouling occurred at JL, and filtration at JL was considered as a form of relaxation [22], although the real relaxation filtration should be 0 L/m2h. However, a flux larger than 0 L/m2h must be applied to measure a value for TMP before and after a JH [22]. At the low flux, the convective flow towards the membrane is reduced and the foulants are removed due to air scouring. Several studies have shown that continuous air bubbling was able to control the deposition at a very low level [24,25]. At different temperatures, the JL of each module was identical (10 L/ (h·m2)). JH started from 15 and stepwise increased by 3 L/(h·m2), respectively. All JL and JH processes lasted 15 min [22]. In this research, an arbitrary minimum increase in the TMP of 20 Pa min−1 was used to determine JC.

2.4.2. Continuous filtration experiments During the filtration process, the reactor temperatures were consistent with the cultivation temperature. The initial concentrations of the microalgae were all adjusted to 0.3 g/L (dry weight) by adding water in every group. During the test, the pipe became flat in several hours if the flux stayed at 30 L/(h·m2). To conduct a 24-h filtration, the peristaltic pump was kept at a constant rotation speed [26].


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Fig. 1. Schematic diagram of the experimental setup in continuous filtration experiment.

During the filtration, a fixed initial flux (JI) was applied, as calculated using Eq. (2): JS ¼ 0:7JC35


where JC35 is the critical flux determined at 35 °C (L/(h·m2)). To reduce the effects of the discrepancies between the experimental conditions as much as possible, the fixed initial flux (JI) was kept constant for the same membranes under different temperatures. One reason that 0.7JC35 was selected as JI is because the membranes had the highest critical flux (JC) at 35 °C. The other reason was that 0.7JC35 approximated the value of JC at 15 °C, and there was sub-critical flux at 20, 25, 30, and 35 °C that would prolong the filtration time and reduce the fouling rate. During filtration, the specific rate of change of the flux was calculated using Eq. (3):

serious membrane fouling. When the membranes were at the same flux, the values of TMP at low temperatures were higher than those at high temperatures. Huang et al. [29] also found that membrane resistance increased as the temperature decreased from 25 to 5 °C during wastewater treatment using an aerobic dynamic membrane bioreactor. In the descending phase, the membranes had higher TMP than the corresponding fluxes in the ascending phase, which suggested that the membranes were already fouled in the ascending phase [22]. In particular, at large fluxes, the membranes had more severe fouling and higher TMP, which could not be completely removed by bubbles in the descending phase. When the flux was 39 or 36 L/(h·m2) in the descending phase, the values of TMP were even higher than those at 42 L/(h·m2). The membrane was fouled more seriously due to the long test time and the high flux. 3.2. Effect of temperature on the permeate drag force

ΔJ ¼

dJ JI dt


where ΔJ is the specific rate of change of the flux (1/s), J is the filtration flux (L/(h·m2)), JI is the fixed initial flux (L/(h·m2)), and t is the filtration time (h). The specific rate of change of the flux is divided into three stages: the rapidly declining stage (ΔJ N 0.1), the slowly declining stage (0.01 b ΔJ b 0.1) and the stable stage (ΔJ b 0.01) [27]. After continuous filtration experiments, algae deposited on the membrane was rinsed with water, and the concentration of the algae was measured, which was used to evaluate the effect of temperature on algae deposition. 3. Results and discussion

In membrane filtration, algae particle deposition onto membrane is influenced by the permeate drag force (FD) [30,31]. The increase of FD enhances the velocity of particles towards the membrane, which accelerates the deposition of particles on the membrane surface, accelerating membrane fouling [30,32]. The permeate drag force is expressed as FD ¼ 6πμ w ra vw φH

where FD is the permeate drag force (nN), μw is the solution viscosity (Pa·s), ra is the particle radius (m), vw is the permeate water velocity (m/s), and φH (F/F∞) is the hydrodynamic correction factor [30,32]. The negative sign in Eq. (4) indicates the permeate drag force as attraction towards the membrane surface. φH was a complex function of the surface's Darcy permeability, separation distance, and particle radius [30–32]. This correction factor at the point of contact was described by

