Journal of Industrial and Engineering Chemistry 80 (2019) 227–238
Contents lists available at ScienceDirect
Journal of Industrial and Engineering Chemistry
journal homepage: www.elsevier.com/locate/jiec
Graphene oxide-silver nanosheet-incorporated polyamide thin-film
composite membranes for antifouling and antibacterial action against
Escherichia coli and bovine serum albumin
Fekri Abdulraqeb Ahmed Alia , Javed Alamb,* , Arun Kumar Shuklab ,
Mansour Alhoshana,b,** , Jamal M. Khaledc , Waheed A. Al-Masrya ,
Naiyaf S. Alharbic , Manawwer Alamd
a
Chemical Engineering Department, College of Engineering, King Saud University, P.O. Box 2455, Riyadh 11451, Saudi Arabia
King Abdullah Institute for Nanotechnology, King Saud University, P.O. Box-2455, Riyadh 11451, Saudi Arabia
c
Botany and Microbiology Department, College of Science, King Saud University, P.O. Box 2455, Riyadh 11451, Saudi Arabia
d
Department of Chemistry, College of Science, King Saud University, P.O. Box 2455, Riyadh 11451, Saudi Arabia
b
A R T I C L E I N F O
A B S T R A C T
Article history:
Received 5 May 2019
Received in revised form 2 July 2019
Accepted 30 July 2019
Available online 7 August 2019
Biofouling leads to degradation of membrane performance characteristics, including permeability,
selectivity, and long-term stability. In this study, silver-doped graphene oxide (GO) was employed as a
nanoadditive to enhance the biofouling resistance of thin-film nanocomposite (TFN) membranes via
interfacial polymerization. Ag functionalization on GO sheets was carried out by a reduction reaction.
Electron microscopy, Raman spectroscopy, and X-ray diffraction analyses were conducted to evaluate Ag
attachment on GO. According to zeta potential and contact angle measurements as well as atomic force
microscopy results, GO-Ag-incorporated TFN membranes showed a high negative charge, hydrophilicity,
and a smooth surface. Bovine serum albumin protein and Escherichia coli (E. coli) were used as model
fouling agents to demonstrate the antifouling characteristics of the membranes. The TFN membrane
containing 80 ppm of GO-Ag had a high water flux recovery ratio (89%) and low irreversible resistance
(10%) after hydraulic washing. The biofouling resistance of the membranes was further studied by a
colony-counting method, while bacterial adhesion was analyzed by spinning disk confocal microscope
imaging. The TFN membrane prepared with 80 ppm GO-Ag reduced 86% of viable E. coli cells in bacterial
suspensions, with only slight bacterial adherence on the membrane surface.
© 2019 The Korean Society of Industrial and Engineering Chemistry. Published by Elsevier B.V. All rights
reserved.
Keywords:
Graphene oxide-silver
Polyamide thin-film composite
Antibacterial and antifouling
Introduction
Membrane fouling is defined as the deposition or adsorption of
unwanted material from a bulk water phase on membrane surfaces
and it impairs the overall membrane performance in terms of
permeability, selectivity, and long-term stability [1]. Depending on
the type of foulant, membrane fouling can be classified into four
categories, viz (i) inorganic (“scaling”) fouling, such as deposition
of inorganic salts and particulates of metal oxides on membrane
surfaces, (ii) organic fouling, such as accumulation of organic
matter (oil, grease, and lipids) and gel layer formation of
* Corresponding author.
** Corresponding author at: Chemical Engineering Department, College of
Engineering, King Saud University, P.O. Box 2455, Riyadh 11451, Saudi Arabia.
E-mail addresses: javaalam@ksu.edu.sa (J. Alam), mhoshan@ksu.edu.sa
(M. Alhoshan).
macromolecular substances on membrane surfaces, (iii) colloidal
fouling, such as the deposition of silica, clay minerals, flocs, and
manganese oxides, and (iv) biofouling, such as the adhesion and
accumulation of microorganisms and their proliferation on
membrane surfaces [2,3]. Among the listed fouling types,
biofouling is considered a major issue in water treatment processes
as it can dramatically reduce treatment process efficiency and cost
effectiveness [4,5]. It is often considered the “Achilles heel” of
membrane-based water treatment because microorganisms can
multiply over time. Even if 99.9% of the prevalent microorganisms
are removed, the remaining cells continue to grow at the expense
of biodegradable substances present in the feed water [6]. Typical
adverse effects of membrane biofouling include (i) a decrease in
water flux due to biofilm formation on the membrane surface, (ii)
an increase in concentration polarization at the surface leads to a
reduction in solute rejection, (ii) an increase in pressure drop (DP),
(iv) biodegradation and biodeterioration of the membrane
https://doi.org/10.1016/j.jiec.2019.07.052
1226-086X/© 2019 The Korean Society of Industrial and Engineering Chemistry. Published by Elsevier B.V. All rights reserved.
