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Desalination 325 (2013) 3036

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Desalination
journal homepage: www.elsevier.com/locate/desal

Biofouling occurrence process and its control in the forward osmosis


Hongsik Yoon, Youngbin Baek, Jihyun Yu, Jeyong Yoon
World Class University (WCU) Program of Chemical Convergence for Energy & Environment (C2E2), School of Chemical and Biological Engineering, Seoul National University,
Institute of Chemical Processes (ICP), Daehak-dong, Gwanak-gu, Seoul 151-742, Republic of Korea

H I G H L I G H T S

Biofouling in FO process occurs less than RO process.


Physical cleaning is not effective for biofouling control.
However, chemical cleaning with chlorine is effective for biofouling control.

a r t i c l e i n f o a b s t r a c t

Article history: The forward osmosis (FO) process is a state-of-the-art desalination process associated with lower energy
Received 25 March 2013 consumption. The process uses natural osmotic pressure as the driving force. Biofouling represents the largest
Received in revised form 18 June 2013 contributor to various membrane fouling problems, and is difcult to control in the reverse osmosis (RO)
Accepted 20 June 2013
membrane process. However, knowledge of membrane biofouling occurrence in the FO process is limited,
Available online 13 July 2013
prompting urgent investigation. This study intended to investigate the biofouling characteristics of the FO
Keywords:
process in comparison with the RO process and its control as biofouling experiments with Pseudomonas
Forward osmosis aeruginosa PA01 GFP, which were conducted in lab-scale cross-ow systems. The biofouling occurrence was
Biofouling analyzed by the ux decline and surface bacterial concentration, while monitoring the biolm morphologies
Reverse osmosis using confocal laser scanning microscopy. In the results, the extent of biofouling occurrence was less severe
Physical cleaning in the FO process than in the RO process under the same permeate drag force. However, the ux recovery
Chemical cleaning was not effective with physical cleaning, in contrast to literature reports regarding the organic and inorganic
foulings in the FO process. In contrast, chemical cleaning with chlorine effectively controlled the biofouling.
2013 Elsevier B.V. All rights reserved.

1. Introduction However, the occurrence of membrane fouling is inevitable, and


diminishes the efciency of the FO process, since the foulants tend to
Water scarcity is one of the most serious challenges faced by the accumulate on the membrane during ltration. In general, the mem-
global society [1]. The reverse osmosis (RO) process is receiving brane fouling categories are organic, inorganic, colloidal, and biological
attention as a potential solution, despite the burden of its high energy fouling. Among these, biofouling accounts for about 40% of the mem-
requirements. However, since the energy efciency of current RO brane fouling in the RO process, which causes an irreversible decrease
technologies has approached the theoretical limit, the development in the permeate ux and salt rejection [12]. Biofouling is difcult to con-
of alternative desalination techniques has been intensively pursued trol due to the strong bacterial adhesion onto the surface and the sticky
to reduce energy consumption [2]. extracellular polymeric substance (EPS) matrix formation [13].
The forward osmosis (FO) process is known to have an advantage in According to previous studies on membrane fouling in the FO pro-
terms of energy consumption, because it uses natural osmotic pressure cess, intensied concentration polarization due to the fouling layer,
as the driving force resulting from an osmotic pressure gradient. The known as cake-enhanced osmotic pressure (CEOP), leads to a severe de-
FO process can be implemented in combination with the RO process cline in the permeate ux [1416]. In addition, the permeate drag force
[3], or combined with a membrane distillation process for separating [17] and the divalent ion in the feed play important roles of fouling in
clean water from the draw solution [4]. In addition, the FO process is the FO process as well as the RO process [18]. The fouling layer in the
applicable to treating wastewater [57], generating electricity [8,9], FO process was reported to be sparsely and thickly formed, in contrast
dewatering orange-peel press liquor [10], and producing fertilizer [11]. to that in the RO, and it can be easily removed by increasing the
cross-ow velocity (CFV) without any cleaning agents [14,19,20]. How-
ever, these studies were limited since they focused on only organic,
Corresponding author. Tel.: +82 2 880 8927; fax: +82 2 876 8911. inorganic, and colloidal foulings in the FO process, and not biofouling.
E-mail address: jeyong@snu.ac.kr (J. Yoon). Although several studies regarding the biofouling occurrence in the