3.1. Effect of temperature on critical flux Fig. 2 shows that JC increases along with the increase of temperature. The membrane permeate flux was sensitive to the temperature change of the feed solution, and the viscosity decreased when the temperature increased [11,28]. Goosen et al. [28] found that the permeate flux increased by 60% when the water temperature increased from 20 to 40 °C. In this study, the JC of the 0.1 μm membrane increased by 56%, when the algae solution temperature increased from 15 to 35 °C. As shown in Table 1, the membranes had the same JC of 30 L/(h·m2) at 20 and 25 °C, but the values of TMP were 1.1 and 0.5 kPa, respectively. That is to say, although some JC had the same value at different temperatures, the membranes with higher TMP at low temperatures had more


φH ¼

 0:5 2Rm ra þ 1:0722 3


where Rm is the membrane hydraulic resistance obtained by Darcy's law (m−1). The preliminary results suggested that when the temperature increased, the critical flux increased and the fouling rate decreased. The changes in the physical-chemical properties of the membrane, such as the pore size or the diffusivity of the solution in the membrane, may be the cause of the increase in the critical flux at high temperatures [28]. However, the solution viscosity change at different temperatures should not be neglected because it will affect the permeate drag force.

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Fig. 2. Flux-TMP profiles of the improved flux-step method under different temperatures.

According to Eq. (4), the permeate drag force (FD) changes with the viscosity and Rm. Fig. 3 shows that the temperature has an obvious influence on the viscosity of the fluid. When the temperature increases from 15 to 35 °C, the viscosity decreases from 2.08 to 1.30 mPa·s. The temperature also affects the membrane hydraulic resistance (Rm), but Lee et al. [15] found that Rm did not change with temperature due to the difference of the membranes. In this study, however, Fig. 3 shows that with increasing temperature, Rm declined. During the critical flux test, the flux was not constant, hence there was not a constant FD in the entire test. However, FD at different Table 1 The values of critical flux and TMP when flux reaching JC at different temperatures. Temperature (°C)






JC (L/(h·m2)) TMP (kPa)

27.0 1.1

30.0 1.1

30.0 0.5

33.0 1.0

42.0 2.5

temperatures could be compared at a given flux. In this study, the average particle radius was 2 μm, and 20 L/(h·m2) was arbitrarily selected as the given flux. Under the same flux of 20 L/(h·m2), FD at the surface membranes increased with the decrease of temperature (shown in Fig. 3). The increase of FD enhanced the velocity of particles towards the membrane, which accelerated the deposition of particles on the membrane surface and aggravated membrane fouling [30,32]. Therefore, at the same flux, with a decrease of temperature, more algae particles deposited onto the membrane, and membrane fouling was more severe, which was why the membrane had a high critical flux at high temperature. 3.3. Effect of temperature on algae In the process of algae filtering, accumulation of algal cells and EOM on the membrane surface can cause serious membrane fouling, leading to a remarkable decrease of membrane flux [33]. Temperature has a


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Fig. 3. At different temperatures the changes of viscosity; and the changes of membrane hydraulic resistances (Rm); and the changes of drag force at the surface of membranes with the same flux of 20 L/m2h (the average particle radius is 2 μm).

significant effect not only on membrane but also on algae growth and secretion of EOM. Therefore, tracking the trend of the algae and EOM concentration under different temperatures could contribute to explaining the cause of membrane fouling.