228
F.A. Ahmed Ali et al. / Journal of Industrial and Engineering Chemistry 80 (2019) 227–238
material, (v) the biofilm provides suitable conditions for the
proliferation of primary or secondary human pathogens on
membrane surfaces, and (vi) increased energy requirements to
overcome biofilm hydraulic resistance and flux decline [2].
Many approaches have been employed to reduce membrane
biofouling, such as bulk modification (including polymer
blending and incorporating hydrophilic functional groups into
the backbone chains of polymers), surface modification, thinfilm deposition, and grafting [7–13]. Different surface modifiers,
such as functional groups [14], polymer brushes [15], modified
nanoparticles [16], and biocidal materials [17], have been used
to mitigate membrane biofouling. Using nanomaterials for
membrane surface modification has recently attracted great
attention because of their unique properties. Several nanomaterials have been incorporated on the surfaces of TFC
membranes to improve their permeability, hydrophilicity,
biofouling resistance, biocidal properties, and chlorine resistance [18]; examples of such nanomaterials are alumina [19],
zeolite [20], titanium dioxide [21], functionalized carbon
nanotubes [22,23], and graphene oxide (GO) [24,25]. Due to
their significant biocidal and hydrophilic properties, GO and
silver nanoparticles (Ag NPs) are considered to be good antibiofouling agents. GO nanosheets are individual two-dimensional carbon sheets containing oxygen-containing functional
groups (e.g., carboxyl, hydroxyl, carbonyl, and epoxy groups),
which impart a strong hydrophilicity [26–30]. Meanwhile, silver
is known to exhibit strong antibacterial and biocidal properties;
Ag NPs and hybrid Ag nanocomposites are being used to
inactivate many types of bacteria, viruses, and fungi. They
release Ag+ ions that destroy microorganism cell membranes
and DNA repetition ability [31].
In the current study, thin-film nanocomposite (TFN) membranes with enhanced biofouling resistance were prepared by
incorporating GO-Ag nanosheets inside thin PA layers. Upon the
addition of GO-Ag nanosheets to PA layers, TFN membrane
properties, such as charge, hydrophilicity, and smoothness were
improved, thus enhancing their antimicrobial properties. GO
nanosheets were functionalized with Ag nanoparticles via a
reduction reaction using sodium borohydride (NaBH4). GO-Agincorporated TFN membranes were fabricated via interfacial
polymerization by distributing GO-Ag nanosheets in an aqueous
m-phenylenediamine (MPD) solution, where they react with
trimesoyl chloride (TMC) to form thin PA layers on porous
polysulfone (PSF) layers. Antifouling properties of the fabricated
TFN membranes were evaluated by studying the adhesion of
bovine serum albumin (BSA) protein and their antimicrobial
properties were characterized using a colony-counting method. A
spinning disk confocal microscope imaging technique was used to
evaluate the inhabitation and adhesion of E. coli bacteria on TFN
membrane surfaces.
Experimental
Materials
Polysulfone was supplied by BASF (Germany). Polyethylene
glycol (PEG 600) was purchased from Merck (Germany) and TMC
(98% purity) monomer was purchased from Merck (USA). MPD
(purity 99%) monomer, GO, BSA, and sodium dodecyl sulfate (SDS)
were purchased from Sigma Aldrich (USA). Sliver nitrate (AgNO3,
ACS, crystal) was purchased from D. F. Goldsmith Chemical &
Metal Corp. (USA). N-Methyl-pyrrolidone (NMP), trimethylamine
(TEA, purity 99%), hexane (C6H14, purity 99%), and different salts
(NaCl, MgCl2, Na2SO4, and MgSO4) were obtained from Oxford Lab
Chem (India). Deionized water (Milli-Q) with a resistivity of
18.2 MV cm was used in all the experiments (Millipore, USA).
Synthesis of GO-Ag nanosheets
GO nanosheet surfaces were functionalized with Ag via AgNO3
reduction according to the following procedure. (i) Approximately
50 mg of GO nanosheets were sonicated in 20 mL of Milli-Q water for
30 min to obtain a stable dispersion. (ii) To this mixture, 18 mL of a
1 mM AgNO3 solution was added to the GO dispersion and sonicated
for an additional 15 min. The reaction mixture was stirred for 20 min at
room temperature earlier the adding of the reducing agent. (iii) 10 mL
of a freshly prepared solution of NaBH4 (1 mM) was gradually added, at
a rate of 1drop/sec, to the mixture while stirring. Steps (ii) and (iii) were
repeated ten times to achieve the silver nanoparticles seeded on the
graphene nanosheets, and therefore, uniformly distribute of the silver
nanoparticles was achieved. After stirring the reaction mixture for 12 h
at room temperature, a green GO-Ag precipitate was obtained. It was
washed 5 times with Milli-Q water, collected after centrifugation at
6000 rpm for 30 min, and dried in an oven at 60 C [32]. A preparation
scheme for GO-Ag nanosheets are shown in Fig.1.
