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Sustainability Engineering and Green Chemistry
Photothermally-active Reduced Graphene Oxide/Bacterial Nanocellulose Composites as Biofouling-resistant Ultrafiltration Membranes Qisheng Jiang, Deoukchen Ghim, Sisi Cao, Sirimuvva Tadepalli, Keng-Ku Liu, Hyuna Kwon, Jingyi Luan, Yujia Min, Young-Shin Jun, and Srikanth Singamaneni Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.8b02772 • Publication Date (Web): 14 Sep 2018 Downloaded from http://pubs.acs.org on September 14, 2018
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Environmental Science & Technology
Photothermally-active Reduced Graphene Oxide/Bacterial Nanocellulose Composites as Biofouling-resistant Ultrafiltration Membranes Qisheng Jiang1,#, Deoukchen Ghim2,#, Sisi Cao1, Sirimuvva Tadepalli1, Keng-Ku Liu1, Hyuna Kwon2,3, Jingyi Luan1, Yujia Min2, Young-Shin Jun2* and Srikanth Singamaneni1*
1
Institute of Materials Science and Engineering and Department of Mechanical Engineering and
Materials Science, Washington University in St. Louis, St Louis, MO 63130 2
Department of Energy, Environmental and Chemical Engineering, Washington University, St.
Louis, MO 63130 3
Department of Energy and Resources Engineering, Seoul National University, Seoul, South
Korea
Address: One Brookings Drive, Campus Box 1099 (SS) and 1180 (YSJ) *E-mail:
[email protected] (SS) and
[email protected] (YSJ) Phone: (314) 935-5407 (SS) and (314)935-4539 (YSJ) #
Q. Jiang and D, Ghim contributed equally
Submitted: May 2018 Revised: September 2018
Environmental Science & Technology *To whom correspondence should be addressed
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ABSTRACT
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By severely decreasing water flux and driving up operational costs, biofouling poses one
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of the most serious challenges to membrane technologies. Here, we introduce a novel anti-
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biofouling ultrafiltration membrane based on reduced graphene oxide (RGO) and bacterial
5
nanocellulose (BNC), which incoporates GO flakes into BNC in situ during its growth. In
6
contrast to previously reported GO-based membranes for water treatment, the RGO/BNC
7
membrane exhibited excellent aqueous stability under environmentally relevant pH conditions,
8
vigorous mechanical agitation/sonication, and even high pressure. Importantly, due to its
9
excellent photothermal properties, under light illumination, the membrane exhibited effective
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bactericidal activity, obviating the need for any treatment of the feed water or external energy.
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The novel design and in situ incorporation of the membranes developed in this study present a
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proof-of-concept for realizing new highly efficient and environmental-friendly anti-biofouling
13
membranes for water purification.
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INTRODUCTION
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Water scarcity is recognized as one of the most critical global challenges in the 21st
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century.1-3 In response to this dire need, various membrane technologies are being actively
17
investigated for water purification and reclamation.4-6 However, fouling and consequent
18
degradation of membranes during performance still remain a ubiquitous problem.7 The three
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major fouling mechanisms, mineral scaling, organic fouling, and biofouling, all lead to a decline
20
in water flux.8 Among them, biofouling, which accounts for more than 45% of all membrane
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fouling, is the Achilles heel of the technologies, due to the difficulty of completely removing
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microorganisms.9-11
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To inhibit the formation of biofilm, various biofouling controlling strategies, such as
24
adjusting pH, adding disinfectants and biocides, and introducing quorum sensing molecules,
25
have been suggested.12-15 However, most of these strategies introduce considerable operational
26
costs and/or potential hazardous contaminants.12
27
incorporation of nanomaterials (e.g., silver nanoparticles, TiO2 nanoparticles, and graphene oxide
28
nanosheets), polymers (e.g., polyethylene glycol, polyvinyl alcohol, polyvinylpyrrolidone, and
29
zwitterionic
30
biomacromolecules) to engineer fouling-resistant membrane surfaces that can reduce biofilm
31
growth and inactivate bacteria.8, 16-21 However, most of these methods involve additional thermal
32
or chemical treatment steps. Furthermore, most techniques are effective for only a short period
33
of time, because biofilm gradually adapts to imposed harsh environments.9 Even if 99.9% of
34
biofilm is removed, the residual cells are sufficient to grow back and form a new biofilm. Highly
35
efficient and cost-effective methods that overcome biofouling on water purification membranes
polymers),
and
other
materials
Researchers have also investigated the
(e.g.,
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small
organic
molecules
and
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over a long period of time would immediately help meet the grand challenge of providing access
37
to clean water.
