Role of Reverse Divalent Cation Diffusion in Forward Osmosis

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Role of Reverse Divalent Cation Diffusion in Forward Osmosis Biofouling Ming Xie, Edo Bar-Zeev, Sara M. Hashmi, Long D Nghiem, and Menachem Elimelech Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.5b02728 • Publication Date (Web): 27 Oct 2015 Downloaded from http://pubs.acs.org on November 1, 2015

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Environmental Science & Technology

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Role of Reverse Divalent Cation Diffusion in Forward Osmosis Biofouling

5 6 7 8 9 10

Ming Xie 1, 2, Edo Bar-Zeev 1,3, Sara M. Hashmi 1, Long D. Nghiem 2, and Menachem

11

Elimelech1* 1

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Department of Chemical and Environmental Engineering Yale University, New Haven, CT 06520-8286, United States 2

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3

Strategic Water Infrastructure Laboratory, School of Civil, Mining and Environmental Engineering, University of Wollongong, Wollongong, NSW 2522, Australia

Zuckerberg Institute for Water Research, Ben Gurion University of the Negev, Sede Boqer Campus, Midreshet Ben Gurion, 84990, Israel

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* Corresponding author: Menachem Elimelech, Email: [email protected], Phone: (203) 432-2789

1

ACS Paragon Plus Environment


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ABSTRACT

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We investigated the role of reverse divalent cation diffusion in forward osmosis (FO) biofouling.

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FO biofouling by Pseudomonas aeruginosa was simulated using pristine and chlorine-treated

26

thin-film composite polyamide membranes with either MgCl2 or CaCl2 draw solution. We

27

related FO biofouling behavior―water flux decline, biofilm architecture, and biofilm

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composition―to reverse cation diffusion. Experimental results demonstrated that reverse

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calcium diffusion led to significantly more server water flux decline in comparison with reverse

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magnesium permeation. Unlike magnesium, reverse calcium permeation dramatically altered the

31

biofilm architecture and composition, where extracellular polymeric substances (EPS) formed a

32

thicker, denser, and more stable biofilm. We propose that FO biofouling was enhanced by

33

complexation of calcium ions to bacterial EPS. This hypothesis was confirmed by dynamic and

34

static light scattering measurements using extracted bacterial EPS with the addition of either

35

MgCl2 or CaCl2 solution. We observed a dramatic increase in the hydrodynamic radius of

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bacterial EPS with the addition of CaCl2, but no change was observed after addition of MgCl2.

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Static light scattering revealed that the radius of gyration of bacterial EPS with addition of CaCl2

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was 20 times larger than that with the addition of MgCl2. These observations were further

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confirmed by transmission electron microscopy imaging, where bacterial EPS in the presence of

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calcium ions was globular, while that with magnesium ions was rod-shaped.

41 42

TOC Art

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2


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INTRODUCTION

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Forward osmosis (FO) could potentially find a wide range of applications in water and

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wastewater treatment, particularly with challenging and difficult to treat wastewaters

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Membrane fouling in FO has been shown to be less detrimental and more reversible compared to

48

pressure-driven membrane processes such as nanofiltration (NF) and reverse osmosis (RO)

49

Studies have demonstrated that FO fouling could be easily controlled by simple physical

50

(hydrodynamic) means, such as increasing the cross flow velocity and subsequently the shear

51

rate at the membrane surface 6. Consequently, there have been several successful demonstrations

52

of FO for the treatment of wastewaters with high fouling propensity with no or limited

53

pretreatment, such as landfill leachate 7, anaerobic digester concentrate

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solution 10, 11, and municipal wastewater 12-14.

8, 9

1

.

2-6

.

, activated sludge

55

Despite the low fouling propensity of FO, membrane performance might still be hindered

56

by membrane biofouling, resulting in higher operational cost and shorter membrane life.

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Membrane biofilms that develop on the membrane surface comprise complex sessile microbial

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communities permanently attached to the surface by gel-like, extracellular polymeric substances

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(EPS)

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dead cells encased in a polymeric matrix

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resistant to removal by various biochemical treatment methods due to the protection provided by

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the EPS scaffold

17, 20

63

and nucleic acids

21-23

15-17

. This microbial cake layer features a multi-cellular architecture comprising live and 18, 19

. Once attached and developed, biofilms are

that contains a mixture of polysaccharides and proteins as well as uronic .

64

Reverse draw solute diffusion, a unique mass transport phenomenon in FO, has the

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potential to impact FO membrane fouling. Permeate water flux in FO is coupled with reverse

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permeation of draw solute

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to promote colloid destabilization, which enhanced membrane fouling and reduced fouling

68

reversibility by simple physical cleaning

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demonstrated to enhance humic acid fouling due to elevated ionic strength at the membrane

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interface 28. Notably, reverse diffusion of divalent cations (e.g., Ca2+ or Mg2+) may induce more

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severe FO organic fouling in comparison with monovalent cations (e.g., Na+)

24-26

. Reverse permeation of NaCl draw solution was recently shown 27

. Moreover, reverse transport of NaCl was

3


29

. For example,


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significant water flux decline was observed in FO due to alginate (polysaccharide) fouling using

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MgCl2 as draw solution 3, 30 .

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It is widely accepted that divalent cations, particularly calcium, could promote membrane

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organic fouling 31, 32. Calcium ions strongly interact with organic foulants via specific interaction

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with carboxylic functional groups, 33, 34 thereby aggravating membrane organic fouling. Divalent

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calcium ions can also enhance membrane biofouling

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dissolved polysaccharide chains to form gelatinous networks characteristic of EPS

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However, to date, no studies exist on the role of reverse permeation of divalent cations on

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biofouling in FO.

35

by forming multiple crosslinks between 15, 22, 36

.