Characterization of GO-Ag nanosheets
The morphologies of GO and GO-Ag nanosheets were studied by
transmission electron microscopy (TEM, JEOL, Japan). Their surface
chemical composition was analyzed using a scanning electron
microscope equipped with an energy-dispersive X-ray spectrometer (SEM-EDX, JEOL, Japan). Raman spectroscopy (NRS-4500,
JASCO, Spain) was conducted to characterize GO nanosheet
functionalization with Ag nanoparticles. The crystalline structures
of GO and GO-Ag nanosheets were characterized by X-ray
diffraction (XRD, Ultima IV, Rigaku, Japan).
Preparation of PSF supports
PSF support membranes were fabricated according to a phase
inversion method. Initially, 17 wt.% of dried PSF and 15 wt.% of PEG
were dissolved in NMP while stirring at 70 C. After complete
dissolution, the polymer solution was cast on a glass plate using a
knife film applicator (DeltaE Srl, Italy) to obtain 90 mm-thick films.
Immediately after casting, the films were immersed in a coagulation
bath at 25 C, where they were held for 24 h to complete the phase
inversion process. Subsequently, the support membrane was
removed from the water bath, cut, and stored until further use.
Fabrication of TFN membranes
TFN membranes were synthesized on PSF supports by interfacial
polymerization. Firstly, a diamine monomer aqueous solution was
prepared by dissolving 1 wt.% MPD, 0.2 wt.% SDS, and 1 wt.% TEA in
Milli-Q water. Later, a MPD/GO-Ag aqueous solution was prepared by
dispersing GO-Ag at different concentrations (20, 40, 60, and 80 ppm)
in MPD (aq.) using an ultrasound sonicator (digital sonifier, Branson
Ultrasonics Corporation, USA) for 30 min. PSF support layers were
submerged in Milli-Q water for 24 h after which they were taken out
and fixed on a plastic plate with a rubber gasket and plastic frame at the
top. Aqueous MPD solutions were poured onto PSF supports and
allowed to penetrate for 10 min. Later, the aqueous solution was
drained off and the solution remaining on surface was removed using a
rubber roller to prevent any droplet formation on the surface.
Interfacial polymerization occurred when 0.1 wt.% of TMC in n-hexane
was poured on the impregnated PSF support, where it reacted with
MPD monomers to form a polyamide thin layer. After 60 s of reaction,
the TMC solutionwas drained off. The fabricated TFN membranes were
rinsed with hexane to any remove unreacted solution and cured in an
air oven at 80 C for 5 min. Finally, the prepared membranes were
stored in a refrigerator at 5 C until further use. A fabrication scheme
for TFN membrane is shown in Fig.1.
F.A. Ahmed Ali et al. / Journal of Industrial and Engineering Chemistry 80 (2019) 227–238
229
Fig. 1. a Schematic illustration of synthesis GO-Ag nanosheets and TFN membrane fabrication. b Schematic illustration of interactions of GO-Ag with TMC and MPD.
Fig. 2. TEM images of (a) GO and (b) GO-Ag nanoparticles.
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F.A. Ahmed Ali et al. / Journal of Industrial and Engineering Chemistry 80 (2019) 227–238
Characterization of TFN membrane
A field-emission scanning electron microscope (FE-SEM, JEOL,
Japan) was used to study the surface morphology of PA TFN
membranes, while their surface chemical composition was analyzed
by SEM-EDX. The surface roughness and relative surface area of PA
TFN membranes were examined using an atomic force microscope
(AFM, Veeco NanoScope V Multi Mode software). The thermal
stability of TFN membranes before and after adding GO-Ag nanosheets was evaluated by thermogravimetric analysis (TGA, Mettler
Toledo, Austria). In this experiment, thin PA layers were isolated from
the TFN structure and a dried sample of the PA TFN membrane was
incubated in dichloromethane to dissolve the PSF support layer; the
PA layer obtained was washed with water and methanol, dried, and
used for TGA. The impact of GO-Ag on the surface charge of the
membrane was studied by zeta potential measurement using a
SurPASS electro-kinetic analyzer (Anton-Paar KG, Graz, Austria). The
hydrophilicity of TFN membranes was analyzed by measuring the
contact angle between water droplets and the membrane surface
using a tensiometer (Atension, MAC 200, The Netherlands).
conditions. Fresh membranes were compacted at 8 bar using MilliQ water until their flux reached a steady state. Water flux through
TFN membranes was evaluated at different TMPs (DP) and
calculated using Eq. (1):
Jw ¼
Q
ADt
ð1Þ
where, Jw is the permeate flux (L m2 h1), Q is the volume of water
permeated (L), A is the effective membrane area (m2), and Dt is the
permeation time (h).