38
The photothermal effect of materials can offer a unique solution to biofouling, obviating
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the need for harsh chemical treatments to achieve bacterial lysis. Photothermally-active materials
40
can effectively absorb light and then convert it into heat. In our recent study, gold nanostars
41
grown on graphene oxide (GO) flakes coating a commercial membrane were utilized as
42
nanoheaters.21 In the study, with laser irradiation, the photothermal properties of the gold
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nanostars and GO were utilized to quickly kill adjacent Escherichia coli bacteria, inhibiting the
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formation of biofilm on reverse osmosis membranes. While this study provided a promising
45
example of utilizing the photothermal effect to minimize biofouling on membranes, it would be
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even more beneficial if the membrane itself were comprised of photothermal materials.
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GO has been recognized as efficient photothermal material because the closely spaced
48
energy level from loosely bonded π electrons absorb the broad electromagnetic spectrum.22-24
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The absorbed light energy excites electrons, and its electron relaxes to ground state through non-
50
radiative decay, releasing the energy by heat.22-24 In addition to having an intriguing
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photothermal property, GO has frequently been employed as a membrane component owing to
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its excellent mechanical strength, facile synthesis, and ease of attachment by vacuum filtration,
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spin-coating, and drop-casting.25-28 In contrast to graphene flakes, which have a strong tendency
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to stack and aggregate in aqueous solutions, GO flakes are easily dispersed, making the
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membrane preparation process easier in aqueous media.29, 30 This dispersibility comes from rich
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oxygen-containing functional groups (carboxyl, epoxy, hydroxyl, and carbonyl groups).31
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However, the stability of current GO-based membranes is compromised by vigorous agitation, 2 ACS Paragon Plus Environment
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and pH and ionic strength variations that are within the typical range of feed waters.32 Thus,
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there is a need to develop new scalable approaches to fabricate stable GO-based membranes.
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Bacterial nanocellulose (BNC) is a highly pure cellulose produced by bacteria with low-
61
molecular weight sugar as a food source. Through a series of biochemical steps, the bacteria
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form exterior cellulose nanofibers in aqueous cultures, and these fibers become entangled to
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form a 3D network hydrogel.33 Similar to other cellulose nanofibers and cellulose nanocrystals
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(CNC), BNC is highly attractive for membrane technologies in view of its excellent mechanical
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properties, tunable porosity, chemical functionalizability, easy synthesis, high scalability, and
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most important, low environmental impact.34 Therefore, BNC is a promising material for
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fabricating functional composites through in situ growth or by adsorption of pre-synthesized
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nanostructures on the nanoscale cellulose fibers.35-44
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Here, we demonstrate a novel and facile approach for fabricating an anti-biofouling
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ultrafiltration membrane, involving in situ incorporation of GO flakes into BNC during its
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growth. The reduced graphene oxide (RGO) incorporated BNC membrane not only exhibited
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outstanding mechanical and chemical stability under environmentally-relevant pH conditions and
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vigorous mechanical agitation/sonication, but also showed stable water flux under high pressure.
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Particularly, owing to its photothermal properties, the membrane exhibited light-enabled
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bactericidal activity, avoiding the need for any treatment of the feed water or any external
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energy. The novel design and preparation method introduced here are suggested the first steps
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toward realizing highly efficient, environmental-friendly, and biofouling-resistant membranes for
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water purification.
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EXPERIMENTAL SECTION
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Fabrication of RGO/BNC membranes. Gluconacetobacter hansenii (ATCC®53582) was
82
employed to synthesize the cellulose nanofibers. To produce a dense bacterial suspension, the
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bacteria were cultured in test tubes containing 16 ml of #1765 medium at 30 °C for 3 days under
84
shaking at 250 rpm. The #1765 growth medium is composed of 2% (w/v) glucose, 0.5% (w/v)
85
yeast extract, 0.5% (w/v) peptone, 0.27% (w/v) disodium phosphate, and 0.5% (w/v) citric acid.
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To synthesize GO, we employed an efficient oxidation process, reported by Tour and co-
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workers.45 For in situ incorporation of GO sheets in a BNC membrane, GO solution (150 mL of
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0.0725wt%) was sonicated (2 hours), centrifuged, re-dispersed in #1765 medium, and then
89
centrifuged again to concentrate a wet mixture of GO and medium after supernatant was
90
decanted. Then the densely cultured Gluconacetobacter hansenii suspension was added to the
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GO/medium wet mixture, making a total of 150 ml with 0.0725 wt% GO contents. The solution
92
was subsequently transferred to a Pyrex bakeware dish (18 cm × 18 cm) and incubated at room
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temperature without disturbance. After 2 days, a thin hydrogel of GO/BNC had formed, and it
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was harvested from the bakeware for cleaning. To remove the residual bacteria and growth
95
medium, the hydrogel was boiled in 2.5 L of 0.1 M NaOH aqueous solution for 2 h. The obtained
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RGO/BNC hydrogel was then dialyzed in de-ionized water for 1 day. The purified RGO/BNC
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hydrogel was dried to obtain an RGO/BNC membrane. In our preliminary test, the size and
98
contents of GO in membranes and membrane thickness affected the water flux and solute
99
rejection of RGO/BNC membranes. The specific GO concentration (0.0725 wt%), employed for
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preparing RGO/BNC membranes, provides the best flux performance and good solute rejection.
