Nanowire-Modified Three-Dimensional Electrode Enabling Low

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Nanowire-Modified 3D Electrode Enabling LowVoltage Electroporation for Water Disinfection Zheng-Yang Huo, Xing Xie, Tong Yu, Yun Lu, Chao Feng, and Hong-Ying Hu Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.6b01050 • Publication Date (Web): 24 Jun 2016 Downloaded from http://pubs.acs.org on June 27, 2016

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Nanowire-Modified 3D Electrode Enabling Low-

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Voltage Electroporation for Water Disinfection

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Zheng-Yang Huoa, Xing Xie*b, Tong Yua, Yun Lua, Chao Fengc and Hong-Ying Hu*ad

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a

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Environmental Protection Key Laboratory of Microorganism Application and Risk

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Control (SMARC), School of Environment, Tsinghua University, Beijing 100084, PR

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China. E-mail: [email protected]; Tel: +86-10-6279-4005.

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b

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Blvd, MC 131-24, Pasadena, CA 91125, USA. E-mail: [email protected]; Tel: +1-

Environmental Simulation and Pollution Control State Key Joint Laboratory, State

Linde+Robinson Laboratories, California Institute of Technology, 1200 E. California

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626-395-8716.

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c

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[email protected].

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d

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Laboratory, Tsinghua-Berkeley Shenzhen Institute, Shenzhen 518055, PR China.

Institute for Advanced Study, Tsinghua University, Beijing 100084, PR China. E-mail:

Shenzhen Environmental Science and New Energy Technology Engineering

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TABLE OF CONTENTS

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ABSTRACT

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More than 10% people in the world are still suffering from inadequate access to clean

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water. Traditional water disinfection methods (e.g., chlorination and ultraviolet radiation)

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have concerns of carcinogenic disinfection byproducts (DBPs) formation, pathogen

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reactivation, and/or excessive energy consumption. Recently, a nanowire-assisted

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electroporation-disinfection method was introduced as an alternative. Here, we develop a

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new copper-oxide nanowire (CuONW)-modified 3D copper foam electrode using a facile

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thermal oxidation approach. An electroporation-disinfection cell (EDC) equipped with

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two such electrodes has achieved superior disinfection performance (>7-log removal and

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no detectable bacteria in the effluent). The disinfection mechanism of electroporation

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guarantees an exceedingly low operation voltage (1 V) and energy consumption (25 J l -1)

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with a short contact time (7 s). Low operation voltage avoids chlorine generation, thus

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reduces the potential of DBPs formation. Due to irreversible electroporation damage on

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cell membranes, no bacteria re-growth/reactivation occurs during storage after EDC

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treatment. Water disinfection using EDCs has great potential for practical applications.

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INTRODUCTION

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Disinfection has protected people from bacterial infection for more than 100 years.

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Chlorination is the most common low-cost disinfection technology, but it inevitably

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produces carcinogenic disinfection byproducts (DBPs), e.g. Trihalomethanes (THM) and

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N-nitrosodimethylamine (NDMA), during disinfection and storage processes afterwards.

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[1-9]

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chlorine disinfection. In order to avoid the formation of chlorinated DBPs, ultraviolet

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(UV) disinfection, a non-oxidizing disinfection technique, has been used as a potential

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alternative. However, due to high energy consumption and the issue of bacteria re-

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growth/reactivation after UV inactivation,

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limited.

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Electroporation, a common and efficient process to introduce DNA into bacteria, can be a

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promising substitute of chlorination for water disinfection. [12-16] During electroporation,

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the permeability of cell membrane increases due to a strong electric field (several kV cm-

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1

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electric field is high enough, the damage to cell membrane is irreversible and inactivation

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occurs.

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[16, 22, 23]

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electroporation tends to avoid the formation of harmful DBPs. However, to generate the

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strong electric field, voltages as high as 1-10 kV are normally required, [25] which results

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in high cost and safety issues. [27]

Safety concerns regarding water reuse are driving the search of alternatives to

[10, 11]

applications of UV disinfection are

), thus the DNA transport across cellular membrane is enhanced.

[13, 16, 21]

[12-15, 17-20]

When the

Electroporation-based inactivation has been demonstrated with bacteria

, protozoa

[19, 24, 25]

and viruses

[26]

. Due to its disinfection mechanism,

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Nanostructures, e.g. nanowires, nanoparticles, nanobelts and nanotubes, have unique

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biological [28-31] and electronic [32-35] properties (e.g., field emission, high surface area and

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high conductivity) and may have specific interaction with bacteria

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control, or inhibit microbial activities).[38, 39] When one-dimension (1D) nanostructures

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are placed on the surface of a flat electrode, a much stronger electric field can be built up

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near the tip.