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In this study, we investigated the role of reverse divalent cation diffusion, specifically of

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calcium and magnesium ions, in FO biofouling. Thin-film composite membranes with varying

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degrees of reverse draw solute flux were obtained by chlorine treatment of the polyamide active

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layer. FO membrane biofouling induced by reverse diffusion of either calcium or magnesium

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ions was quantified in terms of water flux decline and biofilm characteristics. Light scattering

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measurements and transmission electron microscopy imaging were used to elucidate the FO

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membrane biofouling behavior and to identify the underlying biofouling mechanisms induced by

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reverse divalent cation diffusion.

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MATERIALS AND METHODS

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FO Membrane and Active Layer Modification. In all experiments, a pristine, polyamide

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thin-film composite (TFC) FO membrane (Hydration Technologies Innovation, Albany, OR) was

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used as a reference and compared with a chlorine-treated counterpart. The polyamide TFC FO

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membrane was treated with sodium hypochlorite (NaClO) to reduce membrane selectivity (i.e.,

95

decrease salt rejection)

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flux compared to the pristine (untreated) membrane. Specifically, the TFC membrane was

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immersed in 1,000 mg/L NaClO solution adjusted to pH 7.0 for one hour and then soaked in 0.1

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M NaOH solution for eight hours. The membrane was then rinsed thoroughly with deionized

37

, thereby generating a membrane with an increased reverse draw salt

4


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99 100


water and stored wet at 4 °C. The chemically modified membrane was denoted as chlorinetreated membrane.

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Experimental Setup for FO Biofouling. Synthetic wastewater was prepared and

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sterilized for FO biofouling experiments according to the recipe described in our previous study

103

20

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role of reverse salt permeation on biofouling. Ionic strength and pH of the synthetic wastewater

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were 16 mM and 7.6 ± 0.2, respectively. Analytical grade NaCl, MgCl2, or CaCl2 were used as

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draw solutions. The concentration of each draw solution was adjusted to achieve an initial water

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flux of 20 ± 1 L m-2 h-1 in FO biofouling experiments.

; no calcium or magnesium was added into the synthetic wastewater in order to elucidate the

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Biofouling experiments were performed using an axenic monoculture of Pseudomonas

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aeruginosa (ATCC 27853) as a model bacterial strain. P. aeruginosa was cultivated overnight at

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37 °C to an optical density (OD600) of 0.6 in Luria-Bertani (LB) broth (BD Biosciences). A sub

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culture (50 mL) was then centrifuged at 25 °C and 4,000 rpm for 15 minutes to remove LB

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supplements and resuspended in 20 mL of sterile wastewater.

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All FO biofouling experiments were carried out using a custom-made FO setup that was 37, 38

114

used in previous studies

. FO membrane cell dimensions were 7.7 cm × 2.6 cm × 0.3 cm

115

(length, width, and height, respectively), with an active membrane surface area of 20.0 cm2. Both

116

feed and draw cross-flows (8.5 cm/s) were recycled using two gear pumps (Micropump, Cole-

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Parmer). Permeate flux was monitored using an electric balance (Denver Instrument) interfaced

118

with a data acquisition system.

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Before each biofouling experiment, the FO system was cleaned and disinfected. Cleaning

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was carried out by flushing the FO system with 10% bleach, followed by EDTA (5 mM),

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absolute ethanol, and ending with three DI water rinses. Each of the above solutions (2 L) was

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circulated through the system for one hour.

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Biofouling experiments commenced after the permeate water flux was stabilized at 20 ±

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1 L m-2 h-1. Feed wastewater (2 L) was inoculated with 20 mL of P. aeruginosa to achieve an

125

initial bacteria concentration of 6.0 ± 0.5 × 107 cells L-1. Feed wastewater temperature was

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maintained constant at 25 oC using a heater/chiller (Thermo Scientific, IL). Feed wastewater was 5



127

monitored periodically for pH, conductivity, and colony-forming unit (CFU) counts. At the end

128

of each biofouling experiment, membrane subsections were cut from the FO membrane sample

129

to evaluate various biofilm characteristics by confocal laser scanning microscopy (CLSM), total

130

organic carbon (TOC), and protein measurements.

131

Confocal Laser Scanning Microscopy (CLSM) Analysis. Membrane subsections

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were cut (1 cm2) from the center of the biofouled membrane. The membrane section was placed

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in a petri dish with 3 mL of sterile wastewater. The biofouled sample was then stained with

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SYTO 9 and propidium iodide (PI) to identify live and dead cells (LIVE/DEAD BacLight,

135

Invitrogen, USA). Simultaneously, the biofouled membrane samples were stained with 30 µL of

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50 µM concavalin A (Con A, Alexa Flour 633, Invitrogen, MA) to identify biofilm EPS. All

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staining was conducted for 30 minutes in the dark. Biofilm samples were rinsed three times with

138

sterilized wastewater to remove any unbound stains. Biofouled membrane samples were then

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mounted in a custom-made characterization chamber for CLSM imaging 39.

140

Confocal images were captured using a CLSM (Zeiss LSM 510, Carl Zeiss, Inc.)

141

equipped with a Plan-Apochromat 20×/0.8 numerical aperture objective. SYTO 9, PI, and Con A

142

were excited with three sets of lasers, respectively: 488 nm argon, 561 nm diode-pumped solid

143

state, and 633 nm helium-neon laser. A minimum of three Z stack random fields (635 µm × 635

144

µm) were collected for each sample, with a slice thickness of 2.3 µm, using ZEN (Carl Zeiss,

145

Inc.) to obtain a representative biofilm ortho image. Biofilm dimensions were analyzed by

146

capturing a minimum of ten random Z stack regions (90 µm × 90 µm) for each sample, with a

147

slice thickness of 1.2 µm, using ZEN (Carl Zeiss, Inc.).

