- Email: [email protected]
Osmotic pressure effect on membrane fouling in a submerged anaerobic membrane bioreactor and its experimental verification
Bioresource Technology 125 (2012) 97–101
Contents lists available at SciVerse ScienceDirect
Bioresource Technology journal homepage: www.elsevier.com/locate/biortech
Short Communication
Osmotic pressure effect on membrane fouling in a submerged anaerobic membrane bioreactor and its experimental verification Jianrong Chen a, Meijia Zhang a, Aijun Wang a, Hongjun Lin a,⇑, Huachang Hong a,⇑, Xiaofeng Lu b a b
College of Geography and Environmental Sciences, Zhejiang Normal University, 688 Yingbin Avenue, Jinhua, Zhejiang Province 321004, PR China Shanghai Institute of Applied Physics, Chinese Academy of Science, Shanghai 201800, PR China
h i g h l i g h t s " Cake layer formed on membrane was hydrated, rich of EPS and negative charged. " A mathematical model of osmotic pressure from cake layer filtration was developed. " Osmotic pressure accounted for the largest fraction of the operation pressure. " Osmotic pressure effect was a major mechanism responsible for fouling in MBRs.
a r t i c l e
i n f o
Article history: Received 5 June 2012 Received in revised form 9 August 2012 Accepted 10 August 2012 Available online 19 August 2012 Keywords: Membrane bioreactor Membrane fouling Extracellular polymeric substances Osmotic pressure
a b s t r a c t A laboratory-scale submerged anaerobic membrane bioreactor (SAnMBR) treating sewage was used to investigate the membrane fouling mechanism. Characterization of cake layer formed on membrane surface showed that cake layer was hydrated, rich of extracellular polymeric substances (EPS) and negative charged with the charge density of 0.21–0.46 meq/kg MLSS. Detailed analysis revealed a new membrane fouling mechanism, osmotic pressure during cake layer filtration process due to the interception of ions. An osmotic pressure model was then developed to elaborate the existence of osmotic pressure and to estimate the contribution of osmotic pressure to membrane fouling. The calculated results showed that osmotic pressure accounted for the largest fraction of total operation pressure, indicating that osmotic pressure generated by the retained ions was one of the major mechanisms responsible for membrane fouling problem in MBRs. These findings provided a new insight into membrane fouling in MBRs. Ó 2012 Elsevier Ltd. All rights reserved.
1. Introduction Membrane bioreactor (MBR) technology offer many advantages over the conventional activated sludge process, and has been considered as one of the most promising processes for wastewater treatment and reclamation in the past decades (Drews, 2010; Huang et al., 2010; Lin et al., 2012; Spagni et al., 2012). However, its widespread application is restricted by membrane fouling (Drews, 2010; Kola et al., 2012; Lin et al., 2012) which reduces productivity and increases operational costs, mainly due to the requirement of extra cleaning and backwashing and increased trans-membrane pressures (TMP) to obtain constant permeate production (Drews, 2010; Huang et al., 2010). The investigation of the mechanism of membrane fouling is essential to the development of effective fouling control strategies for MBRs. ⇑ Corresponding authors. Tel.: +86 579 82282273 (H. Lin), tel.: +86 579 82283589 (H. Hong). E-mail addresses: [email protected] (H. Lin), [email protected] (H. Hong). 0960-8524/$ - see front matter Ó 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.biortech.2012.08.038
In general, cake layer formation is the predominant cause of membrane fouling in a submerged MBR (SMBR) (Cho and Fane, 2002; Lin et al., 2009). The bulk activated sludge in SMBR is apparently the source of cake layer formed on membrane surface. Therefore, the cake layer properties and membrane fouling are highly determined by the activated sludge properties. A generally accepted model of activated sludge consists of aggregated microbial organisms and colonies, embedded in a matrix of extracellular polymeric substances (EPS). EPS typically contains polysaccharides, proteins, humic compounds and nucleic acids (Laspidou and Rittmann, 2002). All these polymeric substances carry negative charged functional groups including carboxyl, phosphoric, amine and hydroxyl groups (Pan et al., 2010), leading to the presence of large concentrations of counter-ions within the matrix of EPS for reasons of electroneutrality (Keiding et al., 2001). It has been reported that the charge density of activated sludge was within the range of 0.28–0.63 meq/ kg VSS (Morgan et al., 1990; Boyette et al., 2001). The specific structure and charged property of EPS would definitely exert an impact on membrane fouling in MBR. However, the mechanism regarding the
98
J. Chen et al. / Bioresource Technology 125 (2012) 97–101
relationship between charged properties of sludge and membrane fouling remains unclear, and deserves further analysis. The osmotic pressure of a dilute solution is conventionally calculated by the Van’t Hoff equation. During process of ultra and/or micro filtration of bulk sludge liquor in MBRs, there is no difference in dissolved salt concentration between the permeate and bulk sludge liquor as ultrafiltration and/or microfiltration membrane used in MBRs can’t retain ions, and thus there is no osmotic pressure difference between these two entities. However, the situation will change after cake layer was formed as a secondary membrane on membrane surface. These counter-ions closely associated with the matrix of EPS in cake layer will not be readily to go through the membrane, thus, the difference in salt concentration between two sides of the membrane will result in a an osmotic gradient. According to the Van’t Hoff equation, any solution with a total species concentration of 0.02 M at 20 °C, will possess an osmotic pressure of 49 kPa. This is in the same order of magnitude as maximal pressure applied in SMBR operation. Theoretically, osmotic pressure is one of the colligative properties of a solution or suspension. Even the introduction of one single particle will reduce the chemical potential of the solvent, and induce an osmotic pressure. From this point of view, it is irrefutable that an osmotic pressure exists in cake layer filtration process in SMBRs. Previous study has mentioned the existence of osmotic pressure generated by the retained macromolecules (Drews, 2010). However, due to their large molecular weight, the retained macromolecules themselves contributed less to the total molar concentration difference between two sides of the membrane. Calculation according to the Van’t Hoff equation showed that the osmotic pressure of the retained macromolecules was in the order of 102 kPa, and thus was negligible as compared to the operational TMP of MBRs. From theoretical analysis, this study pointed out the existence of osmotic pressure during cake layer filtration in MBRs due to the interception of ions in the matrix of cake layer. A comprehensive review of the literature shows that this type osmotic pressure effect has not been well related to membrane fouling in MBRs to date. While osmotic pressure may indeed be an important mechanism regulating TMP development in MBR operation, direct evidence has yet to be found for the actual occurrence of osmotic pressure in an MBR system. Furthermore, the contribution of osmotic pressure to membrane fouling in MBR and its characteristics remain to be investigated. In this study, a mathematical model was developed to describe osmotic pressure effect on membrane fouling in MBR. Thereafter, a lab-scale submerged anaerobic membrane bioreactor was continually operated to determine the related parameters. The contribution of osmotic pressure to membrane fouling was assessed. This study would give a new insight into membrane fouling in MBRs.