0011-9164/$ see front matter 2013 Elsevier B.V. All rights reserved.
http://dx.doi.org/10.1016/j.desal.2013.06.018
H. Yoon et al. / Desalination 325 (2013) 3036 31

FO process were reported, no systematic study has been done yet on (Cole-Parmer, Vernon Hills, IL) were used to pump both the feed so-
this subject or on how to control the biofouling intensively. For exam- lution and the draw solution. The temperature was maintained at
ple, in the study where algae were employed as a model foulant in bio- 25 1 C by a thermostat (Lab. Companion, Korea). The weight
diesel production, the time scale (only a few hours) was too short for change of the draw solution reservoir was measured to calculate the
observing signicant biofouling [21]. Li et al. mainly studied inorganic water permeate ux. The volumes of the feed and draw solutions
fouling, such as silica scaling [15]. Also, in Zhang et al.'s study, inorganic were 6 L and 4 L, respectively. The FO membrane cell had an effective
fouling occurred with biofouling [22]. membrane area of 4.9 2.1 cm2, and two channels (height: 0.3 cm)
The objective of this study is to investigate the characteristics of for co-current ows of the feed solution and the draw solution.
the biofouling occurrence in the FO process in comparison with the These conditions were selected to minimize the ux decline due to
RO process, and to control it in the FO process using a commercial dilution of the draw solution. The permeate ux decline due to the
FO membrane in a lab-scale cross-ow system. In addition, the effec- occurrence of biofouling was expressed by a normalized factor after
tiveness of physical or chemical cleaning for controlling FO biofouling subtracting the ux decline due to simple dilution of the draw solu-
was investigated. tion (refer to Fig. S1(a)).
The lab-scale cross-ow RO membrane system employed in this
2. Materials & methods study was described in detail in our previous studies [23]. RO mem-
branes with an effective area of 6.8 3.3 cm2 were equipped in the
2.1. Materials membrane cells, and the channel height of a cell was 0.3 cm. The
concentrate and permeate were circulated to maintain the concentra-
A commercial FO membrane employed in the FO process made of tion of the feed solution. The applied pressure in the RO process was
cellulose triacetate (CTA) was purchased from Hydration Technology maintained at 9 1 bar. Other experimental conditions for the RO
Innovations (Scottsdale, AZ, USA). An LFC1 RO membrane was used process (temperature, initial permeate ux, cross-ow velocity, and
in the RO process (purchased from Hydranautics a Nitto Denko, time) were identical to those of the FO process.
Oceanside, CA). This membrane is a polyamide (PA) thin-lm com-
posite RO membrane employed for brackish desalination. Both FO 2.3. Biofouling experiment
and RO membranes were stored as at sheets in deionized (DI) water
at 4 C prior to use. The biofouling experiment in the FO process was performed by
For biofouling occurrence, Pseudomonas aeruginosa PA01 GFP, pro- measuring the permeate ux as an indication of the performance of
vided by Dr. M.J. Franklin (Montana State University, USA), was used the membrane. The protocol for the biofouling experiment in the FO
as a model bacterial strain. The method of bacterial culture was identical process is described as follows. Prior to all the biofouling experiments,
to that in our previous studies [2224]. The feed solution was composed the cross-ow system was cleaned by the sequential recirculation of
of 0.1% tryptic soy broth (TSB; Bacto, Franklin Lakes, NJ), 10 mM sodium 0.5% NaOCl for 30 min, 5 mM of ethylenediaminetetraacetic acid
chloride (Aldrich, St. Louis, MO), and 1 mM calcium chloride (Aldrich, (EDTA) for 30 min at pH 11, and 2 mM of sodium dodecylsulfate
St. Louis, MO) in DI water (Barnsted NANO Pure, USA). A sodium chlo- (SDS) (Aldrich, St. Louis, MO) for 30 min. The FO membrane was placed
ride solution was used as the draw solution. As a cleaning agent, in the membrane cell without spacers, and the cross-ow velocity was
100 mg/L of NaOCl (Aldrich, St. Louis, MO, USA) was used. maintained at 4 cm/s (Re = 234). This condition was selected to pro-
mote drastic ux decrease for a short period of time. 6 L of 10 mM
2.2. Lab-scale cross-ow system NaCl and 1 mM CaCl2 was used as the feed solution. 4 L of 4 M NaCl
was used as the draw solution. After the initial ux was stabilized, the
Biofouling experiments were carried out in a lab-scale cross-ow FO membrane was conditioned with organics (0.1% TSB) for 6 h. Note
FO process, as depicted in Fig. 1. Two variable-speed gear pumps that the ux decline caused by conditioning only was negligible (refer