148

Confocal image analysis was performed using Auto-PHLIP-ML, ImageJ software, and

149

MATLAB. Thickness and biovolume were determined for the live and dead bacterial cells

150

(SYTO 9 and PI staining), and EPS (Con A staining) components of the biofilm. Total

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biovolume and thickness were calculated by summing live, dead, and EPS components.

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Total Organic Carbon (TOC) and Protein Measurement. TOC and protein

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concentration of biofilm were quantified. For TOC measurements, membrane sub-sections (2 cm

154

× 2 cm) were re-suspended in 24 mL sterile wastewater with 10 µL of 1 M HCl. Samples were

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then sonicated on ice in three 30-second cycles to remove organic content from the membrane. 6


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TOC in the resultant solution was then analyzed using a TOC analyzer (TOC-V, Shimadzu,

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Japan). TOC concentrations were normalized by membrane sample area. For protein

158

quantification, membrane sub-sections (2 cm × 2 cm) were cut and suspended in 2 mL

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Eppendorf tubes with 1 mL 1X Lauber buffer (50 mM HEPES (pH 7.3), 100 mM NaCl, 10%

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sucrose, 0.1% 3-[(3-cholamidopropyl)-dimethylammonio]-1 propanesulfonate, and 10 mM

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dithiothreitol) and probe sonicated on ice (three 30-second cycles) using an ultra-cell disruptor.

162

The membrane was then removed and cell extracts were centrifuged at 12,000 rpm for 10

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minutes to remove detritus matter. The supernatant was then collected for protein quantification

164

using BCA protein assay kit (Thermo Scientific, IL).

165 166

Determination of Reverse Draw Solution Flux. The reverse flux of draw solution in FO biofouling was determined using the total mass balance:

J salt =

167

( Ct Vt − C0V0 ) At

168

where C0 and Ct are the concentration of the draw solute in the feed at time 0 and t, respectively;

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V0 and Vt are the volume of the feed at time 0 and t, respectively; A is the membrane area, and t

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is the operating time of the FO experiment. Draw solute concentrations of NaCl, MgCl2, and

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CaCl2 in the feed solution were quantified by ion chromatography (Dionex, Thermo Scientific,

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IL) equipped with an IonPac CS14 cation-exchange column (4 mm × 250 mm (width × length),

173

ion-exchange capacity of 1300 µeq), and 10 mM methanesulfonic acid eluent delivered at 1

174

mL/min.

175

EPS Extraction and Characterization. Bacterial EPS were extracted to elucidate the

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mechanism of interaction with reverse permeation of calcium or magnesium ions. Bacterial EPS

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extraction and purification followed a procedure described in our previous study

178

biofilm culture of P. aeruginosa (ATCC 27853) was cultivated with 20 g of untreated glass

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fibers (Corning Glass Works, Corning, NY) in 250 mL of LB using a modified method

180

employed by Liu and Fang 40. After the extraction, the EPS solution was filtered through a 0.2

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µm hydrophilic nylon filter (Millipore) and dialyzed through a membrane with a molecular

182

weight cut-off of 3,500 Da (Spectra/Por).

7


32

. Briefly, a


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For transmission electron microscopy (TEM) visualization, bacterial EPS extracts were

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dropped on a formvar/carbon coated copper grid (200 meshes, Tedpella, Inc., Redding, CA) and

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stained with acidic (pH 2.5) Alcian blue (500 mg/L) for 10 minutes at room temperature. Excess

186

stain was then removed with a Whatman paper (Whatman, GE, Pittsburgh, PA). The grids were

187

air-dried at room temperature and samples were imaged with a FEI Tecnai Osiris microscope

188

(FEI, Hillsboro, OR), operating at an acceleration voltage of 200 kV.

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Dynamic and static light scattering were performed to investigate the interaction of

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bacterial EPS and calcium or magnesium ions. Light scattering experiments were conducted with

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a multiangle CGS-5000F goniometer setup (ALV GmbH) equipped with eight individual SO-

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SIPD optical detectors and a Verdi V2 continuous wave DPSS laser (COHERENT), operating at

193

532 nm. Dynamic light scattering measurements were obtained with a fixed detector at 90°. Data

194

were collected in intervals of 30 seconds for all samples continuously over three hours. We

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monitored the intensity of the scattered light as a proxy for the growth of the EPS gel

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CONTIN analysis was used to obtain particle size distributions. For static light-scattering

197

measurements, the normalized scattered light intensity was obtained simultaneously by all eight

198

detectors over an angular range of 17 – 135°, corresponding to wave vectors 0.0046 < q < 0.0305

199

nm-1.

41

.

200 201

RESULTS AND DISCUSSION

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Transport Properties of Pristine and Chlorine-Treated TFC FO Membranes. We

203

chemically modified pristine TFC membranes by exposing the polyamide active layer to chlorine

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in order to obtain membranes with varying degrees of salt permeabilities or reverse salt flux.

205

Table 1 summarizes key membrane transport parameters—water permeability (A), salt

206

permeability (B), and membrane structural parameter (S)—of the pristine and chlorine-treated

207

membranes, as determined following our previous publication 42.

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[Table 1]

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Exposure of the membrane polyamide active layer to chlorine alters the structure and

210

properties of the polyamide layer, leading to an increase in water permeability and a decrease in 8


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43, 44

211

membrane selectivity (i.e., salt rejection)

. Such an increase in both membrane A and B

212

values is expected based on the established membrane permeability-selectivity tradeoff

213

tradeoff is an intrinsic relationship between A and B, where increasing the water permeability is

214

accompanied by a rapidly decreasing salt selectivity. The chlorine-treated membrane exhibited

215

one-order of magnitude higher salt (NaCl) permeability compared to the pristine membrane

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(Table 1). As a result, reverse calcium and magnesium fluxes by the chlorine-treated membrane

217

were five times higher than those with the pristine membrane (Figures 1C and 2C).