2. Methods 2.1. Experimental setup and operation A submerged anaerobic membrane bioreactor (SAnMBR) setup with 80 L total volume (0.35 0.35 0.65 m length width height) and 60 L effective volume was used to treat sewage. A flat sheet membrane module (supplied by Shanghai SINAP Membrane Science & Technology Co. Ltd., China) with a total membrane area of 0.6 m2 was submerged in the reactor. The membrane was made of polyvinylidene fluoride (PVDF) materials and had a nominal pore size of 0.3 lm. At the base of the membrane module, a stainless steel tube diffuser was located, and the headspace biogas in the reactor was recirculated to provide mixing and to control solids deposition over the membrane surface. A level controller together with the pump was used in order to maintain a constant water level in the
reactor. The membrane-filtered effluent was intermittently obtained by suction using a peristaltic pump connected to the modules operating in the mode of 9-min-on and 1-min-off. All electric devices were connected to a programmable logic controller (PLC) to automatically control the whole system. The setup was fed by sewage obtained from the local town with an average COD of approximately 425 mg/L, and an adjusted pH of 6.5–7.0. The SAnMBR apparatus was run continuously for about 160 days, and HRT was controlled to be approximately 10 h. The applied membrane flux during steady state operation period was about 11 L/(h m2) (LHM). 2.2. Analytical methods 2.2.1. EPS extraction and measurement The extraction of bound extracellular polymeric substances (EPS) of bulk sludge and cake sludge was based on a cation exchange resin (CER) (DowexÒ MarathonÒ C, Na+ form, Sigma–Aldrich, Bellefonte, PA) method. The EPS were normalized as the sum of protein (PN) and polysaccharide (PS) which was measured colorimetrically by using phenol/sulphuric acid method and Folin’s method, respectively. Bovine serum albumin (BSA) was used as a protein standard, and glucose was used as a polysaccharide standard. The operational details can refer to the pervious study (Lin et al., 2009). 2.2.2. Surface charge determination The surface charge of sludge was determined by colloidal titration (Morgan et al., 1990). Al1 the solutions were adjusted to neutrality prior to titration. Polybrene (0.002 N) and the potassium salt of polyvinyl sulphate (PVSK) (0.001 N) (all chemicals from Sigma, analytical grade) were used as the cationic and anionic standards, respectively. A known amount of cake sludge sample (4 mL, about 2000 mg/L) was diluted with deionized distilled water with an adjusted pH of 7.0 and mixed with an excess amount of Polybrene standard solution. The PVSK standard solution was then used to titrate against the excess amount of polybrene using 0.1% (w/v) toluidine blue as an indicator. The endpoint was indicated by a subtle color change from blue to purple. An equal volume of Polybrene standard solution diluted with the same amount of deionized distilled water for each titration series was used as a blank. 2.2.3. Cake layer porosity determination The fresh cake layer obtained from reactor was observed by conventional optical microscopy (Olympus, Japan). The images were acquired as JEPG format. Thereafter, the images were transferred to gray-scale formation (256 gray-scale levels) with Adobe Photoshop CS3 software. Before analyzing an image, a threshold has to be determined in order to distinguish pores from the background, obtaining a binary image. For each binary image, threshold was estimated as the gray level value that corresponded to that maximum of the gray level histogram second derivation. The porosity of cake layer was determined by analyzing the binary images. For more details refer to Meng et al. (2005). 2.2.4. Water content measurement The water content of cake layer was measured by generally drying the samples in an oven at 105 °C for 12 h. The samples was dried and weighed to determine the water content which was expressed in terms of the mass of water per unit mass of the wet sample. 2.2.5. Water quality measurements Samples of influent and effluent were taken periodically from the system. Parameters, such as chemical oxygen demand (COD), total suspended solids (TSS), turbidity, mixed liquor suspended
J. Chen et al. / Bioresource Technology 125 (2012) 97–101
solids (MLSS) and conductivity, were analyzed as defined in standard methods (APHA, 2005). 2.3. Model development Membrane fouling in MBRs can usually be described by using the followed classical fouling models: pore constriction, pore blockage and cake filtration. Each of these models is based on a generalized form of Darcy’s law, with TMP (DP) expressed as:
DP ¼ lJðRm þ Rc Þ
ð1Þ
Where l is the filtrate viscosity; J is the filtrate flux, which is usually set at a constant value for modern MBR operation; Rm and Rc are the resistance of membrane and cake layer, respectively. As mentioned above, previous studies missed taking into account osmotic pressure effect that originated from cake layer formation during MBR operation. The charged property of cake layer will presQ ent an osmotic pressure (D c). Combined with this effect, DP can be expressed as:
DP ¼ lJðRm þ Rc Þ þ DPc
DPc ¼ DC R T
ð3Þ
Where DC is the species concentration difference between the filter cake and the permeate; R is the universal gas constant; T is absolute temperature. Fig. 1 shows the schematic diagram of cake layer structure formed on membrane surface. The cake layer was highly hydrated, and was assumed to be a homogeneous ions solution. It can be seen from Fig. 1, the relationship between the total volume of cake layer (Vt) and the total cell and solid volume (Vc), and the water volume (Vw) in the cake layer then can be given by Eqs. (4) and (5), respectively:
V c ¼ V t ð1 eÞ
ð4Þ
Vw ¼ Vte
ð5Þ
where e is the porosity of the cake layer. Cake layer surface charges arise from the dissociation of functional groups which is governed by a dissociation constant (Ka). For example, the dissociation equation of the carboxyl group (functional group abundant in EPS) can be expressed as: – COOH=–COO+H+. A dissociation number d, indicating the fraction of ionisable functional groups that are effectively dissociated, can be expressed as:
Permeate Flow +
+ + + +
+
+
+
+ +
+
+
Colloidal particle
+
+
+
+
+ +
Membrane
+ +
+
+ +
+ + +
Sludge floc
+
+ +
Ka K a þ 10pH
ð6Þ
By assuming that dissolved neutral species do not contribute to the molar concentration difference between the cake layer and the permeate (the molar concentration of these species is low enough to be ignored), and the permeate posses an ion concentration Cp, DC can be calculated as:
DC ¼
drqV t ð1 eÞ C p ¼ drqð1 eÞ=e C p Vte
ð7Þ
Where r is the charge density, reflecting the total concentration of available ionisable groups in cake layer, q is the cake layer density. Substituting Eqs. (6) and (7) into Eq. (3), gives the osmotic pressure model:
DPc ¼ K a rqRTð1 eÞ=eðK a þ 10pH Þ C p RT
ð8Þ
Therefore, TMP during MBR operation can be expressed as:
DP ¼ lJRm þ lJRc þ K a rqRTð1 eÞ=eðK a þ 10pH Þ C p RT
ð9Þ
ð2Þ
The osmotic pressure of a dilute solution can be given by Van’t Hoff equation (Eq. (3)), which is derived from chemical potential difference between two entities of membrane. It requires dilute solution because dilute solution follows Raoult law, namly, RTln (1 DC) RTDC.