Salt rejection from PA TFN membranes was measured using a
single-solute solution containing NaCl (2000 ppm) and Na2SO4
(1000 ppm). Salt rejection was evaluated at 8 bar at a flow rate of
1.3 L/min (LPM) at room temperature. Salt concentration in the
permeate was determined by measuring the electrical conductivity of salt ions in the permeate with a conductivity meter
(DeltaOhm HD 2156.1). Subsequently, the salt rejection percentage
(R%) was calculated using Eq. (2):
R % ¼1
sP
100
sF
ð2Þ
TFN membrane performance analysis
where s F and s P represent ion conductivity in the feed and
permeate, respectively.
A cross-flow cell was employed to measure permeate flux and
salt rejection. The filtration system (Sterlitech Corporation, USA)
contained six cells, each with an effective area of 42 cm2. This
allowed to evaluate more than membrane together under the same
Antifouling study
Antifouling tests were conducted on TFN membranes using BSA
protein as a model fouling agent. Initially, the flux of pure water
(J W0 Þ through TFN membranes was measured at 4 bar for 10 h after
which pure water was discharged and the solution reservoir was
filled with 1 g/L BSA protein in a buffer solution; the solution pH
was 7. Later, protein permeate flux (JPP Þ was calculated by collecting
permeate after every 4 h for 72 h. The permeate was returned to the
feed tank to maintain a constant feed concentration. After filtration of
the BSA protein solution was completed, fouled membranes were
washed with Milli-Q water and their pure water flux (JWf Þ was
measured again for 8 h. Finally, antifouling characteristics of the
membranes, including flux recovery ratio (FRR), total fouling ratio
(Rt ), reversible flux decline ratio (Rr ), and irreversible flux decline
ratio (Rir ), were calculated using the following equations.
FRR ð% Þ ¼ J Wf =J W0 100
ð3Þ
Rt ð% Þ ¼ ðJW0 JPP Þ=JW0 100
ð4Þ
Rr ð% Þ ¼ ðJWf JPP Þ=J W0 100
ð5Þ
Rir ð% Þ ¼ ðJW0 JWf Þ=JW0 100
ð6Þ
Evaluation of the antibacterial and antiadhesion properties of TFN
membranes
Fig. 3. Spectral characterization of GO and GO-Ag nanosheets: (a) Raman spectra
and (b) XRD spectra.
To evaluate the bacterial inhibition ability of the developed TFN
membranes, Escherichia coli ATCC 25922 was grown on sterile 24well flat-bottom plates (Corning incorporated, USA); TFN membranes (1 cm2 pieces) were then incubated on these plates. A
bacterial suspension was prepared from a pure single colony of E. coli
ATCC 25922 cultivated on nutrient agar (Scharlau, Spain) and then
subjected to serial dilution using sterile normal saline (0.89% NaCl)
to obtain a concentration of 2.6 102 cells/mL. Both the active and
non-active sides of TFN membrane pieces were sterilized under a
UV-C germicidal lamp in a laminar flow biological cabinet (LabTech,
F.A. Ahmed Ali et al. / Journal of Industrial and Engineering Chemistry 80 (2019) 227–238
231
Fig. 4. FE-SEM images with simulated MountainsMap1 software of the thin PA layer of (a) pristine TFC, (b) TFN 20 ppm, (c) TFN 40 ppm, (d) TFN 60 ppm, and (e) TFN 80 ppm
of GO-Ag nanosheets.
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F.A. Ahmed Ali et al. / Journal of Industrial and Engineering Chemistry 80 (2019) 227–238
Fig. 5. AFM 3D images of membranes (a) pristine TFC, (b) TFN 20 ppm, (c) TFN 40 ppm, (d) TFN 60 ppm, and (e) TFN 80 ppm of GO-Ag nanosheets.
Daihah, Korea). In each well of the sterile 24-well flat-bottom plate,
1 mL of the bacterial suspension was placed; later, sterile TFN
membrane pieces were submerged in these wells (one piece per
well). The plate was then incubated at 25 C for an hour at 200 rpm.
Three replicate experiments were conducted. Two control groups –
the first without membranes and the second with sterile pieces of
cover slip glasses (1 cm2) – were used for comparison.
After incubation, the tested membranes were removed from
wells after which the number of bacteria in the wells was evaluated
using a standard pour plate method. Serial dilutions were prepared
after which 1 mL of each dilution was added to sterile Petri dishes
containing 15 mL of the nutrient medium. The plates were
incubated at 35 C for 24 h following which the number of total
viable bacteria cells was counted as colony forming units (CFUs)
per mL [33]. The experiment was performed under controlled
conditions to prevent microbial contamination. The effectiveness
of TFN membranes in reducing the number of viable bacteria cells
in the suspensions was calculated as follows:
Bm
ð7Þ
100
Bv ð% Þ ¼
Bc
where Bv is the percentage of viable bacteria (%), Bm represents the
number of viable bacterial cells in the treated group, and Bc is the
number of viable bacteria cells in the control group. The total
number of viable bacterial cells was calculated and statistical
analysis was conducted on the obtained data using the Tukey post
hoc test with one-way ANOVA (IBM, SPSS statistics 25). To evaluate
the bio-adhesion of bacterial cells on TFN membranes, the surfaces of
membranes removed from wells containing bacterial suspensions
were washed immediately using sterile normal saline to remove
unattached bacterial cells and then treated with CYTO 9 (3.34 mM)
and propidium iodide (20 mM) (ThermoFisher scientific, USA) at
25 C for 15 min in the absence of light [34]. Later, the membranes
were washed thrice with sterile normal saline and analyzed using a
spinning disk confocal microscope (Zeiss, Germany); the obtained
microscopic images were analyzed using ImageJ software.