218

[Figure 1]

219

[Figure 2]

1, 45

; this

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Reverse Diffusion of Draw Solution Calcium Ions Exacerbates Biofouling.

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Reverse calcium permeation markedly enhanced FO membrane biofouling (Figure 1). Water flux

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decline was aggravated in the following increasing order: pristine TFC membrane using NaCl

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draw solution, pristine TFC membrane using CaCl2 draw solution, and chlorine-treated TFC

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membrane using CaCl2 draw solution (Figure 1A). The order of water flux decline correlated

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with reverse calcium flux (Figure 1C), which increased from zero (pristine TFC membrane using

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NaCl draw solution) to 12.2 mmol m-2 h-1 (chlorine-treated TFC membrane using CaCl2 draw

227

solution).

228

Reverse calcium diffusion significantly altered biofilm architecture (Figure 1B). Biofilm

229

thickness gradually increased as the reverse calcium flux increased. More importantly, at the

230

conclusion of biofouling, biofilm density of the chlorine-treated TFC membrane using CaCl2

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draw solution was twice as high as that of the pristine TFC membrane using NaCl draw solution

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(Table 2). This increase in biofilm density was consistent with the biofilm image captured by

233

confocal microscopy (Figure 1B). The thick and dense biofilm structure induced by reverse

234

calcium permeation accelerated the biofilm-enhanced osmotic pressure phenomenon 23, 46, where

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the biofilm hinders the back diffusion of salt into feed bulk solution, thus elevating the osmotic

236

pressure near the membrane surface on the feed side. As a result, the biofilm-enhanced osmotic

237

pressure decreased the net osmotic pressure driving force, which resulted in a dramatic water

238

flux decline.

239

[Table 2] 9



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240

We hypothesize that the formation of such thick and dense biofilm was driven by the

241

specific interaction of calcium ions with bacterial EPS, as evidenced by the measured biofilm

242

composition (Table 2). Specifically, we observed a significant increase in EPS biovolume, TOC

243

biomass, and total protein mass when reverse calcium flux increased (Table 2). The EPS

244

biovolume obtained from confocal microscopy also increased when reverse calcium flux

245

increased (Figure 1C). The increase in EPS biovolume was not induced by bacterial proliferation,

246

given the similar total cell volumes ranging from 33.3 µm3/µm2 (pristine TFC membrane using

247

NaCl draw solution) to 36.2 µm3/µm2 (chlorine-treated TFC membrane using CaCl2 draw

248

solution) (Table 2), but was mainly driven by calcium complexation with polysaccharides

249

resulting in a more stable and cohesive biofilm structure. Calcium ions can preferentially bind to

250

carboxyl groups of polysaccharides to form a highly interconnected network

251

calcium complexation phenomenon was also observed in RO biofouling, where the presence of

252

calcium promoted EPS adsorption onto the membrane surface 32.

48

47

,

. A similar

253

Reverse Diffusion of Draw Solution Magnesium Ions Does Not Enhance

254

Biofouling. Reverse magnesium flux did not have a significant effect on FO biofouling in

255

comparison with reverse calcium diffusion (Figure 2). Despite the chlorine-treated TFC

256

membrane exhibiting four times higher reverse magnesium flux than the pristine TFC membrane

257

(Figure 2C), only a relatively small difference in water flux decline was observed with the

258

chlorine-treated membrane and the pristine membrane (Figure 2A).

259

No significant variation in the biofilm architecture (Figure 2B) and composition (Table 3)

260

took place when reverse magnesium permeation increased. For instance, biofilm thickness and

261

density were almost identical for the pristine (39 µm, 8.7 ng/µm2) and chlorine-treated (42 µm,

262

9.1 ng/µm2) TFC membrane (Table 3). In addition, negligible difference in biofilm composition,

263

particularly EPS biovolume, was observed between the pristine membrane (12.8 µm3/µm2) and

264

chlorine-treated membrane (15.1 µm3/µm2) using MgCl2 draw solution (Table 3).

265

[Table 3]

266

Calcium Complexation with Bacterial EPS is the Culprit for Enhanced

267

Biofouling. According to our results, the reverse permeation of calcium or magnesium ions

268

resulted in dramatically different FO biofouling behaviors. We provide further support for this 10


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mechanism by comparing the aggregation profiles of bacterial EPS following the addition of

270

calcium or magnesium ions using dynamic and static light scattering measurements (Figure 3).

271

The aggregation profile of bacterial EPS in the presence of calcium ions was markedly different

272

from that in the presence of magnesium ions (Figure 3A). Following calcium addition, the light-

273

scattering intensity increased rapidly with time, indicating rapid gelation and growth of bacterial

274

EPS aggregates

275

bacterial EPS hydrodynamic radius (Rh) from 28 ± 2 to 70 ± 3 nm (Figure S1, Supporting

276

Information). By contrast, the light-scattering intensity of bacterial EPS in the presence of

277

magnesium ions remained unchanged for the entire aggregation experiment (Rh of 21 ± 2 nm,

278

Figure 3A).