Cake layer
d¼
99
Cation
+ +
Solutes
Fig. 1. Schematic diagram of cake layer structure formed on membrane surface.
3. Results and discussion 3.1. Process performance The SAnMBR setup was continuously run for about 160 days for sewage treatment. Results showed that SAnMBR operated at steady state was effective in removing approximately 90% of COD, 99% of TSS and turbidity in the sewage. During the stable operation period, sludge and methane yield rates were determined to be about 0.032 kg MLSS/kg COD and 0.23–0.26 LCH4/gCOD, respectively. These results indicated that SAnMBR was an attractive option for sewage treatment as it combined pollution reduction and energy production. Under operation condition, a sustainable membrane flux of 11 LHM was achieved, comparable with the literature data under anaerobic conditions (Robles et al., 2012). Membrane becoming severely fouled (TMP reached 50–60 kPa) typically required 10–20 days. The cake layers formed on membrane surface at the operation termination (as TMP reached 50–60 kPa) in the different evolution cycles were taken out from reactor for characterization. 3.2. Cake formation and its characteristics The growth of cake layer induced an increase in cake layer thickness, which appeared to be a key parameter determining filtration resistance. However, the thickness of cake layer did not always coincide with the membrane fouling development. This study observed that the initial increase in cake thickness from 0 to about 340 lm corresponded to low membrane fouling rate (about 7.2 1010 m/d), while such an increase in later filtration period (from 340 lm to about 610 lm) corresponded to an over two orders of magnitude higher membrane fouling rate (about 1.7 1013 m/d). The results suggested that, besides cake layer thickness, some other characteristics of cake layer would also determine membrane fouling development. Water content (at 25 °C) of the prepared cake sludge samples was measured to be 91–97%. A centrifuge process could not significantly decrease the water content in cake layer. The results indicated that, apart from the water in cells, water in cake layer was bound. The highly hydrated property of cake layer indicated the existence of some kind of forces pulling the water. The cake sludge was believed to consist of micro-organisms embedded in a matrix of EPS. A further analysis on EPS content was therefore conducted. Fig. 2 showed the comparison of EPS content between cake sludge and bulk sludge. Statistical analysis using analysis of variance (ANOVA) verified that the difference in EPS content between the cake
100
J. Chen et al. / Bioresource Technology 125 (2012) 97–101
Concentration (mg/gMLSS)
100 Bulk sludge 80
Cake sludge
60 40 20 0 Protein
Polysaccharide
Total EPS
Fig. 2. Comparison of EPS content between bulk sludge and cake sludge.
and bulk sludge samples was statistically significant (p < 0.01). Nevertheless, this result indicated that the formed cake layer was rich of EPS which might play a key role in cake formation process. Titration analysis showed that the cake layer formed on membrane surface was negative charged, with the charge density varied between 0.21–0.46 meq/kg MLSS. The result is in line with previous studies (Morgan et al., 1990; Boyette et al., 2001). The charge of cake layer apparently originated from the charge of EPS. It’s well known that the EPS is kind of polyelectrolyte gel (Laspidou and Rittmann, 2002). When a piece of such gel is immersed in a large amount of water, the counter-ions cannot escape outside the gel because of the condition of macroscopic electro-neutrality. Being forced to reside inside the gel, they try to occupy as much volume as possible because in this way they gain some translational entropy (Zeldovich and Khokhlov, 1998). As a result, the cake layer showed to be hydrated. When the cake layer is subjected to filtration, the counter-ions associated with EPS will create a difference in chemical potential between two entities of membrane, which will resist free water escape. Osmosis is one manifestation of chemical potential of a solution. In this regarding, the existence of osmotic pressure during the cake layer filtration process cannot be denied. It should be noted that the mechanism in this study is totally different from the osmotic pressure proposed by Hoek and Elimelech (2003). The involved mechanisms in their study are a combination of hindered back-diffusion of salt ions and altered cross-flow hydrodynamics within colloidal deposit layers on reverse osmosis (RO) membrane, which lead to an enhanced salt concentration polarization layer. From cake layer characterization, this study presented clear experimental evidence that cake layer was negative charged, and would provide an osmotic pressure influencing membrane fouling. However, the degree of this influence remained to be identified.
3.3. Role of osmotic pressure in membrane fouling This study developed a mathematical model which clearly demonstrated the mechanism of osmotic pressure. Moreover, this model provided a way to calculate the value of osmotic pressure which could not be directly measured. The osmotic pressure in the cake layer filtration can be calculated according to Eq. (8), provided that cake layer characterization and some assumptions were made. In this study, pKa value was assumed to be 7.2 since the most abundant amino acids in activated sludge EPS are glutamic acid (12.4%), aspartic acid (11.7%), alanine (8.2%) and leucine (7.5%) with the pKa values of 4.07 (side chain), 3.86, 9.69 and 9.60, respectively (Dignac et al., 1998). The porosity of cake layer was measured to be ranged from 0.32 to 0.49. Due to porosity measurement method based on image analysis cannot count the small pores that real exist but not appear in the image, the measured porosity value should be
lower than the real situation. Therefore, an upper limit of porosity value of 0.49 was adopted. Charge density of cake layer sludge was measured to be in the range of 0.21–0.46 meq/kg MLSS with an average value of approximately 0.28 meq/kg MLSS. Operational temperature and pH were 25 °C and 6.5, respectively. Considering that water content accounts for 91–97% of total weight of cake layer, cake layer density was assumed to be 1.06 g/mL. Permeate ion concentration was assumed to be 0.004 mol/L in consideration of permeate conductivity data. Based on these experimental data and assumptions, the osmotic pressure was calculated as 33.7 kPa according to Eq. (8). At same time, the formed cake layer corresponded to a TMP of about 54 kpa. This means that about 62.4% of TMP originated from osmotic pressure effect. Moreover, such a calculation was conservative. For example, if porosity of the cake layer was assumed to be 0.35, the calculated osmotic pressure would be 71.1 kPa, even larger than the total TMP. It should be noted that the osmotic pressure model was developed based on the assumption that cake layer was homogeneous and distributed evenly on membrane surface. However, many studies have observed an opposite distributed cake layer on membrane surface (Cho and Fane, 2002; Gao et al., 2011). This situation would cause the calculated osmotic pressure to be overestimated to some extent in this study. Nevertheless, this result indicated osmotic pressure could not be ignored once a cake layer formed on membrane surface. The formed cake layer can be viewed as a porous media providing an additional barrier for filtration of the bulk suspension. According to Carman–Kozeny equation, which is the most famous permeability-porosity relation widely used in the field of flow in porous media, the cake layer in this study (610 lm thickness, 0.50 porosity, 6 lm deposited particle size) will induce an operation pressure less than 0.5 ka, which is only about one percent of the final TMP (54 kpa) obtained in the experiments. Current known membrane fouling mechanisms, including pore plugging/clogging by colloidal particles, adsorption of soluble compounds and biofouling, deposition of solids as a cake layer, cake layer consolidation and the spatial and temporal changes of the foulant composition, could not satisfactorily explain the big gap between calculation result and experimental data. This study reveals a new membrane fouling mechanism, osmotic pressure of cake layer filtration. Calculation shows that osmotic pressure of cake layer filtration accounts for the largest fraction of operational TMP, thus offering a more reasonable explanation for the membrane fouling phenomenon in MBRs. Such a comparison verified the proposed model’s feasibility to some extent. Conductivity analysis showed that conductivity of influent was continuously 4–15% higher than that of effluent (24 measurements during 8 days). Considering the low anaerobic sludge yield, this result indicated that certain amount of ions was adsorbed or intercepted in the matrix of cake layer as well as sludge flocs. As argued above, osmotic pressure originated from the interception of ions in the matrix of cake layer. Conductivity data provided direct evidences verifying the existence of osmotic pressure of cake layer filtration, although further studies are needed in order to better understand osmotic pressure and develop effective control strategies.