Results and discussion
Characterization of GO-Ag nanosheets
Morphological analysis of GO-Ag nanosheets
Ag attachment on the surfaces of GO sheets was evaluated by
TEM (Fig. 2b). It can be clearly seen that the GO sheets were highly
decorated with uniformly dispersed spherical Ag particles, which
demonstrates good interactions between Ag and GO. The attached
Ag particles were observed to be in the range of (9.4 2.8) nm. The
strong attachment of Ag to the surfaces of GO sheets may be
F.A. Ahmed Ali et al. / Journal of Industrial and Engineering Chemistry 80 (2019) 227–238
Fig. 6. TFN membranes (a) Zeta potential, and (b) contact angle results.
attributed to interactions between Ag+ ions and the oxygencontaining functional groups on GO sheets, which provide
nucleation sites for the growth of Ag.
Spectral analysis
The chemical structure of Ag-functionalized GO nanosheets was
evaluated by Raman spectroscopy. The attachment of Ag particles on
GO nanosheet surfaces was investigated by monitoring the intensity
ratio of two characteristic peaks at 1345 cm1 and 1580 cm-1, which
correspond to the G band due to the first-order scattering of the E2g
phonons by sp2 carbon atoms and the D bands suggested to
disordered of carbon sp3 atoms and the breathing mode of k-point
photons of A1g symmetry, respectively, as reported by Zhou et al. [35].
Fig. 3a shows the Raman spectra of GO and GO-Ag; after GO-Ag
nanocomposite formation, the intensity ratio between D band and G
band (ID/IG) increases dramatically from 0.114 in GO to 0.138 in GO-Ag
due to the decrease of the average size of sp2 domains by reduction of
GO. This can be described by removing some oxygen functional
groups during the reduction process of silver on graphene, leading to
form complex fragmentation along with the reactive sites of
graphene [32,36]. This confirms the successful decoration of Ag
nanoparticles on GO nanosheets.
Fig. 3b shows the XRD patterns of GO nanosheets and GO-Ag
nanocomposites. The XRD pattern of GO nanosheets displays a
distinct peak at 2u~16.2 , which may be attributed to interlamellar
water trapped between hydrophilic GO nanosheets. A similar
result was reported by Nanda et al. [37]. With respect to the XRD
pattern of GO-Ag, the distinct peaks at 2u = 38.34 , 44.31, 64.58 ,
233
Fig. 7. (a) FT-IR spectrum and (b) TGA analysis of TFN membranes.
and 77.82 are assigned to the (111), (200), (220), and (311)
crystalline planes, respectively, of face-centered cubic (fcc) Ag NPs.
Similar results were reported by other researchers [38,39]. These
XRD results confirm that Ag NPs were successfully loaded onto GO
nanosheets.
Characterization of TFN membranes
Morphological analysis
FE-SEM images of both TFC and TFN membrane surfaces
displayed ridge-valley structures as illustrated in Fig. 4; similar
results can be found in previous reports as well [40,41]. Fig. 3
shows that the surfaces of TFN membranes appear denser relative
to the nodular surfaces of TFC membranes (Fig. 4a); further, a leaflike surface was observed on the TFN membrane (Fig. 4b–d). The
nodular surface structure of TFC membranes resulted in a fast rate
of polymerization between MPD and TMC [42]. The incorporated
GO-Ag nanosheets reacted with MPD and TMC during the
polymerization reaction and the possible reaction mechanism
was displayed in Fig. 1b. While their oxygen-containing functional
groups reacted only with MPD. The acyl chloride groups of TMC
interacted with the hydroxyl and carboxyl groups of GO-Ag
nanosheets. Hence, the polymerization reaction between MPD and
TMC was significantly influenced by the incorporation GO-Ag,
which led to the formation of dense thin PA layers with partially
content of more leaf-like surface on the top of thin PA layer [43].
As shown in Fig. 5, the surface roughness of TFN membranes
decreased after the incorporation of GO-Ag into the thin PA layers
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F.A. Ahmed Ali et al. / Journal of Industrial and Engineering Chemistry 80 (2019) 227–238
Fig. 8. Flux and salts rejection of TFC and TFN membranes.
as compared to pristine TFC membranes. The average roughness of
all the membranes decreases in the following order: pristine TFC
(65.4 nm) > TFN 20 ppm (59.5 nm) > TFN 40 ppm (54.3 nm) > TFN
60 ppm (48.8 nm) > TFN 80 ppm (42.0 nm), respectively. The
decrease in surface roughness can be explained as follows. GO-Ag
nanosheets enhanced the growth of leaf-like structures on the
surfaces of thin PA layers during the IP process. These results agree
with the FE-SEM images (Fig. 4), wherein it could be observed that
GO-Ag nanosheets hindered the formation of nodular structures. A
similar observation was reported on the effect of GO-Ag nanosheets on the surface roughness of TFN membranes [44,45].