41

. The increase in light-scattering intensity corresponds to the growth of

279

[Figure 3]

280

The addition of calcium ions triggered a dramatic change in the structure of bacterial EPS

281

aggregates (Figure 3B). A log/log plot of the relative scattering intensity (I/I0) as a function of

282

the wave vector (q) demonstrates the markedly different structure of bacterial EPS aggregates in

283

the presence of calcium or magnesium (Figure S2, Supporting Information). Specifically, for

284

bacterial EPS aggregates in the presence of calcium, the intensity profile scales as I/I0 ∼ q-Df,

285

with an exponent Df = 1.58, indicating a fractal dimension Df comparable to that expected for

286

diffusion-limited aggregation

287

bacterial EPS in the presence of magnesium (Figure 3B) is attributed to its small hydrodynamic

288

size (21 ± 2 nm) and suggests insignificant aggregation or gelation.

49

. By contrast, the nearly isotropic scattering profile of the

289

The light intensity data from static light-scattering measurements were also plotted as

290

Kc/R ~ q2 (with K being and optical constant, c the solution concentration, R the Rayleigh ratio,

291

and q the wave vector) to estimate the radius of gyration of bacterial EPS in the presence of

292

calcium or magnesium ions 47 (Figure S3, Supporting Information). The y-intercept in Figure S3

293

for bacterial EPS in the presence of calcium ions was nearly 20 times smaller than that in the

294

presence of magnesium ions, indicating the densification and gelation of bacterial EPS with the

295

addition of calcium ions

296

calcium (118 ± 6 nm) was four times larger than that in the presence of magnesium ions (25 ± 3

297

nm) (Figure S3 and Table S1, Supporting Information).

50

. Indeed, the radius of gyration of bacterial EPS in the presence of

11



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298

The markedly different structures of bacterial EPS aggregates were further verified by

299

TEM imaging (Figures 3C and D). The TEM images show that bacterial EPS in the presence of

300

calcium ions is globular and thick, while that with magnesium ions is rod-shaped and patchy.

301

The light-scattering measurements and TEM imaging confirmed that complexation of

302

calcium ions to bacterial EPS resulted in accumulation of more polysaccharides on the

303

membrane surface

51-53

. Calcium ions, possessing a smaller hydrated radius (0.41 nm) than

54

304

magnesium (0.43 nm) , can form inner sphere complexes with carboxyl groups of bacterial EPS

305

55, 56

306

biofilm in comparison with magnesium. As a result, the tightly-bound biofilm structure hindered

307

back diffusion of salts into the feed bulk solution 4, 46, which exacerbated water flux decline due

308

to biofilm-enhanced osmotic pressure and impaired membrane performance.

. This ion complexation and bridging of EPS resulted in a thicker, denser, and more stable

309

The calcium complexation mechanism proposed here highlights the significant

310

enhancement in bacterial EPS aggregation and subsequent FO membrane biofouling due to

311

reverse permeation of calcium ions in comparison with magnesium ions. The proposed

312

biofouling mechanism agrees with previous results of enhanced RO membrane organic fouling

313

with calcium ions compared with magnesium ions. For instance, Lee and Elimelech observed

314

much stronger long-range adhesion forces of alginate in the presence of calcium ions than with

315

magnesium ions 57. They attributed this marked difference in the range of adhesion forces to the

316

specific interaction between calcium ions with the carboxylic groups of alginate and the

317

formation of a cross-linked gel network. In another study, atomic force measurements further

318

confirmed that calcium ions greatly enhanced humic acid fouling by complexation to humic acid,

319

compared with magnesium ions which did not complex to humic acid molecules 34.

320

Implications. The substantially higher biofouling propensity induced by reverse

321

permeation of calcium compared to that with magnesium has significant implications for

322

mitigating FO biofouling. More attention should be paid to the selection of a proper draw

323

solution in order to minimize FO biofouling. Our results suggest the use magnesium-based draw

324

solutions rather than calcium-based solutions, because calcium complexation with bacterial EPS

325

enhances membrane biofouling. However, with the development of FO membranes of high

326

selectivity, application of monovalent draw solution (such as NaCl) is desirable because of the 12


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327

higher draw solute diffusivity in comparison with divalent draw solutes 1, which minimizes

328

internal concentration polarization, thereby achieving better membrane performance.

329

AUTHOR INFORMATION

330

Corresponding Author

331

* Phone: +1 (203) 432-2789. Fax: +1 (203) 432-4387. Email: [email protected]

332

Notes

333

The authors declare no competing financial interest.

334

ACKNOWLEDGMENTS

335

We acknowledge the postdoctoral fellowship to E.B. by the United States-Israel Binational

336

Agricultural Research and Development (BARD) Fund. We also would like to thank Dr. Joseph

337

Wolenski from the Molecular, Cellular, and Developmental Biology Department at Yale

338

University for technical assistance in our use of the CLSM. We also acknowledge the use of

339

facilities (light scattering instrument and transmission electron microscopy) supported by

340

YINQE.

341

ASSOCIATED CONTENTS

342

Supporting Information

343

Details on water flux decline of pristine and chlorine-treated membrane using NaCl draw

344

solution (Figure S1), hydrodynamic radii of bacterial EPS with the addition of calcium or

345

magnesium as a function of time (Figure S2), estimated radius of gyration of bacterial EPS

346

aggregate with the presence of calcium or magnesium ions (Figure S3), calculated factual

347

dimension by a log-log plot of the relative intensity as a function of the wave vector (Figure S4),

348

and estimated radii of gyration and hydrodynamic radii for bacterial EPS aggregates with the

349

presence of magnesium or calcium ions (Table S1). This information is available free of charge

350

via the internet at http://pubs.acs.org/.

351

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365 366

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367 368

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9. Xie, M.; Nghiem, L. D.; Price, W. E.; Elimelech, M., Toward Resource Recovery from Wastewater: Extraction of Phosphorus from Digested Sludge Using a Hybrid Forward Osmosis– Membrane Distillation Process. Environ. Sci. Technol. Lett. 2014, 1, (2), 191-195.