4. Conclusions SAnMBR could effectively remove approximately 90% of COD, 99% of TSS and turbidity in the sewage during the stable operation period. The cake layer formed on membrane surface was hydrated, rich of EPS and negative charged. It was found that osmotic pressure existed during cake layer filtration process due to the interception of ions. An osmotic pressure model was then developed, and the calculation results indicated that osmotic pressure was
J. Chen et al. / Bioresource Technology 125 (2012) 97–101
one of the major mechanisms responsible for membrane fouling problem in MBRs. This study gave a new insight into membrane fouling in MBRs. Acknowledgements Financial support of National Natural Science Foundation of China (No. 51108424, 21107099, 21275130), Qianjiang Talent Project of Zhejiang Province (No. 2012R10061) and Department of Education of Zhejiang Province (No. Y201121142) is highly appreciated. References APHA, 2005. Standard Methods for the Examination of Water and Wastewater, twentieth ed. American Public Health Association, American Water Works Association, Water Environmental Federation, Washington, USA. Boyette, S.M., Lovett, J.M., Gaboda, W.G., Soares, J.A., 2001. Cell surface and exopolymer characterization of laboratory stabilized activated sludge from a beverage bottling plant. Water Sci. Technol. 43 (6), 174–184. Cho, B.D., Fane, A.G., 2002. Fouling transients in nominally sub-critical flux operation of a membrane bioreactor. J. Membr. Sci. 209 (2), 391–403. Dignac, M.F., Urbain, V., Rybacki, D., Bruchet, A., Snidaro, D., Scribe, P., 1998. Chemical description of extracellular polymers: Implication on activated sludge floc structure. Water Sci. Technol. 38 (8–9), 45–53. Drews, A., 2010. Membrane fouling in membrane bioreactors - characterisation, contradictions, cause and cures. J. Membr. Sci. 363 (1–2), 1–28. Gao, W.J., Lin, H.J., Leung, K.T., Schraft, H., Liao, B.Q., 2011. Structure of cake layer in a submerged anaerobic membrane bioreactor. J. Membr. Sci. 374 (1–2), 110– 120. Hoek, E.M., Elimelech, M., 2003. Cake-enhanced concentration polarization: a new fouling mechanism for salt-rejecting membranes. Environ. Sci. Technol. 37 (24), 5581–5588.
101
Huang, X., Xiao, K., Shen, Y.X., 2010. Recent advances in membrane bioreactor technology for wastewater treatment in China. Front. Environ. Sci. Eng. China 4 (3), 245–271. Keiding, K., Wybrandt, L., Nielsen, P.H., 2001. Remember the water - a comment on EPS colligative properties. Water Sci. Technol. 43 (6), 17–23. Kola, A., Ye, Y., Ho, A., Le-Clech, P., Chen, V.K., 2012. Application of low frequency transverse vibration on fouling limitation in submerged hollow fibre membranes. J. Membr. Sci. 409, 54–65. Laspidou, C.S., Rittmann, B.E., 2002. A unified theory for extracellular polymeric substances, soluble microbial products, and active and inert biomass. Water Res. 36 (11), 2711–2720. Lin, H., Gao, W., Meng, F., Liao, B.-Q., Leung, K.-T., Zhao, L., Chen, J., Hong, H., 2012. Membrane bioreactors for industrial wastewater treatment: a critical review. Crit. Rev. Environ. Sci. Technol. 42 (7), 677–740. Lin, H.J., Xie, K., Mahendran, B., Bagley, D.M., Leung, K.T., Liss, S.N., Liao, B.Q., 2009. Sludge properties and their effects on membrane fouling in submerged anaerobic membrane bioreactors (SAnMBRs). Water Res. 43 (15), 3827–3837. Meng, F., Zhang, H., Li, Y., Zhang, X., Yang, F., 2005. Application of fractal permeation model to investigate membrane fouling in membrane bioreactor. J. Membr. Sci. 262 (1–2), 107–116. Morgan, J.W., Forster, C.F., Evison, L., 1990. A comparative study of the nature of biopolymers extracted from anaerobic and activated sludges. Water Res. 24 (6), 743–750. Pan, X., Liu, J., Zhang, D., 2010. Binding of phenanthrene to extracellular polymeric substances (EPS) from aerobic activated sludge: a fluorescence study. Colloids Surf. B 80 (1), 103–106. Robles, A., Ruano, M.V., García-Usach, F., Ferrer, J., 2012. Sub-critical filtration conditions of commercial hollow-fibre membranes in a submerged anaerobic MBR (HF-SAnMBR) system: the effect of gas sparging intensity. Bioresour. Technol. 114, 247–254. Spagni, A., Casu, S., Grilli, S., 2012. Decolourisation of textile wastewater in a submerged anaerobic membrane bioreactor. Bioresour. Technol. 117, 180–185. Zeldovich, K.B., Khokhlov, A.R., 1998. Osmotically active and passive counterions in inhomogeneous polymer gels. Macromolecules 32 (10), 3488–3494.