Zeta potential and contact angle
Fig. 6a illustrates changes occurring in the surface charge of the
fabricated membranes at different pH. The obtained results show
that the surface charge of TFN membranes increased towards
positive values with an increase in the amount of GO-Ag
incorporated in the thin PA layers; at pH 7, surface charge of the
pristine membrane was 16 mV, while the TFN membrane with
80 ppm GO-Ag exhibited a surface charge of 28 mV. This
observation can be attributed to the incorporation of negatively
charged Ag-GO into the thin PA layer [46]. Hydrophilicity of the
fabricated TFN membranes was evaluated by measuring changes in
their contact angles. The results in Fig. 6b show that TFN containing
80 ppm of GO-Ag exhibited the lowest contact angle (35 ) among
all the tested membranes. Meanwhile, the pristine TFC membrane
exhibited a contact angle of 57, indicating that the incorporation
of GO-Ag nanosheets leads to improved hydrophilicity of the thin
PA layer. This difference may be attributed to the presence of
various hydrophilic functional groups in GO-Ag nanosheets [47],
which was also confirmed by FTIR (Fig. 7a).
Spectral analysis
As shown in Fig. 7a, amide groups synthesized via interfacial
polymerization are characterized by distinct peaks in FT-IR spectra
at around 1682, 1584, and 1084 cm–1, which are ascribed to C¼O
stretching (carboxylic), C
N stretching (amide), and N
H
bending vibrations, respectively [48,49]. Incorporation of GO-Ag
into thin PA layers resulted in an enhancement in the peak
intensity at 1682 cm–1, which may be due to the formation of new
amide linkages by the reaction between –NH2 groups in MPD and
COOH groups in GO-Ag [50]. Further, the intensity of peaks at
1088, 1769, and 2974 cm–1 gradually increased with an increase in
the amount of incorporated GO-Ag; the stated peaks correspond to
epoxide, carboxylic, and hydroxyl functional groups, respectively,
and confirm the incorporation GO-Ag in thin PA layers by
Fig. 9. TFN membranes (a) flux change as a function of different time intervals, and
(b) fouling behavior comparison of FRR, Rr, and Rir.
interfacial polymerization. The distinct peak at 1769 cm–1 in the
FT-IR spectrum of TFN membranes corresponds to the stretching
vibrations of C¼O (ester) groups, which were formed by a reaction
between the carboxylic or hydroxyl groups of GO-Ag and
carboxylic groups of the thin PA layers [51].
TGA study
Fig. 7b showed thermograms corresponding to TFC and TFN
membranes with different GO-Ag concentrations. All the membranes exhibited high thermal stability and weight loss at
temperatures greater than 400 C due to the decomposition of
thin PA layers. These thermograms also indicated that a complete
polymerization reaction occurred, i.e., there were no residual
unreacted functional groups, such as amine and acid groups [52].
The TGA curves indicate that GO-Ag addition enhanced the
thermal stability of PA membranes and increased their decomposition temperature from 443 to 475 C when the GO-Ag
concentration was increased from 0 to 80 ppm.
TFN membrane performance
The transport properties of TFN membranes were evaluated to
understand the impact of GO-Ag incorporated in thin PA layers on
membrane water flux and salt rejection. As summarized in Fig. 8,
these parameters were not significantly affected by incorporating
GO-Ag nanosheets. Water flux and NaCl rejection of TFN
membranes decreased slightly from 11.8 LMH to 10.8 LMH and
96.7% to 94.8%, respectively, with an increase in GO-Ag
F.A. Ahmed Ali et al. / Journal of Industrial and Engineering Chemistry 80 (2019) 227–238
concentration from 0 to 80 ppm. Meanwhile, there was no clear
difference in Na2SO4 rejection between TFC and TFN membranes.
Increasing GO-Ag concentration in the thin PA layer may lead to in
situ crosslinking and agglomeration in the PA film, which obstructs
water flux [52]. Moreover, the rate of polyester formation due to
the reaction of GO-Ag with MPD, as confirmed by FT-IR (see
Fig. 7a), increased with an increase in GO-Ag concentration and
possibly contributed to a reduction in water flux and salt rejection.
As reported by Seman et al. [53], the change in thin-film structure
from polyamide to polyester led to a decrease in water flux and salt
rejection. Overall, it seems that GO-Ag incorporated in thin PA
layers did not significantly affect the transport properties of TFN
membranes.
Antifouling analysis
BSA was selected as a model fouling agent to evaluate the
fouling resistance of the developed TFN membranes. Experiments
were conducted according to the method described in Section 2.8.