Fig. 1. Schematic of the lab-scale cross-ow system for the forward osmosis (FO) process. (Effective membrane area: 4.9 2.1 cm2, channel height of both feed solution side and
draw solution side: 0.3 cm, feed solution: 6 L of tryptic soy broth 0.1%, 4 L of draw solution: 4 M NaCl).
32 H. Yoon et al. / Desalination 325 (2013) 3036

to Fig. S1(b) in the Supplementary material). Biofouling was induced on The RF was divided as,
the conditioned membrane for 48 h with P. aeruginosa PA01 GFP at
about 107 CFU/mL of the initial concentration in the feed solution. The RF Rcell REPS RCP : 3
bacterial concentration was maintained within an order of magnitude
during the biofouling test, possibly due to the oligotrophic condition Rcell resistance of bacterial cell (m1)
of the feed solution (not shown). REPS resistance of EPS (m1)
The protocol for the biofouling experiment in the RO process was RCP resistance via concentration polarization in the fouling
similar to that in our previous study [23]. The membrane was placed layer (m1)
in the membrane cell without spacers, and the cross-ow velocity
was maintained at 4 cm/s (Re = 245). After the membrane compac- The summation of Rcell and REPS in Eq. (3) becomes Rc (the resis-
tion by DI water at 15.5 bar for 18 h, the membrane was conditioned tance of cake layer, Eq. (4)) and RF becomes Eq. (5).
by organics (TSB 0.1%) for 6 h. To achieve a fair comparison of the
FO process with the RO process in the fouling experiments, the per- Rc Rcell REPS 4
meate drag force of both processes was controlled to be identical by
adjusting the initial permeate ux to be the same value. RF Rc Rcp : 5
Additionally, the biofouling occurrence in both the FO process
and the RO process was analyzed by measuring the biolm cell con-
centration and observing the morphology of P. aeruginosa PA01 GFP 2.5. Membrane cleaning
biolm on the membrane surface. The central part of the biofouled
membrane after biofouling occurrence, which is the same position Two different cleaning methods were employed to investigate
in every experiment, was carefully cut into two pieces. To detach their effectiveness for biofouling control in the FO process. First, the
the biolm cells from the membranes, one piece of biofouled mem- hydraulic stress was applied by increasing the cross-ow velocity
brane was soaked in 20 mL of DI water. Then, the biolm cell with DI water as a physical cleaning method. The CFV was maintained
was re-suspended by sonication and vortexing for 3 min each. The at 33 cm/s (Re = 1931) for 1 h. As the second method, chemical
biolm cell concentration in the suspended solution was measured cleaning with 100 mg/L of NaOCl at pH 7, which is known as an anti-
by the plate count method. The other piece of biofouled membrane microbial agent for biolm control [26], was employed in addition
was analyzed by confocal laser scanning microscopy (CLSM). Since to the physical cleaning in the rst method. After each cleaning, the
GFP-tagged bacteria were used in this study, the biolm cells could permeate ux was measured under the initial conditions in order to
be observed without dying. Biofouling experiments in both the FO examine whether the cleaning was effective for biofouling control.
process and the RO process were performed in triplicate to examine The membrane cleaning experiments were performed in triplicate
the reproducibility. to check the reproducibility. The biofouling layer was analyzed with
The effect of the initial bacterial concentration and the presence CLSM. The dead cells were stained with SYTO9 (BacLight Live/Dead