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Microstructure characterization and property measurements. Scanning electron microscopy
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(SEM, FEI Nova 2300 Field Emission SEM at an accelerating voltage of 10 kV) provided
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micron-scale images of RGO/BNC and pristine BNC. Atomic force microscopy (AFM) images
104
were obtained for determining the thickness of GO flakes, using a Dimension 3000 (Bruker Inc.)
105
instrument in light tapping mode. To investigate the relative oxygen and carbon ratio of GO and
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RGO flakes, carbon 1s peak was analyzed by X-ray photoelectron spectroscopy (XPS, a Physical
107
Electronics® 5000 VersaProbe II Scanning ESCA Microprobe). The pore size distribution of
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RGO/BNC membranes was measured by the Brunauer-Emmett-Teller (BET) method using an
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Autosorb-1C (AX1C-MP-LP) at 298 K.
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Stability tests of RGO/BNC membrane. To study the stability of the RGO/BNC membrane, we
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placed it in Petri dishes filled with solutions at pH 4, 7, and 9 and sonicated them for 5 hours
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(483 W, 8892, Cole-Parmer). The pH values were chosen because they occur in many natural and
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engineering aqueous systems.46 Subsequently, the release of RGO from the membrane was
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quantified from the UV-Vis absorbance spectra (Shimadzu UV-1800 spectrophotometer, 400 nm
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to 1000 nm) of the solutions. SEM was used to monitor the surface morphologies of the
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RGO/BNC film after sonication. To study the mass change of RGO/BNC membrane before and
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after sonication, thermo-gravimetric analysis (TGA) was performed using a TA Instruments
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Q5000 IR Thermogravimetric Analyzer in air (at rate of 5 °C/min).
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Because the GO membranes were frequently prepared by vacuum filtration, we made two
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types of control samples for comparison.26-28 First, a similar amount of base-washed RGO flakes
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was deposited on top of a BNC hydrogel, using the vacuum-assisted method, and dried to obtain
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a dry film. Second, BNC dispersions were pre-mixed with GO solutions and were then filtered to 5 ACS Paragon Plus Environment
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make membranes. Both control membranes were subjected to the same aqueous stability tests as
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the RGO/BNC membrane (Figure S1 in Supporting Information).
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Evaluation of mass transport performance of RGO/BNC membranes. The mass transport
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performance of RGO/BNC membranes was evaluated to estimate pore size of RGO/BNC by
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using a side-by-side diffusion cell system because it can use much smaller sample volume (~10
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mL) than that of benchtop cross-flow system (~15 L). An RGO/BNC membrane was first
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mounted between the two cells (Adams & Chittenden Scientific Glass, 5 mL volume). Then,
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ethanol and water were used to rinse the membrane several times to avoid subsequent air bubble
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formation. To test diffusion-driven transport through an RGO/BNC membrane, 0.5 mM of
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rhodamine 6G (R6G, ~ 1 nm, 479 Da) and lysozyme (3.8–4 nm, 14300 Da) were used. The
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observation of transport behavior of two model solutes (R6G and lysozyme) across RGO/BNC
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membrane helps to reveal approximate pore size of RGO/BNC membrane, and consequently,
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determines filtration type of RGO/BNC. R6G is cationic dye, thus it is positively charged.47 The
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isoelectric points for lysozyme are 10.5, and its pH value at 0.5 mM concentration is 3.53,
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indicating that lysozyme is positively charged under our experimental condition.48 The solute
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was introduced on the feed side, while the dialysate side was just DI water. Solutions in both
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cells were subjected to vigorous stirring to minimize concentration polarization effects close to
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the membrane. The diffusing concentration of the solute was monitored in the wavelength range
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of 300−700 nm, using a Shimadzu UV-1800 spectrometer. We utilized the RGO/BNC
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membranes grown in independent batches, and diffusion tests were conducted with three
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replicates.
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Ultrafiltration efficiency and flux tests. The water fluxes of the RGO/BNC membrane and
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commercial ultrafiltration membrane (YMGESP3001, GE) were tested using a benchtop cross-
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flow system, and then compared those permeate flux. The commercial ultrafiltration membrane,
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used for comparison, was designed for pre-treatment, dye reduction, and purification with 1,000
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Dalton cut-off sizes. The benchtop cross-flow system included a crossflow membrane cell
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(CF042D, Sterlitech Corp.) and a Hydracell pump (M03S, Wanner Engineering, Inc). During the
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measurement of the permeate flux, we set the pressure and the feed flux at 100 psi and 0.66
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L/min, with 25 °C water. For the experiments, we utilized the RGO/BNC membranes grown in
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independent batches and measured the water flux with three replicates. Furthermore, gold
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nanoparticles (AuNPs) with a diameter around 5 nm were synthesized using the seed-mediated
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growth method,49 and their size distribution was determined from TEM images. AuNP solutions
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were then filtered by RGO/BNC membranes, using above cross-flow system under 100 psi.