The fouling behavior of all TFN membranes was studied by
measuring permeate flux for 90 h and the fouling potential of TFC
and TFN membranes was evaluated by estimating their flux
recovery ratio, total fouling ratio, reversible flux decline ratio, and
irreversible flux decline ratio after flushing them with Milli-Q
water. As shown in Fig. 9a, the permeate flux of TFC and TFN
membranes decreased dramatically when Milli-Q water was
replaced with aqueous BSA; over time, the flux became stable.
Such flux decline can be attributed to the deposition of BSA protein
on membrane surfaces under operational conditions. Protein
deposition contributes to an increase in hydraulic transport
resistance, which in turn significantly decreases permeate flux
with time [54]. As shown in Fig. 9a, after flushing with Milli-Q
water, the reservoir was filled with fresh Milli-Q water in order to
measure the permeate flux of membranes and evaluate their
fouling potential. All the TFN membranes exhibited higher FRR and
Rir and a lower Rr than TFC membranes as shown in Fig. 9b. Higher
FFR values indicate that TFN membranes could be easily cleaned by
simple hydraulic flushing, while lower Rir values indicate that
lesser quantities of BSA were adsorbed on the surfaces of these
membranes. The high Rir values of TFC membranes are ascribed to
hydrophobic and electrostatic interactions between BSA and the
membrane surface, which led to the accumulation of BSA on the
membrane surface and a small permeate flux [55]. The incorporation of GO-Ag nanosheets in the thin PA layers of TFN membranes
improved their hydrophilicity and decreased fouling, which occurs
by the adsorption of hydrophobic BSA protein on membrane
surface. As confirmed by contact angle results (see Fig. 6b), TFN
membranes were more hydrophilic than TFC membranes due to
the presence of different oxygen-containing groups in the GO-Ag
nanosheets [56]. Further, the negative charge of GO-Ag nanosheets
increased the fouling resistance of TFN membranes against the
adsorption of negatively charged BSA by electrostatic repulsion. In
addition, membranes with rough surfaces provide the right places
for foulant attachment in their ridges and valleys. The incorporation of GO-Ag nanosheets in thin PA layers led to a decrease in the
surface roughness of TFN membranes as shown in Fig. 5. The
reduced surface roughness TFN membranes also contributed to a
decrease in BSA fouling on the membrane surface [57]. It is clear
from Fig. 9b that in TFN membranes, FFR increased from 36.36% to
89.27% and Rir decreased from 62.62% to 10.72% with an increase in
GO-Ag nanosheet concentration from 0 to 80 ppm; the membrane
containing 80 ppm of GO-Ag nanosheets exhibited the best fouling
resistance. This is owing to the high hydrophilicity, negative
charge, and smooth surface of the thin PA films, which leads to a
decrease in the amount of BSA adsorbed on the membrane surface
[26]. The results obtained showed that TFN membranes are more
235
resistant to fouling when compared to TFC membranes. Further,
this fouling resistance increased significantly in TFN membranes
with an increase in the GO-Ag nanosheet concentration.
Antimicrobial study
The antibacterial activity of modified TFN membranes was
evaluated by counting the number of CFUs on Petri dishes cultured
with bacteria after exposing them to membrane pieces for 1 h at
200 rpm. E. coli was chosen as the model microorganism owing to
the following reasons. (i) It is usually present in water environments and activated sludge and (ii) it is the best model
microorganism to study the formation and growth of biofilms
[58]. The data in Fig. 10a shows that the all the tested membranes
were capable of reducing the total number of viable bacterial cells
in bacterial suspensions within 1 h. However, TFN membranes
were more active against E. coli as compared to TFC membranes. In
other words, the number of viable cells remaining in a bacterial
suspension exposed to TFN membranes was significantly lower
than that observed in the case of TFC membranes. This result
indicates that GO-Ag nanosheets enhanced the antibacterial
properties of TFN membranes. In previous studies [59–62], it
was reported that Ag NPs could inhibit the growth of microbes
through several mechanisms. These are as follows. (i) Small Ag NPs
(1–10 nm) can penetrate bacterial cell membranes and damage
them, (ii) Ag NPs generate reactive oxygen species (ROS), which
damages the cell membrane, and (iii) Ag NPs release Ag+ ions,
which disrupt adenosine triphosphate (ATP) production and DNA
Fig. 10. Antimicrobial properties of membranes assessed by plate counting
technique.
236
F.A. Ahmed Ali et al. / Journal of Industrial and Engineering Chemistry 80 (2019) 227–238
Table 1
Comparison of other reported with GO-modified membranes.
Nanofillers
Con.
Addition method
Antimicrobial function
Ref.