of organic matter on biofouling occurrence were investigated in the bacterial viability kit, Molecular Probes, USA).
FO process. The ux decline was measured at various initial bacterial
concentrations (105 and 107 CFU/mL each), with the other conditions 3. Results & discussion
the same as those mentioned previously. In addition, the effect of
the presence of organic matter on the biofouling was examined, 3.1. Effect of driving force
maintaining all the same conditions except for the draw solution con-
centration (5 M) and the presence of alginate (50 mg/L). Fig. 2 shows the normalized permeate ux decline of a biofouled
membrane in the FO process as compared with the RO process. The
2.4. Resistance-in-series model red arrow indicates the moment of the bacterial inoculation. As
shown in Fig. 2, the ux decline of the FO process resulting from
The fouling behavior is traditionally explained through resistance- the occurrence of biofouling appeared to be less severe than that of
in-series model [25]. the RO process. For example, the permeate ux in the FO process
In forward osmosis process decreased to 80 4% of the initial ux, while that in the RO process
decreased to 54 2%. This observation is consistent with the previ-
ous studies regarding fouling behavior in the FO process with that
J : 1
Rm RF in the RO process, although the previous studies did not deal with
biofouling [27,28].
In reverse osmosis process Since both processes (FO & RO) were operated under the same con-
ditions (i.e. initial permeate ux, CFV, temp., and time), the lower ux
decline in the FO process can be found in the driving forces of the
P FO process, which is osmotic-driven in contrast to the hydraulic-
J : 2
Rm RF pressure-driven RO process.
A separate experiment was performed in order to examine that
the difference of befouling behavior between the FO process and RO
J the permeate ux (L/m2 h) process (Fig. 2) is caused by the difference in the processes (FO and
the osmotic pressure (bar) RO), not by that in the membrane materials (CTA and PA), or that in
P the applied pressure (bar) the membrane structures (asymmetric and TFC) as an FO membrane
the viscosity (0.0089 g/cm s at 25 C) was employed in the RO process. The results are provided in Fig. S2
Rm resistance of the bare membrane (m1) (Supplementary information). As shown in Fig. S2, the biofouling
RF the resistance via membrane fouling (m1) occurrence in the FO process was less severe than the RO process on
the same membrane, indicating that the difference in the biofouling
Rm measured with DI water under 450 psi (31 bar) was 7.47 occurrence is caused by the difference in the processes, not by the
1014 m1 for CTA-FO membrane and 1.69 1014 m1 for LFC1 membrane materials (CTA and PA), or the membrane structures
membrane. (asymmetric and TFC).
H. Yoon et al. / Desalination 325 (2013) 3036 33

Fig. 2. Degree of biofouling expressed as the permeate ux decline in the forward


osmosis (FO) and the reverse osmosis process (RO) processes. A cellulose triacetate
FO membrane was used for the FO process. A polyamide RO membrane was used
for the RO process. The red arrow indicates the moment of bacterial inoculation in
the feed reservoir (Feed solution: 6 L of 10 mM NaCl, 1 mM CaCl2 and TSB 0.1%,
draw solution: 4 L of 4 M NaCl, applied pressure: 9 1 bar, initial ux of biofouling
test: 21 1 L/m2 h, 25 C, cross-ow velocity: 4 cm/s, and initial P. aeruginosa PA01
GFP concentration in feed: about 107 CFU/mL).