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10. Achilli, A.; Cath, T. Y.; Marchand, E. A.; Childress, A. E., The forward osmosis membrane bioreactor: A low fouling alternative to MBR processes. Desalination 2009, 239, (1– 3), 10-21.

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11. Cornelissen, E. R.; Harmsen, D.; de Korte, K. F.; Ruiken, C. J.; Qin, J.-J.; Oo, H.; Wessels, L. P., Membrane fouling and process performance of forward osmosis membranes on activated sludge. J. Membr. Sci. 2008, 319, (1-2), 158-168.

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12. Cath, T. Y.; Gormly, S.; Beaudry, E. G.; Flynn, M. T.; Adams, V. D.; Childress, A. E., Membrane contactor processes for wastewater reclamation in space: Part I. Direct osmotic concentration as pretreatment for reverse osmosis. J. Membr. Sci. 2005, 257, (1-2), 85-98.

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14. Xie, M.; Nghiem, L. D.; Price, W. E.; Elimelech, M., A Forward Osmosis–Membrane Distillation Hybrid Process for Direct Sewer Mining: System Performance and Limitations. Environ. Sci. Technol. 2013, 47, (23), 13486-13493. 14


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17. De Beer, D.; Stoodley, P., Microbial Biofilms. In The Prokaryotes, Rosenberg, E.; DeLong, E.; Lory, S.; Stackebrandt, E.; Thompson, F., Eds. Springer Berlin Heidelberg: 2013; pp 343-372.

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18. Bar-Zeev, E.; Zodrow, K. R.; Kwan, S. E.; Elimelech, M., The importance of microscopic characterization of membrane biofilms in an unconfined environment. Desalination 2014, 348, (0), 8-15.

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19. Herzberg, M.; Elimelech, M., Biofouling of reverse osmosis membranes: Role of biofilmenhanced osmotic pressure. J. Membr. Sci. 2007, 295, (1–2), 11-20.

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20. Bar-Zeev, E.; Elimelech, M., Reverse Osmosis Biofilm Dispersal by Osmotic BackFlushing: Cleaning via Substratum Perforation. Environ. Sci. Technol. Lett. 2014, 1, (2), 162166.

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21. Wingender, J.; Flemming, H.-C., Biofilms in drinking water and their role as reservoir for pathogens. Int. J. Hyg. Environ. Health 2011, 214, (6), 417-423.

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22. Decho, A. W., Overview of biopolymer-induced mineralization: What goes on in biofilms? Ecol. Eng. 2010, 36, (2), 137-144.

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23. Herzberg, M.; Elimelech, M., Biofouling of reverse osmosis membranes: Role of biofilmenhanced osmotic pressure. J. Membr. Sci. 2007, 295, (1-2), 11-20.

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24. Xie, M.; Nghiem, L. D.; Price, W. E.; Elimelech, M., Comparison of the removal of hydrophobic trace organic contaminants by forward osmosis and reverse osmosis. Water Res. 2012, 46, (8), 2683-2692.

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25. Lee, K. Y.; Mooney, D. J., Alginate: properties and biomedical applications. Prog. Polym. Sci. 2012, 37, (1), 106-126.

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26. Phillip, W. A.; Yong, J. S.; Elimelech, M., Reverse Draw Solute Permeation in Forward Osmosis: Modeling and Experiments. Environ. Sci. Technol. 2010, 44, (13), 5170-5176.

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27. Boo, C.; Lee, S.; Elimelech, M.; Meng, Z.; Hong, S., Colloidal fouling in forward osmosis: Role of reverse salt diffusion. J. Membr. Sci. 2012, 390–391, (0), 277-284.

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28. Xie, M.; Nghiem, L. D.; Price, W. E.; Elimelech, M., Impact of humic acid fouling on membrane performance and transport of pharmaceutically active compounds in forward osmosis. Water Res. 2013, 47, (13), 4567-4575.

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29. She, Q.; Jin, X.; Li, Q.; Tang, C. Y., Relating reverse and forward solute diffusion to membrane fouling in osmotically driven membrane processes. Water Res. 2012, 46, (7), 24782486.

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30. Zou, S.; Wang, Y.-N.; Wicaksana, F.; Aung, T.; Wong, P. C. Y.; Fane, A. G.; Tang, C. Y., Direct microscopic observation of forward osmosis membrane fouling by microalgae: Critical flux and the role of operational conditions. J. Membr. Sci. 2013, 436, 174-185.

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31. Lee, S.; Elimelech, M., Relating organic fouling of reverse osmosis membranes to intermolecular adhesion forces. Environ Sci Technol 2006, 40, (3), 980-7.

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32. Herzberg, M.; Kang, S.; Elimelech, M., Role of Extracellular Polymeric Substances (EPS) in Biofouling of Reverse Osmosis Membranes. Environ. Sci. Technol. 2009, 43, (12), 4393-4398.

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33. Xiang, Y.; Liu, Y.; Mi, B.; Leng, Y., Molecular Dynamics Simulations of Polyamide Membrane, Calcium Alginate Gel, and Their Interactions in Aqueous Solution. Langmuir 2014, 30, (30), 9098-9106.

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34. Li, Q.; Elimelech, M., Organic Fouling and Chemical Cleaning of Nanofiltration Membranes: Measurements and Mechanisms. Environ. Sci. Technol. 2004, 38, (17), 4683-4693.

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35. Bar-Zeev, E.; Passow, U.; Romero-Vargas Castrillón, S.; Elimelech, M., Transparent Exopolymer Particles: From Aquatic Environments and Engineered Systems to Membrane Biofouling. Environ. Sci. Technol. 2015, 49, (2), 691-707.

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36. de Kerchove, A. J.; Elimelech, M., Calcium and Magnesium Cations Enhance the Adhesion of Motile and Nonmotile Pseudomonas aeruginosa on Alginate Films. Langmuir 2008, 24, (7), 3392-3399.