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Before and after filtration, AuNP concentrations in filtration/permeate solutions were measured
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by UV-Vis spectrometry (400 nm to 1000 nm). The rejection rate (RR) was calculated using the
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equation below:
159
ܴܴ =
ா ா
× 100,
160
where ܧ is the optical extinction of the feed solution, and ܧ is the optical extinction of the
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permeate solution.
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Photothermal and bactericidal performance of RGO/BNC membranes under illumination.
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The Photothermal performance of the membranes was tested using a solar simulator (Newport
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66921, Arc Lamp). Both the RGO/BNC membrane and BNC membrane were illuminated at a
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power density of 2.9 kW/m2 for 180 sec. The temperature map of the surface of both membranes
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under water was monitored by an IR camera (Ti 100, FLUKE). To test bactericidal activity, MG
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1655 E. coli was grown in Luria-Bertani liquid medium at 37 °C. All cultures were in 125 mL
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baffled shake flasks (25 mL working volume, shaking at 225 rpm). Cells in log phase (>108 live
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cells/ mL) were harvested after 12 h of incubation and then used for bactericidal tests. A layer of
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MG 1655 E. coli biofilm was grown on the RGO/BNC and BNC membrane surfaces, and then
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exposed to simulated sunlight for 180 secs at 2.9 kW/m2. Before/after light illumination, the
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biofilms were exposed to fluorescent dyes (Molecular Probes Live/Dead Bacterial cell viability
173
kit) for 30 min, and then imaged under a Leica microscope to identify live (blue fluorescent
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filter, 340-380 nm) and dead (green fluorescent filter, 450-490 nm) cells.50
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RESULTS AND DISCUSSION
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Characterization of the RGO/BNC membranes
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The RGO/BNC membranes were fabricated by in situ incorporation of GO flakes within
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the BNC network via bacteria-mediated growth under aerobic and static conditions (Figure 1).
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To determine the average thickness of synthesized GO flakes, they were deposited on a silicon
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substrate and measured with AFM. The thicknesses were ~ 1.0 ± 0.2 nm, corresponding to a
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bilayer of GO (the thickness of a monolayer is ~ 0.7 nm ) (Figure 2A).51 After washing, GO
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flakes were dispersed in broth solution with bacteria at an optimized concentration to achieve a
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desired BNC growth rate (Figure 1A). The GO dispersed solution was left undisturbed under
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ambient conditions to obtain GO/BNC hydrogels. To remove bacteria and residual broth solution
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from in situ grown GO/BNC hydrogel, it was immersed in NaOH solution (0.1 M) at boiling
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temperature, which partially reduced the GO flakes (discussed in detail below). The cleaned
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RGO/BNC hydrogel was dried to obtain a large, robust RGO/BNC membrane (Figure 1B).
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To understand the chemical reduction of GO during cleaning, GO flakes were added to a
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boiling temperature 0.1 M NaOH solution, which turned uniformly distributed GO particles into
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black aggregated particles, indicating the partial reduction and restacking of the RGO. To
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confirm the reduction of GO after exposure to the basic solution, X-ray photoelectron
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spectroscopy (XPS) was utilized (Figure 2B, 2C). The high resolution 1s spectra of carbon were
193
obtained and were deconvoluted into three peaks, corresponding one sp2 domain (C=C with a
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binding energy of 284.6 eV) and two oxidized sp3 domains (C–O with a binding energy of 286.6
195
eV, and C=O with a binding energy of 288.2 eV).52 The relative carbon and oxygen ratio was
196
calculated based on the peak area, and this ratio was utilized to estimate the reduction extent of
197
GO. For synthesized GO, the C/O ratio was 1.7, suggesting that ~ 58% of the GO surface was
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oxidized (Figure 2B). After an extensive base wash, the C/O ratio increased to 4.6, indicating
199
that ~37% of the oxygen functional groups were reduced (Figure 2C). This result confirms that
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base washing to kill residual bacteria also reduces GO flakes in the BNC matrix.