Additionally, the fouling behavior is traditionally explained through


resistance-in-series model. RF was about (1.81 0.47) 1014 m1 in
FO process (Fig. 2, CTA-FO membrane) and (4.29 0.85) 1014 m1
in RO process (Fig. S2, CTA-FO membrane). Since CEOP (cake-enhanced
osmotic pressure) was reportedly more intensied in the FO process
than the RO process, due to the reverse diffused salt from the draw
solution, it is plausible to interpret that RCP in the FO process can be
expected to be higher than the RCP in the RO process [14]. Then, as RF
in the FO process was lower than RF in the RO process, it can be
explained that Rc in the FO process is lower than Rc in the RO process,
possibly contributed by the absence of high hydraulic pressure.
As shown in Fig. 3 which shows the biolm morphologies of
the biofouled layers formed in the FO process and the RO process,
the biofouling layer appeared to be loosely formed in the FO process
(Fig. 3(a)), but was thicker than that in the RO process (Fig. 3(b)).
The biolm thickness, analyzed by CLSM, was about 60 5 m on
the FO membrane in the FO process and about 45 3 m on the
Fig. 3. CLSM images of P. aeruginosa PA01 GFP biolm morphology (a) on the biofouled
RO membrane in the RO process. As the FO membrane was employed forward osmosis (FO) membrane in the FO process and (b) on the biofouled RO mem-
in RO process in a separate experiment (refer to Fig. S3), the thickness brane in the RO process (green color: live cell, x axis: 202 m, y axis: 202 m, and z
of the biolm was similar to that in the RO membrane in the RO pro- axis: (a) 60 m, (b) 44 m).
cess as 40 4 m, indicating that the difference of thickness is from
the difference of process, not from difference of membrane materials.
This rst time observation of the biolm morphologies in the On the other hand, the concentration of bacteria on the surface
FO process in comparison with RO process provides the interpreta- of the biofouled membrane was measured as about (2.5 1.4)
tion that these differences (morphology & thickness) was caused by 108 CFU/cm2 in the FO process, and about (3.9 1.5) 108 CFU/cm2
the nature of the different driving forces between the FO process in the RO process. Transforming this number concentration into mass
(biofouled layer is not pressurized and inuenced only by natural os- concentration using the slope of 1 108 CFU/mg [31], the concentra-
motic pressure) and RO process (biofould layer is pressured by hydrau- tion of bacteria on the surface of the biofouled membrane can be
lic pressure). expressed as about 2.5 1.4 mg/cm2 in the FO process, and about
Additionally, to understand the role of EPS, the protein concentra- 3.9 1.5 mg/cm2 in the RO process which were about 100 times
tion on the biofouled membrane which is one of the representative higher than those of EPS. Then, Rcell in Rc (Eq. (4)) is expected to be
components of EPS (as measured by LowryFolin method) was mea- dominant factor rather than REPS (i.e., Rcell REPS).
sured as about 0.0211 0.006 mg/cm2 in FO process, and about
0.0238 0.004 mg/cm2 in RO process. This result indicates that the 3.2. Effect of feed condition
effect of EPS appears to be not critical on the fouling resistance since
this level of protein concentration is just 10% compared to the previ- Fig. 4 shows the effect of initial bacterial concentration (a) and the
ous research [29,30] which emphasized the role of EPS. This difference presence of organics (b) on the occurrence of biofouling, expressed as
may be due to the oligotrophic condition in this study resulting in low the ux decline. The red arrow indicates the moment of the bacterial
presence of EPS released from bacteria. inoculation. As shown in Fig. 4(a), the ux decline at two different
34 H. Yoon et al. / Desalination 325 (2013) 3036