3.3.1. Effect of temperature on growth The growth performance of C. pyrenoidosa is different at different temperatures (shown in Fig. 4). The concentration of algae increased with the increase of temperature from 15 to 30 °C, and the highest concentration was 0.66 g/L (dry weight) at 30 °C. However, the concentration of biomass decreased to only 0.41 g/L when the culturing temperature subsequently increased to 35 °C. Han et al. [34] found that algae had a lower growth rate at 36 °C due to stronger respiration during the night. In the previous study, it was found that due to the lack of glucose, there was a low algae concentration at 35 °C, although

it had the fastest growth rate at the earlier stage with sufficient glucose [35]. 3.3.2. Effect of temperature on EOM During membrane filtration, EOM, including the bound and dissolved forms, is considered to be an important factor in membrane fouling [8]. Temperature is an important factor influencing the production of EOM. As shown in Fig. 4, the secretion of dEOM (d-polysaccharides and d-proteins), bEOM (b-polysaccharides and b-proteins) and total EOM (TEOM, including dEOM and bEOM) by microalgae varied at different culturing temperatures. At 15 °C, the algae solution had the lowest cell concentration, but the highest TEOM (263.2 mg/L). At low temperature, algae did not grow as fast as at high temperature due to the adjustment of synthesis, and the production of EOM was closely linked to synthesis [36]. There were also reports that at low temperature, the fixed carbon was transferred to

Fig. 4. Concentrations of total EOM and algae; and specific EOM secretion rate (SEOM) under different temperature conditions on the 11th day.

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EOM and overflow metabolism occurred [37]. As the temperature increased, the growth of the algae cells gradually recovered, and the content of TEOM decreased from 263.2 to 198.5 mg/L when the temperature increased from 15 to 20 °C. From 20 to 25 °C, as the concentration of algae increased, the volume of TEOM increased to 258.4 mg/L. At 25 and 30 °C, the concentration of TEOM exhibited small differences. However, at 35 °C, the algae solution contained the lowest amounts of TEOM (139 mg/L) due to the lower algae concentration. As shown in Fig. 4, the variations of dEOM and bEOM were similar to TEOM. The specific EOM secretion rate (SEOM) was introduced to elucidate the capacity of EOM secretion (Fig. 4). At 15 °C, the algae had the highest specific TEOM secretion rate (STEOM), specific dEOM secretion rate (SdEOM) and specific bEOM secretion rate (SbEOM), and the values were 822.5, 425.1 and 397.4 mg/g, respectively. As the temperature increased from 15 to 20 °C, SEOM (STEOM, SdEOM and SbEOM) declined sharply due to the recovery of growth activity [38]. Although the value of SEOM decreased with the increase of temperature from 15 to 35 °C, the SEOM did not vary significantly when the algae grew at temperatures of 20, 25, 30 and 35 °C. Wolfstein et al. [38] also found that the algae had the highest SEOM at the lowest temperatures (4 and10 °C), and the difference of SEOM at 15, 25 and 35 °C decreased.

3.4. Effect of temperature on continuous filtration During the continuous filtration, the concentration of algae was almost constant (0.3 g/L) in every group, and the SEOM (STEOM, SdEOM and SbEOM) declined with the increase of temperature. Therefore, the content of EOM in the tank decreased with the increase of temperature. Fig. 5 shows the flux and TMP variation with time during filtration under different temperature conditions. At 35 °C, because the fixed initial flux was 0.7 times JC35, the flux and TMP were relatively steady during the first 60 min. As time passed, the flux/TMP experienced a sharp decrease/increase stage followed by a relatively slow period of reduction until a stable stage was obtained. At 15, 20, 25 and 30 °C, the fluxes of all of the modules decreased rapidly at the beginning, followed by a slowly declining stage and a subsequent stable period. Fig. 5 shows that there was a higher final flux and lower final TMP at higher temperatures. As shown in Fig. 5, the final flux at 35 °C was approximately 2.5 times than at 15 °C. When the continuous filtration tests were completed, the decrease rates of flux were 85.5%, 79.6%, 70.5%, 64.3% and 59.7% at 15, 20, 25, 30 and 35 °C, respectively. At 15 °C, in addition to being the lowest temperature, the concentration of EOM was much higher than at other temperatures; thus, the membrane exhibited the highest rate of decreasing flux [29]. In continuous filtration, the membrane had less fouling and higher flux at higher temperatures, which indicated that high temperature is beneficial for algae harvesting by the membrane. As found in the research of Lee et al. [15], there was a high initial flux at high temperature, but there was also a high fouling rate