GO
GO
pTA-f-GO
Ag
0.03 wt.%
160 ppm
76 ppm
AgNO3
4g L1
In MPD PI method
In TMC PI method
In MPD PI method
By situ reduction on commercial RO
Cells were viable 38%
Cells were viable 37% after 3 h
83.8% reduction of live E. coli after 24 h
62.7% reduction of live B. subtilis after 10 h
42.4% reduction live E. coli after 24 h
64.5% reduction of live E. coli cells after 1 h
[68]
[69]
[70]
[71]
85.6% reduction of live E. coli cells after 1 h
This work
GO
GO-Ag
80 ppm
Functionalization of GO by covalent
binding reaction on polyamide
In MPD PI method
[72]
Fig. 11. Confocal microscopy analysis of the E. coli bacterial morphology on the membrane surface. (For interpretation of the references to colour in this figure legend, the
reader is referred to the web version of this article.)
replication by interacting with the disulfide or thiol groups of
enzymes or DNA. All these mechanisms could lead to the
disruption and damage of bacterial cells and consequently, their
death. In another study, it was reported that direct contact with
graphene-based materials led to the irreversible damage and
destruction of bacterial cells [63]. Akhavan et al. suggested that cell
damage may be attributed to the interaction and penetration of
sharp edges of graphene oxide nanosheets into bacterial cells
F.A. Ahmed Ali et al. / Journal of Industrial and Engineering Chemistry 80 (2019) 227–238
leading to a loss of membrane integrity and cell death [64]. The
results shown in Fig. 10b confirm that an increase in the
concentration of GO-Ag nanosheets led to an increase in
the percentage of non-viable cells in bacterial suspensions. The
TFN membrane incorporated with 80 ppm of GO-Ag exhibited an
antibacterial efficiency of 85.6%. Statistical analysis confirmed that
when compared to pristine TFC membranes, the reduction
observed in viable bacterial cell population was significant
(P < 0.05) in the suspensions treated with TFN membranes
containing GO-Ag nanosheets. Our findings indicate that GO-Agincorporated TFN membranes strongly inhibited bacterial growth
on membrane surfaces. The incorporation of GO-Ag in the thin PA
layers of TFN membranes enhanced their physicochemical and
biological properties, thus contributing to the development of
antifouling and antimicrobial membranes. The antimicrobial
activity of the membranes developed in this work was compared
with that of other previously reported GO-modified membranes
(Table 1).
The anti-adhesive performance of the developed TFN membranes was evaluated by spinning disk confocal microscope
imaging of the bacteria remaining on membrane surfaces; prior
to this test, membranes were removed from wells containing
bacterial suspensions and washed to remove any unattached
bacteria. As depicted in Fig.11, a smaller number of E. coli units were
found to have adhered on TFN membranes as compared to pristine
TFC membranes. This can be attributed to electrostatic repulsion
between the anionic thin PA layers of TFN membranes (see Fig. 6a)
and negatively charged E. coli bacteria. Further, the high
hydrophilicity (see Fig. 6b) and low surface roughness (see
Fig. 5) of TFN membranes contributes to a decrease in the rate
of adhesion of E. coli on their surfaces. In general, bacteria readily
adhere to hydrophobic surfaces due to hydrophobic interactions
between the cell wall and surface [65]. In the case of a hydrophilic
surface, hydrogen bonding between the surface and water
molecules leads to the formation of a hydration layer, which
prevents E. coli from approaching and adhering on the surface
[66,67]. Epifluorescence microscopy images (Fig. 11) show dead
bacterial cells (red color) and viable bacterial cells (green color) on
the surfaces of TFC membrane and TFN membranes. The results
confirm that interactions between TFN membranes and E. coli lead
to a relatively higher antimicrobial activity when compared to TFC
membranes. The data show that GO-Ag nanomaterials reinforced
the antibacterial and anti-adhesive features of TFN membranes,
which suppressed the first stage of bacterial biofilm formation by
preventing bacterial attachment on the surface.
Conclusion
This work reports the use of silver-functionalized graphene
oxide (GO-Ag) nanosheets as additives for reducing biofouling in
polyamide TFC membranes. GO-Ag incorporation improved the
properties of TFN membranes in terms of their hydrophilicity,
surface charge, smoothness, and biocidal properties, thereby
leading to enhanced fouling and bacterial resistance against E.
coli and bovine serum albumin without adversely affecting
membrane selectivity. It was found that TFN membranes containing 80 ppm of GO-Ag exhibited a high antimicrobial activity of~86%;
further, these membranes led to a very low bacterial adhesion.
Moreover, most of the bacterial cells adhering on the membrane
surface were found to be non-viable, as observed by spinning disk
confocal microscopy. Additionally, GO-Ag-modified membranes
exhibited higher water flux recovery ratios and lower irreversible
fouling after hydraulic washing when compared to pristine TFC
membranes. Therefore, these membranes can potentially be
suggested for water separation and purification applications.
237
Acknowledgments
The authors extend their appreciation to the Deanship of
Scientific Research at King Saud University for funding this work
through research group no. RG-1439-85. The authors thank the
Deanship of Scientific Research and RSSU at King Saud University
for their technical support.
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