Fig. 4. Effect of (a) initial bacterial concentration and (b) organic matter on biofouling Fig. 5. Effect of physical and chemical cleaning for biofouling control. The red arrow
occurrence expressed as permeate ux decline in the Forward osmosis (FO) process. As indicates the moment of bacterial inoculation in the feed. (a) Physical cleaning for
organic matter, sodium alginate 50 mg/L was used. The red arrow indicates the moment 1 h with hydraulic stress. (b) Chemical cleaning for 1 h with chlorine (biofouling
of bacterial inoculation in the feed reservoir (standard feed condition: 6 L of 10 mM experiment feed solution: 6 L of 10 mM NaCl, 1 mM CaCl2 and TSB 0.1%, draw
NaCl, 1 mM CaCl2, TSB 0.1%, draw solution: (a) 4 L of 4 M NaCl, (b) 4 L of 5 M NaCl, initial solution: 4 L of 4 M NaCl, initial ux: 22.5 1 L/m2 h, initial P. aeruginosa PA01 GFP
ux: (a) 22 1 L/m2 h, (b) 24 1 L/m2 h, initial P. aeruginosa PA01 GFP concentration: concentration in feed: about 107 CFU/mL, 25 C, cross-ow velocity: 4 cm/s; cleaning
(a) about 107 CFU/mL, 25 C, cross-ow velocity: 4 cm/s). experiment CFV: 33 cm/s, (a) feed reservoir: DI water, draw reservoir: 4 M NaCl,
(b) feed reservoir: chlorine 100 mg/L at pH 7, draw reservoir: 4 M NaCl).

bacterial concentrations (105 & 107 CFU/mL) was similar for 90 h


of biofouling experiments. For example, the permeate ux of 105 & cleaning only with hydraulic stress (b) chemical cleaning with hydrau-
107 CFU/mL with the initial bacterial concentration decreased to lic stress). For membrane cleaning with hydraulic stress, the cross-ow
69% and 67% of the initial ux, respectively, after 90 h. Note that the velocity was increased from 4 cm/s to 33 cm/s for 1 h. Note that ux
biolm cell concentration of both cases on the membrane was within decline as low as 86 2% of initial ux was observed for 54 h of bio-
an order of magnitude (not shown). fouling experiments. As shown in Fig. 5(a), physical cleaning was not
On the other hand, Fig. 4(b) shows that the presence of organic mat- effective to control the FO biofouling. For example, even though the
ter (alginate of 50 mg/L) in the feed water led to more severe decline in physical cleaning with hydraulic stress was performed, any signicant
the permeate ux. For example, the presence of organic matter (alginate ux recovery was not observed, showing a value of 85 4% of the ini-
of 50 mg/L) without bacteria led to substantial ux decline to 61% of the tial ux in Fig. 5(a). In addition, a large number of bacteria still remained
initial ux after 54 h, while the presence of bacteria (P. aeruginosa PA01 on the physically cleaned membrane ((7.1 6.9) 108 CFU/cm2),
GFP 107 CFU/mL) in addition to the same load of organic matter (alginate compared to the untreated membrane ((2.5 1.4) 108 CFU/cm2).
of 50 mg/L) led to further ux decline, but not signicantly. Note that the Moreover, even the osmotic back-ush with high CFV was not effective
permeate ux was reduced to 88% of the initial ux due to the membrane for recovering from the reduction in ux that occurred due to the
fouling with only bacteria (P. aeruginosa PA01 GFP 107 CFU/mL). biofouled membrane (refer to Fig. S4). Even though the biofouling
layer was loosely formed as shown in Fig. 3(a), the behavior of the
3.3. Membrane cleaning for controlling FO biofouling biofouling formation appears to have the nature of a mature biolm,
leading to resistance against physical stress.
Fig. 5 shows two cases of membrane cleaning approaches for Fig. 5(b) shows the ux change as the biofouled membrane was
biofouled FO membranes in terms of ux recovery ((a) physical treated by 100 mg/L of chlorine with hydraulic stress (33 cm/s of
H. Yoon et al. / Desalination 325 (2013) 3036 35

occurrence, as demonstrated by the permeate ux decline, was less se-


vere in the FO process than the RO process. However, physical cleaning
was not effective to recover the declined ux due to biofouling, in
contrast to the organic and inorganic foulings in the FO process. In con-
trast, chemical cleaning with chlorine was quite effective for biofouling
control.

Acknowledgment

This research was supported by the WCU (World Class University)


program through the National Research Foundation of Korea funded
by the Ministry of Education, Science and Technology (R31-10013)
and the National Research Foundation of Korea Grant funded by the
Korean Government (NRF-2010-C1AAA01-0029061).

Appendix A. Supplementary data

Supplementary data to this article can be found online at http://


dx.doi.org/10.1016/j.desal.2013.06.018.

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