Fig. 6. The deposition of algae on membrane under different temperatures.

due to the differences of the operating conditions between Lee's experiment and this experiment. 3.5. Effect of temperature on the deposition of algae During the filtration of algae by a membrane, with the increase of algae cells deposited on the membrane, there is more serious membrane fouling and a faster flux decline. The content of algae on the membrane was measured to estimate the effect of temperature on the deposition on the membrane. With the increase of temperature, the value of deposited algae decreased from 4.26 to 3.31 g/m2 (shown in Fig. 6), indicating that temperature had a significant influence on algae deposition. Based on the calculation of the permeate drag force, at higher temperature, there was a lower drag force, which could slow the deposition rate of algae on the membrane, which explained why there was less algae deposited on the membrane at higher temperature. The more algae that is deposited on the membrane, the more serious the membrane fouling is [39], which could explain the reason why there was a higher flux and less fouling at higher temperature. 4. Conclusions This study showed that although a temperature of 35 °C led to the highest critical flux and best filtration performance, the algae growth rate was very low. From 25 to 30 °C, the highest algae concentration occurred, and the secretion capacity of EOM at 25 and 30 °C was only slightly different from that at 35 °C. Thus, the optimum strategy is to maintain the algae cultivation temperature at 25 to 30 °C and the filtration temperature at 35 °C. However, for large-scale outdoor cultivation, seasonal changes in the temperature are not easily controlled; although the temperature increase can reduce EOM secretion and membrane fouling, heating to increase the cultivation or filtration temperature will require an additional cost. Thus, in algae cultivation and harvesting, a high temperature should be maintained without extra cost for as long as possible. At 30 to 35 °C, the algae concentration decreased, so the cultivation temperature should not exceed 30 °C. Acknowledgements This work was financially supported by the National Key Technologies R&D Program of China (No. 2012BAJ25B02). References

Fig. 5. Variations in flux and TMP during continuous filtration under different temperatures ( is the stable stage during the first 60 min).

[1] J.W. Richardson, M.D. Johnson, X. Zhang, P. Zemke, W. Chen, Q. Hu, A financial assessment of two alternative cultivation systems and their contributions to algae biofuel economic viability, Algal Res. 4 (2014) 96–104. [2] O. Acosta, F. Vaillant, A.M. Pérez, M. Dornier, Potential of ultrafiltration for separation and purification of ellagitannins in blackberry (Rubus adenotrichus Schltdl.) juice, Sep. Purif. Technol. 125 (2014) 120–125.