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In the absence of GO flakes, bacteria-mediated growth results in a white, translucent
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BNC membrane with outstanding flexibility and mechanical strength (Figure 2D).53 Because
203
bacteria-mediated synthesis of nanocellulose requires oxygen, a dense network of nanocellulose
204
fibers (20 –100 nm in diameter) forms near the air/liquid interface, where abundant oxygen is
205
available (Figure 2E). As the oxygen diffuses deeper into the medium, the first dense layer sinks,
206
and makes way for the formation of subsequent BNC layers, which, upon sinking, stack together
207
to form a 3D BNC network.33, 44 Due to this “layer-by-layer” formation, the cellulose nanofibrils 9 ACS Paragon Plus Environment
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are preferentially oriented parallel to the surface (i.e., normal to the thickness) of the membrane,
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which results in denser physical entanglements of the cellulose nanofibers parallel to the surface
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(Figure 2F). To form RGO/BNC membranes, GO flakes were added during in situ growth, and a
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subsequent base washing process was conducted (Figure 2G). Compared to pristine BNC
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membrane, the RGO/BNC membrane is smoother and has fewer fibrils protruding from the
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surface, due to the presence of 2D RGO sheets (Figure 2H). For quantitative comparisons,
214
nanoscale surface roughness of BNC and RGO/BNC membranes were measured by AFM, and
215
the results showed the surface roughness of 32.4 ± 9.46 nm and 25.0 ± 14.2 nm, respectively,
216
indicating the rougher surface of BNC membranes (Figure S6). Cross-sectional SEM images
217
showed that the membrane was ~8 µm thick (Figure 2I). The images also show the embedded
218
RGO flakes between BNC layers due to the “layered” formation of BNC, starting from the
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liquid/air interface as described above (Figure 2I). Because the hydrophilicity is an important
220
property to influence the water flux of membrane, the contact angles of RGO/BNC and BNC
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membranes were measured (Figure S6). Due to reduction of hydrophilic GO flakes during
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inevitable cleaning process, RGO/BNC membrane showed higher contact angle (65 ± 13°) than
223
that of BNC membrane (23 ± 5°).
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Mechanical and chemical stability of the RGO/BNC membranes
225
To investigate the mechanical and chemical stability of the membrane, we exposed it to
226
ultrasonic agitation for 5 hours in solutions at pH 4, 7, and 9 (see Figure S1 in Supporting
227
Information). Even after this vigorous mechanical agitation at environmentally-relevant pH
228
conditions, the membrane did not exhibit any signs of disintegration or loss of RGO flakes
229
(Figure 3A and its inset). This result was further supported by SEM images of the membrane
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surface, which did not show a discernable change in the morphology after sonication (Figure
231
3B). Then, to evaluate the thermal stability of the RGO/BNC membrane, TGA was conducted.
232
The membrane showed a first mass loss of ~2 wt.% at ~100 °C, due to the loss of absorbed
233
water. A second mass loss of ~3 wt.% at ~200 °C was attributed to the decomposition of
234
functional groups of GO.54 A third mass loss of ~46 wt.% began at 280°C, and was due to the
235
degradation of cellulose. A fourth mass loss (~49 wt.%) at 390 °C was attributable to the
236
continued decomposition of cellulose residual and sublimation or burning of damaged graphitic
237
regions.55 Based on the mass loss profiles of the RGO/BNC membrane, RGO, and pristine BNC
238
membrane, the mass loading of RGO in RGO/BNC was calculated to be ~45 wt.%, and it
239
suggested excellent thermal stability of the RGO/BNC membrane up to 200 °C. The RGO/BNC
240
membrane after ultrasonic treatment also showed an identical mass loss profile, implying that the
241
embedded RGO flakes within the BNC matrix remained intact (Figure 3C).
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As mentioned above, GO-based membranes have been extensively investigated in the
243
past several years. Most of these membranes were fabricated by vacuum filtration of GO flakes
244
onto a supporting membrane, but this coating method always leaves doubt about its long-term
245
aqueous stability.32 Here, we compared the mechanical stability of in situ embedded RGO/BNC
246
with that of an RGO/BNC membrane prepared by depositing RGO particles (base-washed) on
247
top of a BNC membrane using vacuum filtration. After 5 h of ultrasonic agitation in solutions at
248
pH 4, 7, and 9, the RGO particles had disintegrated completely, and the solution exhibited broad
249
absorbance, a feature of RGO flakes in solution (Figure 3D). This disintegration was further
250
confirmed by surface SEM images and quantified by TGA. After sonication, the membrane
251
prepared through vacuum filtration showed an initial mass loss (~5%) at 100 °C, attributed to
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absorbed water, and the decomposition of cellulose at ~280 °C (~63%) and at ~340 °C (~32%).
253
All of these findings indicated the absence of RGO flakes (Figure 3F).
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Conventional GO-based membranes rely on hydrogen bonding or metal ion incorporation
255
for mechanical stability. However, mechanical agitation during water filtration or cleaning
256
procedures, as well as pH variations in the feed water, can compromise the mechanical stability
257
of these membranes (Figure S1 in Supporting Information). In contrast, in situ RGO/BNC
258
membranes are robust because during the BNC growth, plate-like GO particles are physically
259
locked into the layered BNC matrices, which provides its excellent mechanical and chemical
260
stability. Moreover, intensive vortexing has been employed to wash used in situ RGO/BNC
261
membranes, and did not cause any discernable damage on these membranes, suggesting the
262
mechanical stability under the mechanical stress (Figure S1D). This finding further suggests the
263
durability of the in situ RGO/BNC membrane during potential cleaning process.