Contents lists available at SciVerse ScienceDirect
Bioresource Technology journal homepage: www.elsevier.com/locate/biortech
Short Communication
Osmotic pressure effect on membrane fouling in a submerged anaerobic membrane bioreactor and its experimental verification Jianrong Chen a, Meijia Zhang a, Aijun Wang a, Hongjun Lin a,⇑, Huachang Hong a,⇑, Xiaofeng Lu b a b
College of Geography and Environmental Sciences, Zhejiang Normal University, 688 Yingbin Avenue, Jinhua, Zhejiang Province 321004, PR China Shanghai Institute of Applied Physics, Chinese Academy of Science, Shanghai 201800, PR China
h i g h l i g h t s " Cake layer formed on membrane was hydrated, rich of EPS and negative charged. " A mathematical model of osmotic pressure from cake layer filtration was developed. " Osmotic pressure accounted for the largest fraction of the operation pressure. " Osmotic pressure effect was a major mechanism responsible for fouling in MBRs.
a r t i c l e
i n f o
Article history: Received 5 June 2012 Received in revised form 9 August 2012 Accepted 10 August 2012 Available online 19 August 2012 Keywords: Membrane bioreactor Membrane fouling Extracellular polymeric substances Osmotic pressure
a b s t r a c t A laboratory-scale submerged anaerobic membrane bioreactor (SAnMBR) treating sewage was used to investigate the membrane fouling mechanism. Characterization of cake layer formed on membrane surface showed that cake layer was hydrated, rich of extracellular polymeric substances (EPS) and negative charged with the charge density of 0.21–0.46 meq/kg MLSS. Detailed analysis revealed a new membrane fouling mechanism, osmotic pressure during cake layer filtration process due to the interception of ions. An osmotic pressure model was then developed to elaborate the existence of osmotic pressure and to estimate the contribution of osmotic pressure to membrane fouling. The calculated results showed that osmotic pressure accounted for the largest fraction of total operation pressure, indicating that osmotic pressure generated by the retained ions was one of the major mechanisms responsible for membrane fouling problem in MBRs. These findings provided a new insight into membrane fouling in MBRs. Ó 2012 Elsevier Ltd. All rights reserved.
1. Introduction Membrane bioreactor (MBR) technology offer many advantages over the conventional activated sludge process, and has been considered as one of the most promising processes for wastewater treatment and reclamation in the past decades (Drews, 2010; Huang et al., 2010; Lin et al., 2012; Spagni et al., 2012). However, its widespread application is restricted by membrane fouling (Drews, 2010; Kola et al., 2012; Lin et al., 2012) which reduces productivity and increases operational costs, mainly due to the requirement of extra cleaning and backwashing and increased trans-membrane pressures (TMP) to obtain constant permeate production (Drews, 2010; Huang et al., 2010). The investigation of the mechanism of membrane fouling is essential to the development of effective fouling control strategies for MBRs. ⇑ Corresponding authors. Tel.: +86 579 82282273 (H. Lin), tel.: +86 579 82283589 (H. Hong). E-mail addresses: [email protected] (H. Lin), [email protected] (H. Hong). 0960-8524/$ - see front matter Ó 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.biortech.2012.08.038
In general, cake layer formation is the predominant cause of membrane fouling in a submerged MBR (SMBR) (Cho and Fane, 2002; Lin et al., 2009). The bulk activated sludge in SMBR is apparently the source of cake layer formed on membrane surface. Therefore, the cake layer properties and membrane fouling are highly determined by the activated sludge properties. A generally accepted model of activated sludge consists of aggregated microbial organisms and colonies, embedded in a matrix of extracellular polymeric substances (EPS). EPS typically contains polysaccharides, proteins, humic compounds and nucleic acids (Laspidou and Rittmann, 2002). All these polymeric substances carry negative charged functional groups including carboxyl, phosphoric, amine and hydroxyl groups (Pan et al., 2010), leading to the presence of large concentrations of counter-ions within the matrix of EPS for reasons of electroneutrality (Keiding et al., 2001). It has been reported that the charge density of activated sludge was within the range of 0.28–0.63 meq/ kg VSS (Morgan et al., 1990; Boyette et al., 2001). The specific structure and charged property of EPS would definitely exert an impact on membrane fouling in MBR. However, the mechanism regarding the
98
J. Chen et al. / Bioresource Technology 125 (2012) 97–101
relationship between charged properties of sludge and membrane fouling remains unclear, and deserves further analysis. The osmotic pressure of a dilute solution is conventionally calculated by the Van’t Hoff equation. During process of ultra and/or micro filtration of bulk sludge liquor in MBRs, there is no difference in dissolved salt concentration between the permeate and bulk sludge liquor as ultrafiltration and/or microfiltration membrane used in MBRs can’t retain ions, and thus there is no osmotic pressure difference between these two entities. However, the situation will change after cake layer was formed as a secondary membrane on membrane surface. These counter-ions closely associated with the matrix of EPS in cake layer will not be readily to go through the membrane, thus, the difference in salt concentration between two sides of the membrane will result in a an osmotic gradient. According to the Van’t Hoff equation, any solution with a total species concentration of 0.02 M at 20 °C, will possess an osmotic pressure of 49 kPa. This is in the same order of magnitude as maximal pressure applied in SMBR operation. Theoretically, osmotic pressure is one of the colligative properties of a solution or suspension. Even the introduction of one single particle will reduce the chemical potential of the solvent, and induce an osmotic pressure. From this point of view, it is irrefutable that an osmotic pressure exists in cake layer filtration process in SMBRs. Previous study has mentioned the existence of osmotic pressure generated by the retained macromolecules (Drews, 2010). However, due to their large molecular weight, the retained macromolecules themselves contributed less to the total molar concentration difference between two sides of the membrane. Calculation according to the Van’t Hoff equation showed that the osmotic pressure of the retained macromolecules was in the order of 102 kPa, and thus was negligible as compared to the operational TMP of MBRs. From theoretical analysis, this study pointed out the existence of osmotic pressure during cake layer filtration in MBRs due to the interception of ions in the matrix of cake layer. A comprehensive review of the literature shows that this type osmotic pressure effect has not been well related to membrane fouling in MBRs to date. While osmotic pressure may indeed be an important mechanism regulating TMP development in MBR operation, direct evidence has yet to be found for the actual occurrence of osmotic pressure in an MBR system. Furthermore, the contribution of osmotic pressure to membrane fouling in MBR and its characteristics remain to be investigated. In this study, a mathematical model was developed to describe osmotic pressure effect on membrane fouling in MBR. Thereafter, a lab-scale submerged anaerobic membrane bioreactor was continually operated to determine the related parameters. The contribution of osmotic pressure to membrane fouling was assessed. This study would give a new insight into membrane fouling in MBRs.