H. Chu et al. / Algal Research 16 (2016) 458–464

[3] X. Zhang, Q. Hu, M. Sommerfeld, E. Puruhito, Y. Chen, Harvesting algal biomass for biofuels using ultrafiltration membranes, Bioresour. Technol. 101 (2010) 5297–5304. [4] F. Zhao, Y. Su, X. Tan, H. Chu, Y. Zhang, L. Yang, X. Zhou, Effect of temperature on extracellular organic matter (EOM) of Chlorella pyrenoidosa and effect of EOM on irreversible membrane fouling, Colloids Surf. B: Biointerfaces 136 (2015) 431–439. [5] T. Fujioka, L.D. Nghiem, Fouling control of a ceramic microfiltration membrane for direct sewer mining by backwashing with ozonated water, Sep. Purif. Technol. 142 (2015) 268–273. [6] X. Zhang, L. Fan, F.A. Roddick, Feedwater coagulation to mitigate the fouling of a ceramic MF membrane caused by soluble algal organic matter, Sep. Purif. Technol. 133 (2014) 221–226. [7] W. Zhang, W. Zhang, X. Zhang, P. Amendola, Q. Hu, Y. Chen, Characterization of dissolved organic matters responsible for ultrafiltration membrane fouling in algal harvesting, Algal Res. 2 (2013) 223–229. [8] F. Qu, H. Liang, J. He, J. Ma, Z. Wang, H. Yu, G. Li, Characterization of dissolved extracellular organic matter (dEOM) and bound extracellular organic matter (bEOM) of Microcystis aeruginosa and their impacts on UF membrane fouling, Water Res. 46 (2012) 2881–2890. [9] X. Tan, H. Chu, Y. Zhang, L. Yang, F. Zhao, X. Zhou, Chlorella pyrenoidosa cultivation using anaerobic digested starch processing wastewater in an airlift circulation photobioreactor, Bioresour. Technol. 170 (2014) 538–548. [10] H.Q. Chu, X.B. Tan, Y.L. Zhang, L.B. Yang, F.C. Zhao, J. Guo, Continuous cultivation of Chlorella pyrenoidosa using anaerobic digested starch processing wastewater in the outdoors, Bioresour. Technol. 185C (2015) 40–48. [11] I. Eziyi, A. Krothapalli, J.D. Osorio, J.C. Ordonez, J.V.C. Vargas, Effects of salinity and feed temperature on permeate flux of an air gap membrane distillation unit for sea water desalination, 2013 1st Ieee Conf. Technol. Sustain. (Sustech) 2013, pp. 142–145. [12] Y. Magara, M. Itoh, The effect of operational factors on solid/liquid separation by ultra-membrane filtration in a biological denitrification system for collected human excreta treatment plants, Water Science & Technology 23 (1991) 1583–1590. [13] A. Converti, A.A. Casazza, E.Y. Ortiz, P. Perego, M. Del Borghi, Effect of temperature and nitrogen concentration on the growth and lipid content of Nannochloropsis oculata and Chlorella vulgaris for biodiesel production, Chem. Eng. Process.: Process Intensif. 48 (2009) 1146–1151. [14] S. Lan, L. Wu, D. Zhang, C. Hu, Effects of light and temperature on open cultivation of desert cyanobacterium Microcoleus vaginatus, Bioresour. Technol. 182 (2015) 144–150. [15] H. Lee, S.G. Kim, J.S. Choi, S.K. Kim, H.J. Oh, W.T. Lee, Effects of water temperature on fouling and flux of ceramic membranes for wastewater reuse, Desalin. Water Treat. 51 (2013) 5222–5230. [16] H. Chu, H. Yu, X. Tan, Y. Zhang, X. Zhou, L. Yang, D. Li, Extraction procedure optimization and the characteristics of dissolved extracellular organic matter (dEOM) and bound extracellular organic matter (bEOM) from Chlorella pyrenoidosa, Colloids Surf. B: Biointerfaces 125 (2015) 238–246. [17] S. Tsuneda, H. Aikawa, H. Hayashi, A. Yuasa, A. Hirata, Extracellular polymeric substances responsible for bacterial adhesion onto solid surface, FEMS Microbiol. Lett. 223 (2003) 287–292. [18] M.Y. Chen, D.J. Lee, J.H. Tay, Extracellular polymeric substances in fouling layer, Separ Sci Technol 41 (2006) 1467–1474. [19] X.Q. Zhang, P.L. Bishop, B.K. Kinkle, Comparison of extraction methods for quantifying extracellular polymers in biofilms, Water Sci. Technol. 39 (1999) 211–218. [20] S. Kim, H. Park, Applicability assessment of subcritical flux operation in crossflow microfiltration with a concentration polarization model, J. Environ. Eng.-Asce 128 (2002) 335–340.

