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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

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nanocellulose (BNC), which incoporates GO flakes into BNC in situ during its growth. In

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contrast to previously reported GO-based membranes for water treatment, the RGO/BNC

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membrane exhibited excellent aqueous stability under environmentally relevant pH conditions,

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vigorous mechanical agitation/sonication, and even high pressure. Importantly, due to its

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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

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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

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investigated for water purification and reclamation.4-6 However, fouling and consequent

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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

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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

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adjusting pH, adding disinfectants and biocides, and introducing quorum sensing molecules,

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have been suggested.12-15 However, most of these strategies introduce considerable operational

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costs and/or potential hazardous contaminants.12

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incorporation of nanomaterials (e.g., silver nanoparticles, TiO2 nanoparticles, and graphene oxide

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nanosheets), polymers (e.g., polyethylene glycol, polyvinyl alcohol, polyvinylpyrrolidone, and

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zwitterionic

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biomacromolecules) to engineer fouling-resistant membrane surfaces that can reduce biofilm

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growth and inactivate bacteria.8, 16-21 However, most of these methods involve additional thermal

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or chemical treatment steps. Furthermore, most techniques are effective for only a short period

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of time, because biofilm gradually adapts to imposed harsh environments.9 Even if 99.9% of

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biofilm is removed, the residual cells are sufficient to grow back and form a new biofilm. Highly

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efficient and cost-effective methods that overcome biofouling on water purification membranes

polymers),

and

other

materials

Researchers have also investigated the

(e.g.,

1 ACS Paragon Plus Environment

small

organic

molecules

and


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over a long period of time would immediately help meet the grand challenge of providing access

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to clean water.

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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

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can effectively absorb light and then convert it into heat. In our recent study, gold nanostars

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grown on graphene oxide (GO) flakes coating a commercial membrane were utilized as

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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

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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

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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-

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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-

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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

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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

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shaking at 250 rpm. The #1765 growth medium is composed of 2% (w/v) glucose, 0.5% (w/v)

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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

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centrifuged again to concentrate a wet mixture of GO and medium after supernatant was

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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

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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

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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

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contents of GO in membranes and membrane thickness affected the water flux and solute

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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

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were obtained for determining the thickness of GO flakes, using a Dimension 3000 (Bruker Inc.)

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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

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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:

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ܴܴ =

ா೑ ா೛

× 100,

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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

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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

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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

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eV, and C=O with a binding energy of 288.2 eV).52 The relative carbon and oxygen ratio was

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calculated based on the peak area, and this ratio was utilized to estimate the reduction extent of

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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

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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

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bacteria-mediated synthesis of nanocellulose requires oxygen, a dense network of nanocellulose

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fibers (20 –100 nm in diameter) forms near the air/liquid interface, where abundant oxygen is

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available (Figure 2E). As the oxygen diffuses deeper into the medium, the first dense layer sinks,

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and makes way for the formation of subsequent BNC layers, which, upon sinking, stack together

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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,

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nanoscale surface roughness of BNC and RGO/BNC membranes were measured by AFM, and

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the results showed the surface roughness of 32.4 ± 9.46 nm and 25.0 ± 14.2 nm, respectively,

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indicating the rougher surface of BNC membranes (Figure S6). Cross-sectional SEM images

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showed that the membrane was ~8 µm thick (Figure 2I). The images also show the embedded

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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

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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

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that of BNC membrane (23 ± 5°).

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Mechanical and chemical stability of the RGO/BNC membranes

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To investigate the mechanical and chemical stability of the membrane, we exposed it to

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ultrasonic agitation for 5 hours in solutions at pH 4, 7, and 9 (see Figure S1 in Supporting

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Information). Even after this vigorous mechanical agitation at environmentally-relevant pH

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conditions, the membrane did not exhibit any signs of disintegration or loss of RGO flakes

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(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

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3B). Then, to evaluate the thermal stability of the RGO/BNC membrane, TGA was conducted.