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magnitude stronger. As a result, even when the applied voltage is low, the electric field

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near the tip structure can still be strong enough to cause irreversible electroporation.

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Based on this phenomenon, the Cui group developed a conducting filter, where the two

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electrodes were prepared by modifying carbon nanotube (CNT)-coated polyurethane

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sponges with Ag nanowires.

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electrodes when water flew through the device. The CNT-coated sponge functioned as a

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macroscale porous conducting matrix, while the silver nanowires on the surface provided

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millions of nanoscale tips to achieve the strong electric field. This conducting filter

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achieved >6-log removal efficiency for bacteria disinfection. The same research group

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also developed other electrodes for electroporation based water disinfection: an Ag

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nanowires-modified CNT-coated cotton textile

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(CuONW)-modified copper mesh

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The voltages applied in these studies were significantly lower than that normally required

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for irreversible electroporation, but still higher than the typical voltages for water

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electrolysis (>2 V). [45-47] Therefore, one concern for this new disinfection process is that

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notable energy would be consumed for unnecessary water decomposition. Another

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concern is on the persistence of the inactivation caused by electroporation. It is not clear

[40, 41]

[36, 37]

(e.g., promote

If the tip is small enough, the electric field can be several orders of

[42]

A voltage of 10-20 V was applied across the two

[44]

[43]

and a copper-oxide nanowire

. Similar disinfection performance was reported.

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whether the inactivated bacteria can be reactivated during the water storage after

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treatment.

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Here in this study, we introduced a new CuONW-modified 3D copper foam electrode

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prepared by a facile thermal oxidation approach (Fig. 1a). An electroporation-disinfection

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cell (EDC) equipped with two CuONW-modified copper foam electrodes achieved

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superior disinfection performance with low applied voltages, energy consumption and

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DBPs formation potential. In addition, no bacteria re-growth/reactivation occurred during

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the storage process. This novel disinfection process is promising for practical water

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treatment.

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MATERIALS AND METHODS

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Electrode

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construction. Copper foams were cut into Φ = 1 cm × 0.5 cm as cylinder electrodes.

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Electrodes were etched with 1 M hydrochloric acid to remove the oxide layer and washed

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with de-ionized (DI) water for 3 times. Then electrodes were heated in air at 400 ºC for

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120 minutes. Prepared electrodes were then put into a plexiglass coaxial electrode holder

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(5 cm × 5 cm × 2.5 cm) with a plastic mesh (~100 µ0) in the middle in case of short

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circuit.

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Copper-oxide nanowire (CuONW) Characterization. Field-emission scanning

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electron microscopy (FE-SEM) images were taken on a FEI STRATA DB235 microscope

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at voltage of 5 kV. The crystal characterization of the CuONW was determined using a

fabrication

and

electroporation-disinfection

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cell

(EDC)

device

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single nanowire device by sonicating a CuONW-modified 3D copper foam electrode in

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ethanol to form a suspension containing individual nanowires. Nanowires were drop-cast

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onto a transmission electron microscopy (TEM) copper gird for analysis. TEM was

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performed on a JEOL JEM-200CX microscope with an accelerating voltage of 160 kV.

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Total chlorine and current measurement. Total chlorine concentrations in both control

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and treated samples were measured by a Hanna HI96724 total chlorine pocket

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colorimeter. All the voltages applied to EDC treatment were provided by a direct current

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power supply (DG1718E-5). The anode of the power supply was connected to one

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electrode and the cathode to the other. During EDC treatment, water samples were passed

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through electrodes and certain voltages were applied to those two electrodes. Currents in

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the circuit were measured by a digital multimeter (UNI-T UT39C).

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Bacteria inactivation with EDC. Escherichia coli (ATCC 15597), Enterococcus faecalis

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(ATCC 19433) and Bacillus subtilis (ATCC 6633) were cultured to log phase (12 h) and

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then diluted using normal saline solution (9.0 g l-1 sodium chloride) to ~107 CFU ml-1.

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Secondary effluents were collected from two wastewater treatment plants (WWTPs) with

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bacteria concentration of ~104 CFU ml-1. Each water sample (250 ml) flew through the

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EDC device at different hydraulic retention times (HRTs) varied from 1 to 15 s. At the

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same time, voltages varied from 0 to 5 V were applied to the device. Effluents were

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collected in sterilized centrifugal tubes. Bacterial concentrations of effluents and control

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samples were measured using standard spread plating techniques. Each sample was

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serially diluted, and then plated in duplicate and incubated at 37 °C for 24 h. Control

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samples was passed EDC at the same flow rate with the experiment samples without

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applying voltage. Treated and control samples were compared to determine the

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inactivation efficiency.