264
Mass transport performance and water flux tests
265
To probe the diffusive transport capability of small molecules across the RGO/BNC
266
membranes, we employed a two-cell setup (Figure 4A) and tested it with 0.5 mM of two model
267
solute systems, having different sizes and molecular weights: rhodamine 6G (R6G, ~ 1 nm, 479
268
Da) and lysozyme (3.8–4 nm, 14300 Da).56 Because ultrafilters have pore sizes between 1 nm to
269
100 nm, and thus remove contaminants via a size exclusion mechanism, these two different
270
solutes helped to determine the pore size and filtration capability of RGO/BNC membranes.57 A
271
UV-vis spectrometer was used to monitor the concentration of model solutes from the feed side
272
to the permeate side (see experimental section for details). For pristine BNC membrane, all two
273
solutes rapidly diffused through because the BNC fiber network is composed of micro-scale
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pores even if the nanofibers are densely packed (Figure 4B). By contrast, the addition of
275
graphene oxide flakes within the matrix completely blocked the diffusion of lysozyme (3.8–4
276
nm), although R6G (~1 nm) passed through (Figure 4B). These results are in accordance with
277
the BET measurements which indicate the pore size of the RGO/BNC membrane is around 2.2
278
nm (radius), which falls into the range of ultrafiltration membranes (Figure S3).58 Moreover, the
279
unique mass transport properties of GO-based membranes originate from the nanocapillary
280
network formed by lamellar stacking of GO, and the mass-transport behavior can be adjusted by
281
tuning functional groups or inserting external species with desired dimensions. 25,28 In this work,
282
the presence of bacterial cellulose nanofibers between RGO flakes will lead to an overall
283
tortuous network of pores in the membrane, even though no visible pores can be seen in a SEM
284
image of the surface of RGO/BNC membranes.
285
To further demonstrate the potential of the novel RGO/BNC membrane for an
286
ultrafiltration system, we performed flux tests and particle rejection tests using size-controlled
287
gold nanoparticles (AuNPs) via a benchtop cross-flow system (setup diagram in Figure 4C). For
288
a particle rejection test, spherical gold nanoparticles with diameters of 5.15 ± 0.4 nm were
289
synthesized using the seed-mediated method.49 The prepared AuNPs showed a very narrow size
290
distribution (RSD < 8 %), which made the particle rejection study accurate (Figure S2B in
291
Supporting Information). The particle rejection rates were calculated by measuring the UV-vis
292
extinction spectra of solutions before/after filtration through the RGO/BNC membranes (Figure
293
4D). This result suggested that AuNP of 5 nm diameter were ~100% rejected (inset of Figure
294
4D). In the same way, the rejection test was also performed for a commercial ultrafiltration
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membrane (pore size of around 1.66 nm), which also showed ~ 100% rejection for 5 nm gold
296
nanoparticles (Figure S2C in Supporting Information).
297
Under 100 psi, the RGO/BNC membranes showed higher water fluxes than a commercial
298
ultrafiltration (UF) membrane. Because the pore size for both membrane types belongs to the
299
range between UF and nanofiltration (NF), we intentionally tested water flux at a higher
300
operating pressure than the usual operating pressure for UF (7.3–73 psi). Over a five-hour-long
301
flux test after stabilization, the water flux of the RGO/BNC membrane was found to be 52.6 ±
302
2.5 L/m2 h, and that of the commercial ultrafiltration membrane was 21.6 ± 0.8 L/m2 h (Figure
303
4E). Importantly, the RGO/BNC membrane withstood an operating pressure as high as 100 psi
304
without any supporting membrane. This performance emphasized the remarkable mechanical
305
strength of RGO/BNC, considering that most of the GO-based membranes reported in the
306
literature require a support membrane or a carefully designed apparatus due to their limited
307
mechanical strength.59-63
308
Photothermal and bactericidal performance under illumination
309
Next, we examined the photothermal and bactericidal ability of the RGO/BNC membrane
310
using a Newport 66921 Arc Lamp with a power density of 2.9 kW/m2. We used IR imaging to
311
monitor the temperature profile of the RGO/BNC membrane in an aqueous environment during
312
illumination (Figure 5B). The reduction of GO flakes during inevitable sample preparation
313
(cleaning) process provides the benefits for better photothermal conversion efficiency because
314
the abundant delocalized π electrons in conjugated sp2-bonded carbon create the closely spaced
315
energy levels.22-24 Upon illumination, the temperatures of the RGO/BNC membrane rapidly
316
increased from room temperature (26 °C) to ~60 °C (Figure 5C). Specifically, the temperature
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rapidly increased during the first 20 seconds after the onset of irradiation and remained constant
318
over the entire duration (120 sec). In comparison, the pristine BNC membranes showed only a
319
small temperature increase (3 °C). The large rise in temperature was caused by the broad optical
320
absorption of many RGO flakes arranged within the BNC matrix. Once light was absorbed by
321
the RGO flakes, they immediately generated heat, which then dissipated to the surrounding water
322
and BNC.44 Due to the decrease of thermal radiation along the distance between IR camera and
323
surface (~30 cm), the temperature profile obtained from the IR camera underestimated the actual
324
temperature at the surface of the RGO/BNC membrane. Therefore, biological species were
325
exposed to temperature higher than ~60 °C. To test whether the heat generated by light exposure
326
would affect the mass transport and water flux performance of the RGO/BNC membrane, we
327
performed BET and water flux tests before and after long duration of light exposure (2.9
328
kW/m2).