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The membrane showed a first mass loss of ~2 wt.% at ~100 °C, due to the loss of absorbed

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water. A second mass loss of ~3 wt.% at ~200 °C was attributed to the decomposition of

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functional groups of GO.54 A third mass loss of ~46 wt.% began at 280°C, and was due to the

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degradation of cellulose. A fourth mass loss (~49 wt.%) at 390 °C was attributable to the

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continued decomposition of cellulose residual and sublimation or burning of damaged graphitic

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regions.55 Based on the mass loss profiles of the RGO/BNC membrane, RGO, and pristine BNC

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membrane, the mass loading of RGO in RGO/BNC was calculated to be ~45 wt.%, and it

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suggested excellent thermal stability of the RGO/BNC membrane up to 200 °C. The RGO/BNC

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membrane after ultrasonic treatment also showed an identical mass loss profile, implying that the

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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

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past several years. Most of these membranes were fabricated by vacuum filtration of GO flakes

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onto a supporting membrane, but this coating method always leaves doubt about its long-term

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aqueous stability.32 Here, we compared the mechanical stability of in situ embedded RGO/BNC

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with that of an RGO/BNC membrane prepared by depositing RGO particles (base-washed) on

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top of a BNC membrane using vacuum filtration. After 5 h of ultrasonic agitation in solutions at

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pH 4, 7, and 9, the RGO particles had disintegrated completely, and the solution exhibited broad

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absorbance, a feature of RGO flakes in solution (Figure 3D). This disintegration was further

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confirmed by surface SEM images and quantified by TGA. After sonication, the membrane

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prepared through vacuum filtration showed an initial mass loss (~5%) at 100 °C, attributed to



252

absorbed water, and the decomposition of cellulose at ~280 °C (~63%) and at ~340 °C (~32%).

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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

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for mechanical stability. However, mechanical agitation during water filtration or cleaning

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procedures, as well as pH variations in the feed water, can compromise the mechanical stability

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of these membranes (Figure S1 in Supporting Information). In contrast, in situ RGO/BNC

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membranes are robust because during the BNC growth, plate-like GO particles are physically

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locked into the layered BNC matrices, which provides its excellent mechanical and chemical

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stability. Moreover, intensive vortexing has been employed to wash used in situ RGO/BNC

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membranes, and did not cause any discernable damage on these membranes, suggesting the

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mechanical stability under the mechanical stress (Figure S1D). This finding further suggests the

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durability of the in situ RGO/BNC membrane during potential cleaning process.

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Mass transport performance and water flux tests

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To probe the diffusive transport capability of small molecules across the RGO/BNC

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membranes, we employed a two-cell setup (Figure 4A) and tested it with 0.5 mM of two model

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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

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100 nm, and thus remove contaminants via a size exclusion mechanism, these two different

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solutes helped to determine the pore size and filtration capability of RGO/BNC membranes.57 A

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UV-vis spectrometer was used to monitor the concentration of model solutes from the feed side

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to the permeate side (see experimental section for details). For pristine BNC membrane, all two

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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

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graphene oxide flakes within the matrix completely blocked the diffusion of lysozyme (3.8–4

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nm), although R6G (~1 nm) passed through (Figure 4B). These results are in accordance with

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the BET measurements which indicate the pore size of the RGO/BNC membrane is around 2.2

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nm (radius), which falls into the range of ultrafiltration membranes (Figure S3).58 Moreover, the

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unique mass transport properties of GO-based membranes originate from the nanocapillary

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network formed by lamellar stacking of GO, and the mass-transport behavior can be adjusted by

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tuning functional groups or inserting external species with desired dimensions. 25,28 In this work,

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the presence of bacterial cellulose nanofibers between RGO flakes will lead to an overall

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tortuous network of pores in the membrane, even though no visible pores can be seen in a SEM

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image of the surface of RGO/BNC membranes.

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To further demonstrate the potential of the novel RGO/BNC membrane for an

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ultrafiltration system, we performed flux tests and particle rejection tests using size-controlled

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gold nanoparticles (AuNPs) via a benchtop cross-flow system (setup diagram in Figure 4C). For

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a particle rejection test, spherical gold nanoparticles with diameters of 5.15 ± 0.4 nm were

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synthesized using the seed-mediated method.49 The prepared AuNPs showed a very narrow size

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distribution (RSD < 8 %), which made the particle rejection study accurate (Figure S2B in

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Supporting Information). The particle rejection rates were calculated by measuring the UV-vis

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extinction spectra of solutions before/after filtration through the RGO/BNC membranes (Figure

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4D). This result suggested that AuNP of 5 nm diameter were ~100% rejected (inset of Figure

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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

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nanoparticles (Figure S2C in Supporting Information).

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Under 100 psi, the RGO/BNC membranes showed higher water fluxes than a commercial

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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


340

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



384

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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401

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



Page 22 of 33

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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.


SEM images of E. coli on

Page 23 of 33

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Figure 1.



433

Figure 2.


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Figure 3.



435 436

Figure 4.


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Figure 5.



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TOC Art:

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