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37. Yip, N. Y.; Tiraferri, A.; Phillip, W. A.; Schiffman, J. D.; Hoover, L. A.; Kim, Y. C.; Elimelech, M., Thin-Film Composite Pressure Retarded Osmosis Membranes for Sustainable Power Generation from Salinity Gradients. Environ. Sci. Technol. 2011, 45, (10), 4360-4369.

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38. Yip, N. Y.; Tiraferri, A.; Phillip, W. A.; Schiffman, J. D.; Elimelech, M., High Performance Thin-Film Composite Forward Osmosis Membrane. Environ. Sci. Technol. 2010, 44, (10), 3812-3818.

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39. Bar-Zeev, E.; Zodrow, K.; Kwan, S.; Menachem, E., The importance of microscopic charaterization of membrane biofilms in an unconfined environment. Desalination 2014, 348, 815.

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40. Liu, H.; Fang, H. H. P., Extraction of extracellular polymeric substances (EPS) of sludges. J. Biotechnol. 2002, 95, (3), 249-256.

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41. Hintermair, U.; Hashmi, S. M.; Elimelech, M.; Crabtree, R. H., Particle Formation during Oxidation Catalysis with Cp Iridium Complexes. J. Am. Chem. Soc. 2012, 134, (23), 9785-9795.

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42. Cath, T. Y.; Elimelech, M.; McCutcheon, J. R.; McGinnis, R. L.; Achilli, A.; Anastasio, D.; Brady, A. R.; Childress, A. E.; Farr, I. V.; Hancock, N. T.; Lampi, J.; Nghiem, L. D.; Xie, M.; Yip, N. Y., Standard Methodology for Evaluating Membrane Performance in Osmotically Driven Membrane Processes. Desalination 2013, 312, 31-38.

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43. Kwon, Y.-N.; Leckie, J. O., Hypochlorite degradation of crosslinked polyamide membranes: II. Changes in hydrogen bonding behavior and performance. J. Membr. Sci. 2006, 282, (1–2), 456-464. 16


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44. Do, V. T.; Tang, C. Y.; Reinhard, M.; Leckie, J. O., Degradation of Polyamide Nanofiltration and Reverse Osmosis Membranes by Hypochlorite. Environ. Sci. Technol. 2012, 46, (2), 852-859.

467 468 469

45. Geise, G. M.; Park, H. B.; Sagle, A. C.; Freeman, B. D.; McGrath, J. E., Water permeability and water/salt selectivity tradeoff in polymers for desalination. J. Membr. Sci. 2011, 369, (1–2), 130-138.

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46. Hoek, E. M. V.; Elimelech, M., Cake-Enhanced Concentration Polarization: A New Fouling Mechanism for Salt-Rejecting Membranes. Environ. Sci. Technol. 2003, 37, (24), 55815588.

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47. Sarkisova, S.; Patrauchan, M. A.; Berglund, D.; Nivens, D. E.; Franklin, M. J., CalciumInduced Virulence Factors Associated with the Extracellular Matrix of Mucoid Pseudomonas aeruginosa Biofilms. J. Bacteriol. 2005, 187, (13), 4327-4337.

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48. Fang, Y.; Al-Assaf, S.; Phillips, G. O.; Nishinari, K.; Funami, T.; Williams, P. A.; Li, L., Multiple Steps and Critical Behaviors of the Binding of Calcium to Alginate. J. Phys. Chem. B 2007, 111, (10), 2456-2462.

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49. Mylon, S. E.; Chen, K. L.; Elimelech, M., Influence of Natural Organic Matter and Ionic Composition on the Kinetics and Structure of Hematite Colloid Aggregation: Implications to Iron Depletion in Estuaries. Langmuir 2004, 20, (21), 9000-9006.

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50. Shen, C. L.; Fitzgerald, M. C.; Murphy, R. M., Effect of acid predissolution on fibril size and fibril flexibility of synthetic beta-amyloid peptide. Biophys. J. 1994, 67, (3), 1238-1246.

484 485 486

51. de Kerchove, A. J.; Elimelech, M., Formation of Polysaccharide Gel Layers in the Presence of Ca2+ and K+ Ions: Measurements and Mechanisms. Biomacromolecules 2006, 8, (1), 113-121.

487 488

52. Hong, S.; Elimelech, M., Chemical and physical aspects of natural organic matter (NOM) fouling of nanofiltration membranes. J. Membr. Sci. 1997, 132, (2), 159-181.

489 490 491

53. Seidel, A.; Elimelech, M., Coupling between chemical and physical interactions in natural organic matter (NOM) fouling of nanofiltration membranes: implications for fouling control. J. Membr. Sci. 2002, 203, (1–2), 245-255.

492 493

54. Nightingale, E. R., Phenomenological Theory of Ion Solvation. Effective Radii of Hydrated Ions. J. Phys. Chem. 1959, 63, (9), 1381-1387.

494 495

55. Bruni, F.; Imberti, S.; Mancinelli, R.; Ricci, M. A., Aqueous solutions of divalent chlorides: Ions hydration shell and water structure. J. Phys. Chem. 2012, 136, (6), -.

496 497

56. Piirtola, L.; Uusitalo, R.; Vesilind, A., Effect of mineral materials and cations on activated and alum sludge settling. Water Res. 2000, 34, (1), 191-195.

498 499

57. Lee, S.; Elimelech, M., Relating Organic Fouling of Reverse Osmosis Membranes to Intermolecular Adhesion Forces. Environ. Sci. Technol. 2006, 40, (3), 980-987.