329
membrane remained stable with minor variation after light exposure (Figures S3 and S4).
Both the pore size distribution and the water flux performance of RGO/BNC
330
To test the bactericidal ability, the RGO/BNC membrane was covered with stained E. coli
331
bacteria from a live/dead cell viability assay, and then light was shined on the membrane surface.
332
Before irradiation, both RGO/BNC and pristine BNC membranes showed substantial and well
333
distributed green fluorescence, corresponding to live bacteria, and no sign of red fluorescence,
334
indicating the absence of dead bacteria (Figure 5D). After irradiation (2.9 kW/m2) for 180 secs,
335
the bacteria on the RGO/BNC membrane exhibited predominantly red fluorescence (dead
336
bacteria) and a complete visible absence of green fluorescence. However, the E.coli-covered
337
pristine BNC membrane exhibited green fluorescence corresponding to live bacteria, even after
338
irradiation (Figure 5E). The SEM images showed morphology changes and leakage of bacteria,
339
indicating that the high temperature at the RGO/BNC membrane had disrupted the cell walls and 15 ACS Paragon Plus Environment
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cell membranes (Figure 5F, G). Before light irradiation, live E. coli bacteria on an RGO/BNC
341
membrane showed a rod-like structure, while after irradiation they were significantly shrunken
342
and wrinkled. Because the cell walls of E. coli are known to deteriorate near 70 °C,64 this change
343
implied that upon illumination, the surface of the RGO/BNC membrane had rapidly heated to
344
above 70 °C and killed bacteria within a short time (180 sec). Live E. coli bacteria on an
345
RGO/BNC membrane without illumination showed no dead bacteria cells even after 1 hour
346
exposure, indicating the bactericidal activity of RGO/BNC membrane only occur upon light
347
illumination (Figure S5). Here, we demonstrated the excellent bactericidal performance of the
348
RGO/BNC membrane in harvesting light, and this capability makes the RGO/BNC membrane
349
highly attractive for energy-saving and environmentally-friendly water purification applications.
350
ENVIRONMENTAL IMPLICATIONS
351
In this study, we presented an innovative approach that uses the photothermal effect of
352
RGO by embedding it in BNC structures. This new type of membrane can enhance the stability
353
and durability of a membrane and inhibit or delay microorganism growth on its surface. While
354
the most contemporary approaches to resisting biofouling rely on temporary chemical treatments,
355
combining the photothermal effect with a noble membrane design shows that anti-biofouling can
356
be achieved with sustainable and abundant sunlight.
357
We note that fully utilizing the photothermal property of RGO/BNC membranes can be
358
challenging. A possible implementation involves modifying a spiral-wound module system, as
359
shown in Figure 5A. The inner and outer surfaces of the membrane modules or feed channel
360
spacers can be equipped with low-energy LEDs for illumination, and can potentially be powered
361
by renewable energy sources, such as low-cost photovoltaic devices or triboelectric
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nanogenerators (TENGs).65 In TENGs, mechanical energy generated through fluid flow in the
363
UF process can be harnessed to produce light and to heat the membrane surface, reducing the
364
overall operational expense. In addition to spiral-wound module system, this suggested system
365
can also be applied to plate sheet membrane module by adding LED-equipped plates between the
366
membrane modules. This would be an exciting future research direction for realizing
367
photothermal membrane water filtration.
368
Here we demonstrated the anti-biofouling property of RGO/BNC membrane, which
369
originated from localized surface heating by photothermal effect of RGO particles. While we
370
successfully inhibit the biofilm growth on membrane by inactivating the bacteria, systematic
371
tests for the effects of extracellular polymeric substance and soluble microbial products
372
potentially produced by microorganism, mineral scaling, and organic fouling on membrane’s
373
performance (e.g., localized heating on the fouling behavior of membranes) should be conducted
374
in the future.