2. Methods 2.1. Experimental setup and operation A submerged anaerobic membrane bioreactor (SAnMBR) setup with 80 L total volume (0.35 0.35 0.65 m length width height) and 60 L effective volume was used to treat sewage. A flat sheet membrane module (supplied by Shanghai SINAP Membrane Science & Technology Co. Ltd., China) with a total membrane area of 0.6 m2 was submerged in the reactor. The membrane was made of polyvinylidene fluoride (PVDF) materials and had a nominal pore size of 0.3 lm. At the base of the membrane module, a stainless steel tube diffuser was located, and the headspace biogas in the reactor was recirculated to provide mixing and to control solids deposition over the membrane surface. A level controller together with the pump was used in order to maintain a constant water level in the
reactor. The membrane-filtered effluent was intermittently obtained by suction using a peristaltic pump connected to the modules operating in the mode of 9-min-on and 1-min-off. All electric devices were connected to a programmable logic controller (PLC) to automatically control the whole system. The setup was fed by sewage obtained from the local town with an average COD of approximately 425 mg/L, and an adjusted pH of 6.5–7.0. The SAnMBR apparatus was run continuously for about 160 days, and HRT was controlled to be approximately 10 h. The applied membrane flux during steady state operation period was about 11 L/(h m2) (LHM). 2.2. Analytical methods 2.2.1. EPS extraction and measurement The extraction of bound extracellular polymeric substances (EPS) of bulk sludge and cake sludge was based on a cation exchange resin (CER) (DowexÒ MarathonÒ C, Na+ form, Sigma–Aldrich, Bellefonte, PA) method. The EPS were normalized as the sum of protein (PN) and polysaccharide (PS) which was measured colorimetrically by using phenol/sulphuric acid method and Folin’s method, respectively. Bovine serum albumin (BSA) was used as a protein standard, and glucose was used as a polysaccharide standard. The operational details can refer to the pervious study (Lin et al., 2009). 2.2.2. Surface charge determination The surface charge of sludge was determined by colloidal titration (Morgan et al., 1990). Al1 the solutions were adjusted to neutrality prior to titration. Polybrene (0.002 N) and the potassium salt of polyvinyl sulphate (PVSK) (0.001 N) (all chemicals from Sigma, analytical grade) were used as the cationic and anionic standards, respectively. A known amount of cake sludge sample (4 mL, about 2000 mg/L) was diluted with deionized distilled water with an adjusted pH of 7.0 and mixed with an excess amount of Polybrene standard solution. The PVSK standard solution was then used to titrate against the excess amount of polybrene using 0.1% (w/v) toluidine blue as an indicator. The endpoint was indicated by a subtle color change from blue to purple. An equal volume of Polybrene standard solution diluted with the same amount of deionized distilled water for each titration series was used as a blank. 2.2.3. Cake layer porosity determination The fresh cake layer obtained from reactor was observed by conventional optical microscopy (Olympus, Japan). The images were acquired as JEPG format. Thereafter, the images were transferred to gray-scale formation (256 gray-scale levels) with Adobe Photoshop CS3 software. Before analyzing an image, a threshold has to be determined in order to distinguish pores from the background, obtaining a binary image. For each binary image, threshold was estimated as the gray level value that corresponded to that maximum of the gray level histogram second derivation. The porosity of cake layer was determined by analyzing the binary images. For more details refer to Meng et al. (2005). 2.2.4. Water content measurement The water content of cake layer was measured by generally drying the samples in an oven at 105 °C for 12 h. The samples was dried and weighed to determine the water content which was expressed in terms of the mass of water per unit mass of the wet sample. 2.2.5. Water quality measurements Samples of influent and effluent were taken periodically from the system. Parameters, such as chemical oxygen demand (COD), total suspended solids (TSS), turbidity, mixed liquor suspended
J. Chen et al. / Bioresource Technology 125 (2012) 97–101
solids (MLSS) and conductivity, were analyzed as defined in standard methods (APHA, 2005). 2.3. Model development Membrane fouling in MBRs can usually be described by using the followed classical fouling models: pore constriction, pore blockage and cake filtration. Each of these models is based on a generalized form of Darcy’s law, with TMP (DP) expressed as:
DP ¼ lJðRm þ Rc Þ
ð1Þ
Where l is the filtrate viscosity; J is the filtrate flux, which is usually set at a constant value for modern MBR operation; Rm and Rc are the resistance of membrane and cake layer, respectively. As mentioned above, previous studies missed taking into account osmotic pressure effect that originated from cake layer formation during MBR operation. The charged property of cake layer will presQ ent an osmotic pressure (D c). Combined with this effect, DP can be expressed as:
DP ¼ lJðRm þ Rc Þ þ DPc
DPc ¼ DC R T
ð3Þ
Where DC is the species concentration difference between the filter cake and the permeate; R is the universal gas constant; T is absolute temperature. Fig. 1 shows the schematic diagram of cake layer structure formed on membrane surface. The cake layer was highly hydrated, and was assumed to be a homogeneous ions solution. It can be seen from Fig. 1, the relationship between the total volume of cake layer (Vt) and the total cell and solid volume (Vc), and the water volume (Vw) in the cake layer then can be given by Eqs. (4) and (5), respectively:
V c ¼ V t ð1 eÞ
ð4Þ
Vw ¼ Vte
ð5Þ
where e is the porosity of the cake layer. Cake layer surface charges arise from the dissociation of functional groups which is governed by a dissociation constant (Ka). For example, the dissociation equation of the carboxyl group (functional group abundant in EPS) can be expressed as: – COOH=–COO+H+. A dissociation number d, indicating the fraction of ionisable functional groups that are effectively dissociated, can be expressed as:
Permeate Flow +
+ + + +
+
+
+
+ +
+
+
Colloidal particle
+
+
+
+
+ +
Membrane
+ +
+
+ +
+ + +
Sludge floc
+
+ +
Ka K a þ 10pH
ð6Þ
By assuming that dissolved neutral species do not contribute to the molar concentration difference between the cake layer and the permeate (the molar concentration of these species is low enough to be ignored), and the permeate posses an ion concentration Cp, DC can be calculated as:
DC ¼
drqV t ð1 eÞ C p ¼ drqð1 eÞ=e C p Vte
ð7Þ
Where r is the charge density, reflecting the total concentration of available ionisable groups in cake layer, q is the cake layer density. Substituting Eqs. (6) and (7) into Eq. (3), gives the osmotic pressure model:
DPc ¼ K a rqRTð1 eÞ=eðK a þ 10pH Þ C p RT
ð8Þ
Therefore, TMP during MBR operation can be expressed as:
DP ¼ lJRm þ lJRc þ K a rqRTð1 eÞ=eðK a þ 10pH Þ C p RT
ð9Þ
ð2Þ
The osmotic pressure of a dilute solution can be given by Van’t Hoff equation (Eq. (3)), which is derived from chemical potential difference between two entities of membrane. It requires dilute solution because dilute solution follows Raoult law, namly, RTln (1 DC) RTDC.