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Bacteria storage experiment. Normal saline solution (9.0 g l-1 sodium chloride) and DI

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water were sterilized at 121 ºC for 20 minutes. Secondary effluents were filtered by 0.22

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µm membrane to remove all the indigenous bacteria. E. coli samples (~ 107 CFU ml-1)

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were passed through the EDC operated at 1 V with a HRT of 3 s, 5 s or 7 s. Treated E.

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coli were harvested by centrifugation (HITACHI RX2 series, 14500 rpm corresponding

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to 17600 g for 15 minutes at 15 ºC) and then re-suspended in different substrates

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(distilled water, saline or filtered secondary effluent). Treated samples were then stored at

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25 ºC, which represents a typical temperature of nature aquatic environment. Then E. coli

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concentrations of samples were measured using standard spread plating techniques.

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Bacteria sample preparation for scanning electron microscopy (SEM). All bacteria

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samples for SEM were harvested by centrifuging at 14500 rpm (17600 g) for 15 minutes

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at 15 ºC (HITACHI RX2 series), and supernatants were removed. Then bacteria were

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fixed overnight in the fixative containing 0.1 M phosphate buffered solution (pH 7.3), 2%

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glutaraldehyde and 4% paraformaldehyde at 4 ºC, then washed with DI water. Samples

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were then dehydrated in increasing concentrations of ethanol solution (50, 70, 90 and

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100%), and dried in 100% tert-butyl alcohol. Samples were dispersed on a metal grid in

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preparation of SEM characterization.

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Live/Dead baclight staining experiment. All bacteria samples were harvested by

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centrifuging at 14500 rpm (17600 g) for 15 minutes at 15 ºC (HITACHI RX2 series).

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Samples were re-suspended in 0.1 M phosphate buffered solution (pH 7.3) to 100 µL.

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Live/Dead Baclight kit (Molecular Probes®) was used to implement the staining

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experiment. Equal volumes (2.5 µl) of SYTO 9 (0.6 mM) and PI (3 mM) dye solutions

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were added into samples including control. Samples were stored in dark for 30 minutes

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and examined using fluorescent microscopy.

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RESULTS AND DISCUSSION

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Fabrication and characterization of electroporation-disinfection cells (EDCs) with

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copper-oxide nanowire (CuONW)-modified copper foam electrodes.

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Copper foams were selected as the initial substrates to fabricate electrodes due to

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electrical conductivity, high porosity and surface area (more than 95% and ~104 m2 m-3,

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respectively)

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modified copper foams were synthesized through a simple one-step thermal oxidation

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approach: heating in air at 400 ºC for 2 h (Fig. 1b). During oxidization, CuONWs grew

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on the copper substrate and copper foam changed the color from bronze to black (Fig.

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1b). Because the physical surface of the copper foam was continuous in 3D, the CuONW-

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modification layer was also 3D continuous (Fig. 1c). The pore size of the copper foam

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was ~500 µm (Fig. 1c). CuONWs were rooted on the foam surface with lengths more

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than 10 µm (Fig. 1d) and diameters mostly less than 30 nm (Fig. 1e). High-resolution

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TEM image and electron diffraction pattern (Fig. 1f) confirmed the monoclinic structure

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of CuONW. Estimated from the density and pore size of the copper foam, the porosity

[48-50]

and relatively low cost (~$65 per m2 of 1 cm thick sheet). CuONW-

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and specific surface area were ~98% and ~104 m2 m-3, respectively. The CuONW-

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modified copper foam still maintained a high conductance of ~0.4 S cm-1 as a solid bulk

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material.

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An EDC was built by placing two pieces of the CuONW-modified copper foam

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electrodes (φ1 cm × 0.5 cm) in a plexiglass coaxial electrode holder (5 cm × 5 cm × 2.5

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cm) (Figs. 1a and S1). For electroporation-based disinfection, our new electrode revealed

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obvious advantages. The 3D macroscale porous structure allowed water to easily flow

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through with little hydraulic resistance. Moreover, the complex flowing pattern within the

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porous electrode increased the opportunity for microbes to approach the electrode surface

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where electric filed was significantly enhanced by the CuONWs and electroporation-

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disinfection occurred. The big pores with sizes of several hundred µm were unlikely to be

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clogged by microbes, which were normally less than 10 µm. Since CuONWs were

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directly grown out of the copper foam by in situ thermal oxidation, the physical contact

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between them was stable and electrical connection was guaranteed.