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500

Table 1: Key membrane transport parameters (average ± standard deviation from triplicate

501

measurement) of pristine and chlorine-treated thin-film composite polyamide FO membrane

502 A

B

NaCl rejection

S

(L m-2 h-1 bar-1)

(L m-2 h-1)

(%)

(µm)

Pristine

1.72 ± 0.02

0.17 ± 0.01

98.1 ± 0.8 %

425 ± 31

Chlorine-treated

2.93 ± 0.04

1.42 ± 0.08

93.3 ± 1.0%

413 ± 20

Membrane

503

18


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504

Table 2: Comparing key parameters of biofilm architecture and composition using NaCl and CaCl2 draw solution by pristine and

505

chlorine-treated thin-film composite (TFC) membranes

506 Biofilm architecture

Biofilm composition

Average biofilm a thickness (µm)

Biofilm density (ng/µm3) b

“Live” cell biovolume a (µm3/µm2)

“Dead” cell biovolume a (µm3/µm2)

EPS biovolume a (µm3/µm2)

Total protein mass (pg/µm2) c

TOC biomass (pg/µm2) c

Pristine TFC membrane, NaCl draw

37 ± 2

8.3 ± 1.1

21.2 ± 4.1

12.1 ± 2.3

8.3 ± 3.6

21.7 ± 2.5

0.33 ± 0.07

Pristine TFC membrane, CaCl2 draw

40 ± 3

8.9 ± 0.8

22.5 ± 5.1

14.6 ± 1.1

9.9 ± 2.2

28.1 ± 4.5

0.41 ± 0.03

Chlorine-treated TFC membrane, CaCl2 draw

66 ± 4

18 ± 1

24 ± 2.4

12.2 ± 2.9

25.6 ± 1.4

43.1 ± 6.2

1.27 ± 0.05

Operating condition

507 508

a

biofilm thickness and biovolume were averaged, with standard deviation (SD) calculated from ten random samples in duplication experiments. b

509

Biofilm density was estimated by TOC biomass per total biovolume (including “live”, “dead” and EPS). c Average TOC and protein biomasses

510

were presented with SD calculated from four measurements by two membrane coupons.

19



Page 20 of 23

511

Table 3: Comparing key parameters of biofilm architecture and composition using NaCl and MgCl2 draw solution by pristine and

512

chlorine-treated thin-film composite (TFC) membranes

513 Biofilm architecture

Biofilm composition

Average biofilm a thickness (µm)

Biofilm density b (ng/µm3)

“Live” cell biovolume a (µm3/µm2)

“Dead” cell biovolume a (µm3/µm2)

EPS biovolume a (µm3/µm2)

Total protein mass a (pg/µm2)

TOC biomass c (pg/µm2)

Pristine TFC membrane, NaCl draw

37 ± 2

8.3 ± 1.1

21.2 ± 4.1

12.1 ± 2.3

8.3 ± 3.6

21.7 ± 2.5

0.33 ± 0.07

Pristine TFC membrane, MgCl2 draw

39 ± 1

8.7 ± 1.2

18.6 ± 1.1

13.4 ± 4.5

12.8 ± 2.9

30.7 ± 4.5

0.39 ± 0.06

Chlorine-treated TFC membrane, MgCl2 draw

42 ± 4

9.1 ± 1.2

19.6 ± 1.1

11.4 ± 5.5

15.1 ± 1.8

31.1 ± 2.5

0.42 ± 0.07

Operating condition

514 515

a

biofilm thickness and biovolume were averaged, with standard deviation (SD) calculated from ten random samples in duplication experiments. b

516

Biofilm density was estimated by TOC biomass per total biovolume (including “live”, “dead” and EPS). c Average TOC and protein biomasses

517

were presented with SD calculated from four measurements by two membrane coupons.

20


Page 21 of 23


518 519 520 521

Figure 1: (A) Representative water flux in forward osmosis biofouling as a function of

522

cumulative permeate volume. (B) Representative three-dimensional biofilm architecture was

523

captured by confocal laser scanning microscope (CLSM) (a perspective of a 635 µm × 635 µm

524

field of view), taken at the conclusion of each biofouling run. Biofilms were stained with Con A

525

(blue), SYTO 9 (green), and PI (red) dyes specific for EPS (polysaccharides), “live” cells, and

526

“dead” cells, respectively. (C) EPS biovolume as a function of reverse Ca2+ flux. Error bars

527

represent standard deviations for both reverse Ca2+ flux (four measurements in duplicate

528

experiments) and EPS biovolumes (ten random samples in duplication experiments).

21



Page 22 of 23

529 530 531

Figure 2: (A) Representative water flux in forward osmosis biofouling as a function as

532

cumulative permeate volume. (B) Representative three-dimensional biofilm architecture was

533

captured by confocal laser scanning microscope (CLSM) (a perspective of a 635 µm × 635 µm

534

field of view), taken at the conclusion of each biofouling run. Biofilms were stained with Con A

535

(blue), SYTO 9 (green), and PI (red) dyes specific for EPS (polysaccharides), “live” cells, and

536

“dead” cells, respectively. (C) EPS biovolume as a function of reverse Mg2+ flux. Error bars

537

represent standard deviations for both reverse Mg2+ flux (four measurements in duplicate

538

experiments) and EPS biovolumes (ten random samples in duplication experiments).

22 ACS Paragon Plus Environment

Page 23 of 23


539 540 541

Figure 3: (A) Dynamic and (B) static light scattering measurements of bacterial EPS

542

aggregation with calcium or magnesium ion. Representative TEM image of (C) bacterial EPS

543

aggregate with the presence of calcium ions and (D) bacterial EPS aggregate with the presence

544

of magnesium ions.

23 ACS Paragon Plus Environment

Role of Reverse Divalent Cation Diffusion in Forward Osmosis

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