Cake layer
d¼
99
Cation
+ +
Solutes
Fig. 1. Schematic diagram of cake layer structure formed on membrane surface.
3. Results and discussion 3.1. Process performance The SAnMBR setup was continuously run for about 160 days for sewage treatment. Results showed that SAnMBR operated at steady state was effective in removing approximately 90% of COD, 99% of TSS and turbidity in the sewage. During the stable operation period, sludge and methane yield rates were determined to be about 0.032 kg MLSS/kg COD and 0.23–0.26 LCH4/gCOD, respectively. These results indicated that SAnMBR was an attractive option for sewage treatment as it combined pollution reduction and energy production. Under operation condition, a sustainable membrane flux of 11 LHM was achieved, comparable with the literature data under anaerobic conditions (Robles et al., 2012). Membrane becoming severely fouled (TMP reached 50–60 kPa) typically required 10–20 days. The cake layers formed on membrane surface at the operation termination (as TMP reached 50–60 kPa) in the different evolution cycles were taken out from reactor for characterization. 3.2. Cake formation and its characteristics The growth of cake layer induced an increase in cake layer thickness, which appeared to be a key parameter determining filtration resistance. However, the thickness of cake layer did not always coincide with the membrane fouling development. This study observed that the initial increase in cake thickness from 0 to about 340 lm corresponded to low membrane fouling rate (about 7.2 1010 m/d), while such an increase in later filtration period (from 340 lm to about 610 lm) corresponded to an over two orders of magnitude higher membrane fouling rate (about 1.7 1013 m/d). The results suggested that, besides cake layer thickness, some other characteristics of cake layer would also determine membrane fouling development. Water content (at 25 °C) of the prepared cake sludge samples was measured to be 91–97%. A centrifuge process could not significantly decrease the water content in cake layer. The results indicated that, apart from the water in cells, water in cake layer was bound. The highly hydrated property of cake layer indicated the existence of some kind of forces pulling the water. The cake sludge was believed to consist of micro-organisms embedded in a matrix of EPS. A further analysis on EPS content was therefore conducted. Fig. 2 showed the comparison of EPS content between cake sludge and bulk sludge. Statistical analysis using analysis of variance (ANOVA) verified that the difference in EPS content between the cake
100
J. Chen et al. / Bioresource Technology 125 (2012) 97–101
Concentration (mg/gMLSS)
100 Bulk sludge 80
Cake sludge
60 40 20 0 Protein
Polysaccharide
Total EPS
Fig. 2. Comparison of EPS content between bulk sludge and cake sludge.
and bulk sludge samples was statistically significant (p < 0.01). Nevertheless, this result indicated that the formed cake layer was rich of EPS which might play a key role in cake formation process. Titration analysis showed that the cake layer formed on membrane surface was negative charged, with the charge density varied between 0.21–0.46 meq/kg MLSS. The result is in line with previous studies (Morgan et al., 1990; Boyette et al., 2001). The charge of cake layer apparently originated from the charge of EPS. It’s well known that the EPS is kind of polyelectrolyte gel (Laspidou and Rittmann, 2002). When a piece of such gel is immersed in a large amount of water, the counter-ions cannot escape outside the gel because of the condition of macroscopic electro-neutrality. Being forced to reside inside the gel, they try to occupy as much volume as possible because in this way they gain some translational entropy (Zeldovich and Khokhlov, 1998). As a result, the cake layer showed to be hydrated. When the cake layer is subjected to filtration, the counter-ions associated with EPS will create a difference in chemical potential between two entities of membrane, which will resist free water escape. Osmosis is one manifestation of chemical potential of a solution. In this regarding, the existence of osmotic pressure during the cake layer filtration process cannot be denied. It should be noted that the mechanism in this study is totally different from the osmotic pressure proposed by Hoek and Elimelech (2003). The involved mechanisms in their study are a combination of hindered back-diffusion of salt ions and altered cross-flow hydrodynamics within colloidal deposit layers on reverse osmosis (RO) membrane, which lead to an enhanced salt concentration polarization layer. From cake layer characterization, this study presented clear experimental evidence that cake layer was negative charged, and would provide an osmotic pressure influencing membrane fouling. However, the degree of this influence remained to be identified.
3.3. Role of osmotic pressure in membrane fouling This study developed a mathematical model which clearly demonstrated the mechanism of osmotic pressure. Moreover, this model provided a way to calculate the value of osmotic pressure which could not be directly measured. The osmotic pressure in the cake layer filtration can be calculated according to Eq. (8), provided that cake layer characterization and some assumptions were made. In this study, pKa value was assumed to be 7.2 since the most abundant amino acids in activated sludge EPS are glutamic acid (12.4%), aspartic acid (11.7%), alanine (8.2%) and leucine (7.5%) with the pKa values of 4.07 (side chain), 3.86, 9.69 and 9.60, respectively (Dignac et al., 1998). The porosity of cake layer was measured to be ranged from 0.32 to 0.49. Due to porosity measurement method based on image analysis cannot count the small pores that real exist but not appear in the image, the measured porosity value should be
lower than the real situation. Therefore, an upper limit of porosity value of 0.49 was adopted. Charge density of cake layer sludge was measured to be in the range of 0.21–0.46 meq/kg MLSS with an average value of approximately 0.28 meq/kg MLSS. Operational temperature and pH were 25 °C and 6.5, respectively. Considering that water content accounts for 91–97% of total weight of cake layer, cake layer density was assumed to be 1.06 g/mL. Permeate ion concentration was assumed to be 0.004 mol/L in consideration of permeate conductivity data. Based on these experimental data and assumptions, the osmotic pressure was calculated as 33.7 kPa according to Eq. (8). At same time, the formed cake layer corresponded to a TMP of about 54 kpa. This means that about 62.4% of TMP originated from osmotic pressure effect. Moreover, such a calculation was conservative. For example, if porosity of the cake layer was assumed to be 0.35, the calculated osmotic pressure would be 71.1 kPa, even larger than the total TMP. It should be noted that the osmotic pressure model was developed based on the assumption that cake layer was homogeneous and distributed evenly on membrane surface. However, many studies have observed an opposite distributed cake layer on membrane surface (Cho and Fane, 2002; Gao et al., 2011). This situation would cause the calculated osmotic pressure to be overestimated to some extent in this study. Nevertheless, this result indicated osmotic pressure could not be ignored once a cake layer formed on membrane surface. The formed cake layer can be viewed as a porous media providing an additional barrier for filtration of the bulk suspension. According to Carman–Kozeny equation, which is the most famous permeability-porosity relation widely used in the field of flow in porous media, the cake layer in this study (610 lm thickness, 0.50 porosity, 6 lm deposited particle size) will induce an operation pressure less than 0.5 ka, which is only about one percent of the final TMP (54 kpa) obtained in the experiments. Current known membrane fouling mechanisms, including pore plugging/clogging by colloidal particles, adsorption of soluble compounds and biofouling, deposition of solids as a cake layer, cake layer consolidation and the spatial and temporal changes of the foulant composition, could not satisfactorily explain the big gap between calculation result and experimental data. This study reveals a new membrane fouling mechanism, osmotic pressure of cake layer filtration. Calculation shows that osmotic pressure of cake layer filtration accounts for the largest fraction of operational TMP, thus offering a more reasonable explanation for the membrane fouling phenomenon in MBRs. Such a comparison verified the proposed model’s feasibility to some extent. Conductivity analysis showed that conductivity of influent was continuously 4–15% higher than that of effluent (24 measurements during 8 days). Considering the low anaerobic sludge yield, this result indicated that certain amount of ions was adsorbed or intercepted in the matrix of cake layer as well as sludge flocs. As argued above, osmotic pressure originated from the interception of ions in the matrix of cake layer. Conductivity data provided direct evidences verifying the existence of osmotic pressure of cake layer filtration, although further studies are needed in order to better understand osmotic pressure and develop effective control strategies.