375
The novel fabrication method of incorporating RGO during ‘layer-by-layer’ growth of
376
BNC yields a well stacked the structure, with a pore size in the UF membrane range. In addition,
377
BNC production is considered eco-friendly because it needs only low-molecular weight sugar
378
and oxygen as food sources. Until now, many researchers prepared GO membranes through
379
vacuum filtration or spin coating without a polymer matrix25-28, but these fabrication methods
380
inevitably raised the mechanical stability concerns. However, the RGO/BNC membrane,
381
reported here, exhibits stable water flux under 100 psi loading and maintains chemical stability at
382
solution pH varying from 4 to 9. The water flux is higher than that of commercial UF membranes
383
under identical pressure. In summary, RGO/BNC membrane demonstrated here not only
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provides a novel anti-biofouling approach powered by solar energy, but also suggests a scalable,
385
eco-friendly, and cost-effective way to fabricate UF membranes for water purification.
386
SUPPORTING INFORMATION
387
The Supporting Information is available free of charge on the ACS Publications Website at DOI:
388
Additional physical and chemical stability test (Figure S1), AuNPs rejection data (Figure S2),
389
nitrogen isotherm and pore size distribution (Figure S3), water flux test under cyclic illumination
390
(Figure S4), bacterial cell viability and fluorescence images (Figure S5), and surface roughness
391
and contact angles (Figure S6) were included.
392
ACKNOWLEDGEMENTS
393
The authors acknowledge support from National Science Foundation Environmental Engineering
394
Program (CBET- 1604542) and Air Force Office of Scientific Research (Award # FA9550-15-1-
395
0228). H. Kwon received a fellowship from Washington University’s McDonnell Academy
396
Global Energy and Environment Partnership. The authors thank Prof. Lihong Wang from the
397
Department of Biomedical Engineering at Washington University for providing access to an IR
398
camera, and the Nano Research Facility (NRF) at Washington University for providing access to
399
electron microscopy facilities. The authors acknowledge Professor James C. Ballard for carefully
400
reviewing the manuscript.
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List of Figures
402
Figure 1. Fabrication of RGO/BNC membrane. Photographs show (A) GO in bacterial medium
403
and (B) in situ grown RGO/BNC membrane after cleaning and drying.
404
Figure 2. Chemical composition and microstructure of RGO/BNC membrane. (A) AFM image
405
of GO flakes deposited on a silicon substrate. X-ray photoelectron spectra of (B) pristine and (C)
406
base-washed GO. Photograph (D) and SEM images of (E) the surface and (F) a cross-section of a
407
pristine BNC membrane. Photograph (G) and SEM images of (H) the surface and (I) a cross-
408
section of an RGO/BNC membrane.
409
Figure 3. Stability of RGO/BNC membrane. UV-vis absorption spectra of (A) RGO/BNC and
410
(D) RGO-coated BNC immersed solutions (at pH 7) before and after ultrasonic agitation for 5 h.
411
The insets are photographs of an RGO/BNC membrane and an RGO-coated BNC membrane
412
after sonication. SEM images of (B) an RGO/BNC membrane and (E) an RGO-coated BNC
413
membrane after ultrasonic agitation. TGA analyses of (C) an RGO/BNC membrane and (F) an
414
RGO-coated BNC membrane before and after ultrasonic agitation.
415
Figure 4. Mass transport performance and water flux tests. (A) Schematic diagram of a two-cell
416
diffusion setup. (B) Diffusion of model solutes through pristine BNC and RGO/BNC
417
membranes. The average values of concentrations in the diffused part were obtained from three
418
replicates for diffusion studies. (C) Schematic diagram of cross-flow flux test setup. RGO/BNC
419
membranes were placed in between the cross-flow cell and tightly sealed. (D) UV-vis extinction
420
spectra indicating the rejection of 5 nm AuNPs filtered through RGO/BNC membranes using the
421
cross-flow system under 100 psi (inset shows feed and permeate solutions). (E) Water flux of
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RGO/BNC membranes (~8 µm thick) and commercial ultrafiltration membranes with three
423
replicates. 100 psi was applied for the flux tests.
424
Figure 5. Photothermal and bactericidal performance under illumination. (A) Schematic showing
425
antifouling mechanism of RGO/BNC membrane and a possible configuration of a spiral-wound
426
UF module coupled with LEDs. (B) IR images showing the temperature of the pristine BNC and
427
the RGO/BNC membrane in water under illumination at various time points. (C) Plot showing
428
the temperature of pristine BNC and the RGO/BNC membrane in water under 2.9 kW/m2
429
illumination, as a function of irradiation time. Fluorescence images of E. coli on BNC and
430
RGO/BNC membranes (D) before and (E) after irradiation.
431
RGO/BNC membranes (F) before and (G) after irradiation.
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Figure 2.
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Figure 3.
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Figure 4.
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TOC Art:
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