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Performance of EDC for water disinfection.

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The performance of our EDC was evaluated by treating the water samples that contained

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~107 colony forming units (CFU) ml-1 (Cin - concentration in influent) E. coli. To obtain

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specifics hydraulic retention times (HRTs), water samples flew through the EDC with

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aimed flow rates that were controlled by a peristaltic pump. Considering that the volume

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of electrodes (φ1 cm × 1 cm) is 0.785 cm3, flow rates were kept in the range of 6.72 to

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47.1 ml min-1, corresponding to hydraulic retention times (HRTs) of 7 to 1 s. At a

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specific HRT, a voltage varied from 0 to 10 V was applied across the two copper foam

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electrodes. The E. coli concentrations in the effluent (Ceff) were carefully analyzed and

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log removal efficiencies were calculated (E = -log (Ceff/Cin)). As the results shown in Fig.

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2a, removal efficiencies generally increased with HRT and applied voltage. When the

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HRT was 1 s, the EDC equipped with CuONW-modified copper foam electrodes

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achieved >7-log removal efficiency at 5 V and no E. coli detection in the effluent.

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Increasing the HRT to 5 and 7 s effectively lowered the voltages requirement for

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achieving the same performance to 2 and 1 V, respectively. Scanning electron

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microscopy (SEM) images confirm the occurrence of membrane damage. Compared to

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untreated E. coli whose cell membranes were complete and smooth (Fig. 2b), treated E.

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coli (1 V, 7 s) had obvious electroporation holes on the surface (Figs. 2c and S2)

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indicating lethal membrane damage. The results of staining test with Live/Dead Baclight

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kit (Figs. 2d and e) also suggested that E. coli cells lost the membrane integrities during

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treatment, because Syto 9 entered all the cells despite of membrane integrity and PI only

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entered the cells with damaged membrane (see supporting information for additional

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discussion). [51] When EDC equipped with non-treated copper foams (no-CuONWs on the

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surface), the removal efficiency was marginal if the applied voltages were less than 5 V.

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To investigate the energy consumption and potential health risk from formation of DBPs,

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currents in the circuit and total chlorine concentrations in the effluent were measured.

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The sample was normal saline, which contained 9.0 g l-1 sodium chloride. The HRT was

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fixed at 7 s corresponding to the fastest flow rate for complete inactivation after 1 V

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treatment and applied voltages varied from 0 to 5 V. As the results shown in Fig. 2f,

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when applied voltages were not high than 1 V, currents were minimum ( secondary effluent > DI water. The E. coli concentration at

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specific storage time over 24 h were analyzed. As the results shown in Figs. 3a-c, E. coli

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was inactivated immediately and completely with 1 V, 7 s treatment. During the storage

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process in normal saline (Fig. 3a), sterile secondary effluent (Fig. 3b) and DI water (Fig.

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3c) afterwards, no E. coli was detected, indicating no re-growth/reactivation.

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When the water sample was treated with 1 V, 3 s, E. coli was almost not inactivated

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directly after treatment and the concentrations of re-suspended E. coli were similar with

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the initial cell concentrations (~107 CFU ml-1). However, cell inactivation gradually

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occurred during storage. When treated E. coli were cultured in normal saline, sterile

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secondary effluent and DI water for 24 h, their concentrations decreased to 104, 102 CFU

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ml-1 and no live bacteria detection, respectively (Fig. 3d). The extension of membrane

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damage caused by electroporation would be enlarged by great difference of salinities

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between cytoplasm and substrate (Figs. 3d and e). Hence, bacteria inactivation during

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storage were varied in different storage substrates: DI water > secondary effluent >

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normal saline. Such inactivation phenomenon was more obvious after 1 V, 5 s treatment

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(Fig. 3e). For untreated samples, E. coli inactivation during storage was insignificant

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(Fig. 3f). These results suggested that although not inactivating E. coli cells immediately,

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the short time (3 s and 5 s) EDC treatment had caused cell damage, which was

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irreversible and eventually resulted in cell inactivation when E. coli were stored in the

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tested substrates.

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Characterization of E. coli in EDC-treated water during storage.