4. Conclusions SAnMBR could effectively remove approximately 90% of COD, 99% of TSS and turbidity in the sewage during the stable operation period. The cake layer formed on membrane surface was hydrated, rich of EPS and negative charged. It was found that osmotic pressure existed during cake layer filtration process due to the interception of ions. An osmotic pressure model was then developed, and the calculation results indicated that osmotic pressure was
J. Chen et al. / Bioresource Technology 125 (2012) 97–101
one of the major mechanisms responsible for membrane fouling problem in MBRs. This study gave a new insight into membrane fouling in MBRs. Acknowledgements Financial support of National Natural Science Foundation of China (No. 51108424, 21107099, 21275130), Qianjiang Talent Project of Zhejiang Province (No. 2012R10061) and Department of Education of Zhejiang Province (No. Y201121142) is highly appreciated. References APHA, 2005. Standard Methods for the Examination of Water and Wastewater, twentieth ed. American Public Health Association, American Water Works Association, Water Environmental Federation, Washington, USA. Boyette, S.M., Lovett, J.M., Gaboda, W.G., Soares, J.A., 2001. Cell surface and exopolymer characterization of laboratory stabilized activated sludge from a beverage bottling plant. Water Sci. Technol. 43 (6), 174–184. Cho, B.D., Fane, A.G., 2002. Fouling transients in nominally sub-critical flux operation of a membrane bioreactor. J. Membr. Sci. 209 (2), 391–403. Dignac, M.F., Urbain, V., Rybacki, D., Bruchet, A., Snidaro, D., Scribe, P., 1998. Chemical description of extracellular polymers: Implication on activated sludge floc structure. Water Sci. Technol. 38 (8–9), 45–53. Drews, A., 2010. Membrane fouling in membrane bioreactors - characterisation, contradictions, cause and cures. J. Membr. Sci. 363 (1–2), 1–28. Gao, W.J., Lin, H.J., Leung, K.T., Schraft, H., Liao, B.Q., 2011. Structure of cake layer in a submerged anaerobic membrane bioreactor. J. Membr. Sci. 374 (1–2), 110– 120. Hoek, E.M., Elimelech, M., 2003. Cake-enhanced concentration polarization: a new fouling mechanism for salt-rejecting membranes. Environ. Sci. Technol. 37 (24), 5581–5588.
101
Huang, X., Xiao, K., Shen, Y.X., 2010. Recent advances in membrane bioreactor technology for wastewater treatment in China. Front. Environ. Sci. Eng. China 4 (3), 245–271. Keiding, K., Wybrandt, L., Nielsen, P.H., 2001. Remember the water - a comment on EPS colligative properties. Water Sci. Technol. 43 (6), 17–23. Kola, A., Ye, Y., Ho, A., Le-Clech, P., Chen, V.K., 2012. Application of low frequency transverse vibration on fouling limitation in submerged hollow fibre membranes. J. Membr. Sci. 409, 54–65. Laspidou, C.S., Rittmann, B.E., 2002. A unified theory for extracellular polymeric substances, soluble microbial products, and active and inert biomass. Water Res. 36 (11), 2711–2720. Lin, H., Gao, W., Meng, F., Liao, B.-Q., Leung, K.-T., Zhao, L., Chen, J., Hong, H., 2012. Membrane bioreactors for industrial wastewater treatment: a critical review. Crit. Rev. Environ. Sci. Technol. 42 (7), 677–740. Lin, H.J., Xie, K., Mahendran, B., Bagley, D.M., Leung, K.T., Liss, S.N., Liao, B.Q., 2009. Sludge properties and their effects on membrane fouling in submerged anaerobic membrane bioreactors (SAnMBRs). Water Res. 43 (15), 3827–3837. Meng, F., Zhang, H., Li, Y., Zhang, X., Yang, F., 2005. Application of fractal permeation model to investigate membrane fouling in membrane bioreactor. J. Membr. Sci. 262 (1–2), 107–116. Morgan, J.W., Forster, C.F., Evison, L., 1990. A comparative study of the nature of biopolymers extracted from anaerobic and activated sludges. Water Res. 24 (6), 743–750. Pan, X., Liu, J., Zhang, D., 2010. Binding of phenanthrene to extracellular polymeric substances (EPS) from aerobic activated sludge: a fluorescence study. Colloids Surf. B 80 (1), 103–106. Robles, A., Ruano, M.V., García-Usach, F., Ferrer, J., 2012. Sub-critical filtration conditions of commercial hollow-fibre membranes in a submerged anaerobic MBR (HF-SAnMBR) system: the effect of gas sparging intensity. Bioresour. Technol. 114, 247–254. Spagni, A., Casu, S., Grilli, S., 2012. Decolourisation of textile wastewater in a submerged anaerobic membrane bioreactor. Bioresour. Technol. 117, 180–185. Zeldovich, K.B., Khokhlov, A.R., 1998. Osmotically active and passive counterions in inhomogeneous polymer gels. Macromolecules 32 (10), 3488–3494.