[21] J.A. Howell, Subcritical flux operation of microfiltration, J. Membr. Sci. 107 (1995) 165–171. [22] P. van der Marel, A. Zwijnenburg, A. Kemperman, M. Wessling, H. Temmink, W. van der Meer, An improved flux-step method to determine the critical flux and the critical flux for irreversibility in a membrane bioreactor, J. Membr. Sci. 332 (2009) 24–29. [23] M.R. Bilad, D. Vandamme, I. Foubert, K. Muylaert, I.F. Vankelecom, Harvesting microalgal biomass using submerged microfiltration membranes, Bioresour. Technol. 111 (2012) 343–352. [24] F. Wicaksana, A.G. Fane, P. Pongpairoj, R. Field, Microfiltration of algae (Chlorella sorokiniana): critical flux, fouling and transmission, J. Membr. Sci. 387-388 (2012) 83–92. [25] W. Luo, F.I. Hai, W.E. Price, L.D. Nghiem, Water extraction from mixed liquor of an aerobic bioreactor by forward osmosis: membrane fouling and biomass characteristics assessment, Sep. Purif. Technol. 145 (2015) 56–62. [26] Y. Li, M.R. Bilad, I.F.J. Vankelecom, Application of a magnetically induced membrane vibration (MMV) system for lignocelluloses hydrolysate filtration, J. Membr. Sci. 452 (2014) 165–170. [27] Y. Zhang, Y. Zhao, H. Chu, X. Zhou, B. Dong, Dewatering of Chlorella pyrenoidosa using diatomite dynamic membrane: filtration performance, membrane fouling and cake behavior, Colloids Surf. B: Biointerfaces 113 (2014) 458–466. [28] M.F.A. Goosen, S.S. Sablani, S.S. Al-Maskari, R.H. Al-Belushi, M. Wilf, Effect of feed temperature on permeate flux and mass transfer coefficient in spiral-wound reverse osmosis systems, Desalination 144 (2002) 367–372. [29] Z. Huang, Y. Qie, Z. Wang, Y. Zhang, W. Zhou, Application of deep-sea psychrotolerant bacteria in wastewater treatment by aerobic dynamic membrane bioreactors at low temperature, J. Membr. Sci. 475 (2015) 47–56. [30] A. Subramani, E. Hoek, Direct observation of initial microbial deposition onto reverse osmosis and nanofiltration membranes, J. Membr. Sci. 319 (2008) 111–125. [31] A. Subramani, X.F. Huang, E. Hoek, Direct observation of bacterial deposition onto clean and organic-fouled polyamide membranes, J. Colloid Interface Sci. 336 (2009) 13–20. [32] S. Kang, A. Subramani, E. Hoek, M. Deshusses, M. Matsumoto, Direct observation of biofouling in cross-flow microfiltration: mechanisms of deposition and release, J. Membr. Sci. 244 (2004) 151–165. [33] F. Qu, H. Liang, J. Tian, H. Yu, Z. Chen, G. Li, Ultrafiltration (UF) membrane fouling caused by cyanobateria: fouling effects of cells and extracellular organics matter (EOM), Desalination 293 (2012) 30–37. [34] F. Han, W. Wang, Y. Li, G. Shen, M. Wan, J. Wang, Changes of biomass, lipid content and fatty acids composition under a light-dark cyclic culture of Chlorella pyrenoidosa in response to different temperature, Bioresour. Technol. 132 (2013) 182–189. [35] F. Zhao, X. Tan, Y. Zhang, H. Chu, L. Yang, X. Zhou, Effect of temperature on the conversion ratio of glucose to Chlorella pyrenoidosa cells: reducing the cost of cultivation, Algal Res. 12 (2015) 431–435. [36] D.J. Smith, G.J. Underwood, The production of extracellular carbohydrates by estuarine benthic diatoms: the effects of growth phase and light and dark treatment, J. Phycol. 36 (2000) 321–333. [37] D.P. Maxwell, S. Falk, C.G. Trick, N.P. Huner, Growth at low temperature mimics high-light acclimation in Chlorella vulgaris, Plant Physiol. 105 (1994) 535–543. [38] K. Wolfstein, L.J. Stal, Production of extracellular polymeric substances (EPS) by benthic diatoms: effect of irradiance and temperature, Mar. Ecol. Prog. Ser. 236 (2002) 13–22. [39] F. Zhao, H. Chu, Y. Su, X. Tan, Y. Zhang, L. Yang, X. Zhou, Microalgae harvesting by an axial vibration membrane: the mechanism of mitigating membrane fouling, J. Membr. Sci. 508 (2016) 127–135.