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Results of staining experiment (Figs. 4a and b) suggested that treated (1 V, 3 s) E. coli

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cells lost membrane integrities during storage. As shown in Fig. 4a, compared with

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untreated sample containing few PI stained (membrane-compromised) bacteria, the

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sample right after 1 V, 3 s treatment (0 h) contained considerable PI stained E. coli. More

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bacteria were stained by PI after 4 h, indicating more E. coli had compromised

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membranes. The number of PI stained bacteria decreased after 12 h, because the total

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number of integral bacteria decreased, indicated by the Syto 9 staining results (Fig. 4b).

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The proportion of PI stained bacteria continuously increased to ~97% after 24 h (Fig. 4c),

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which confirmed no bacterial re-growth/reactivation. SEM images (Figs. 4d-k) further

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showed the morphologies of E. coli stored in normal saline for 0-24 h after 1 V, 3 s

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treatment. Similar with untreated E. coli (Fig. 4d), E. coli cells right after treatment still

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had complete and smooth membranes (Fig. 4e). However, significant damages could be

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observed on the surface after 4 h storage (Fig. 4f), and after 12 h storage, the treated E.

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coli strains could hardly maintain their cell configuration due to severely compromised

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membranes (Figs. 4g and h). After 24 h, cells were disintegrated completely: cell

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membranes twisted together and their structures could hardly be observed (Figs. 4i-k).

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These evidences demonstrated that no bacteria re-growth/reactivation but inactivation

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occurred during storage after EDC treatment. These outstanding features enabled EDC

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treatment become a promising substitution for the common UV irradiation disinfection

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by avoiding bacteria re-growth/reactivation after treatment.

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With sufficient EDC treatment (e.g., 1 V, 7 s), bacteria were inactivated immediately and

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became uncultivable (Fig. 2). The mechanism has been reveled previously. Nanowire-

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enhanced electric field has strong dipole-dipole interaction with the lipid bilayer of cell

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membrane, which lead to thinning of membrane and finally large electroporation pores.

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[12, 18, 20]

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inactivation occurs (Fig. 2c).

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or high voltage) EDC treatment, low dosage treatment (1 V, 5 s in our case) would form

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primary small electroporation pores on cell membrane with radii of at most several

Consequently, cell inclusion flows out exceedingly and immediate bacteria [12, 53]

Compared to high dosage (either long treatment time

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hundred nanometers (Fig. 5).[12] These primary electroporation pores were too small for

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PI intercalation (Fig. 4c) and cell inclusion outflow, thus treated bacteria were detectable

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when cultured in nutrient rich substrate right after treatment (e.g., nutrient agar) (Fig. 3e).

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However, stabilized by strong electric field, these primary small electroporation pores

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were irreversible due to adhesion of hydrophilic groups of phospholipid from cell

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membrane and became water pathways (Step 1, Fig. 5).

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water inflow and cell inclusion outflow were prompted by difference of salinities

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between cytoplasm and substrate, which enlarged the electroporation “pores” during

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storage (Fig. 4c and Figs. 4f-h). [17] As a result, secondary damage of membrane formed,

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cell structure broke down (Figs. 4i-k) and the cell died subsequently (Step 2, Fig. 5). It

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was worth noting that the extension of membrane damage would be enlarged by great

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difference of salinities between cytoplasm and substrate (Figs. 3d and e). Hence, bacteria

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inactivation during storage were varied in different storage substrates: DI water >

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secondary effluent > normal saline. Considering that nature water bodies (rivers and

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lakes) had similar salinity as secondary effluent, EDC effluent would be safe and reliable

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when was discharged into environment.

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Since UV disinfection destroys the bacteria DNA structure instead of the membrane

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integrity, the UV treated bacteria that become uncultivable right after treatment can

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maintain the integrate membranes for over 24 h.

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recover and become cultivable again in suitable environment.

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treated bacteria will lose membrane integrities and cannot recover during storage due to

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irreversible electroporation damages. Thus, no bacteria re-growth/reactivation occurs

[10]

[17]

Through the water pathway,

These uncultivable bacteria can

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[11]

Conversely, the EDC

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during storage if bacteria have been inactivated and become uncultivable after EDC

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treatment, which makes EDC a more reliable disinfection technology compared to UV.

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In summary, we have developed a new CuONW-modified 3D copper foam electrode by a

319

facile thermal oxidation approach. An EDC equipped with two such electrodes has

320

achieved superior disinfection performance (> 7 log removal and no detectable bacteria in

321

the effluent) with an applied voltage as low as 1 V and energy consumption of 25 J l-1,

322

and with low potential of DBP formation. No bacteria re-grow during storage after EDC

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treatment due to irreversible electroporation damage on cell membrane. EDCs can be

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easily powered by batteries or solar cells. The energy consumption is