Electrochemical Approach for Effective Antifouling ... - ACS Publications

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Electrochemical Approach for Effective Antifouling and Antimicrobial Surfaces Sheng Long Gaw,† Sujoy Sarkar,‡ Sivan Nir,‡ Yafit Schnell,‡ Daniel Mandler,‡ Zhichuan J. Xu,*,† Pooi See Lee,*,† and Meital Reches*,‡ †

School of Materials Science and Engineering, Nanyang Technological University, 50 Nanyang Avenue, 639798, Singapore Institute of Chemistry The Hebrew University of Jerusalem, Edmond J. Safra Campus, Givat Ram, Jerusalem 9190401, Israel

‡

S Supporting Information *

ABSTRACT: Biofouling, the adsorption of organisms to a surface, is a major problem today in many areas of our lives. This includes: (i) health, as biofouling on medical device leads to hospital-acquired infections, (ii) water, since the accumulation of organisms on membranes and pipes in desalination systems harms the function of the system, and (iii) energy, due to the heavy load of the organic layer that accumulates on marine vessels and causes a larger consumption of fuel. This paper presents an effective electrochemical approach for generating antifouling and antimicrobial surfaces. Distinct from previously reported antifouling or antimicrobial electrochemical studies, we demonstrate the formation of a hydrogen gas bubble layer through the application of a low-voltage squarewaveform pulses to the conductive surface. This electrochemically generated gas bubble layer serves as a separation barrier between the surroundings and the target surface where the adhesion of bacteria can be deterred. Our results indicate that this barrier could effectively reduce the adsorption of bacteria to the surface by 99.5%. We propose that the antimicrobial mechanism correlates with the fundamental of hydrogen evolution reaction (HER). HER leads to an arid environment that does not allow the existence of live bacteria. In addition, we show that this drought condition kills the preadhered bacteria on the surface due to water stress. This work serves as the basis for the exploration of future self-sustainable antifouling techniques such as incorporating it with photocatalytic and photoelectrochemical reactions. KEYWORDS: antifouling, antibacterial, electrochemical technique, electrolysis, gas bubbles

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INTRODUCTION Biofouling is the accumulation of unwanted biological species on a surface. It comprises is a series of processes that are initiated by colonization of bacteria leading to biofilms formation.1 It often leads to the reduction in system performance. For instance, biofouling on marine vessels increases the surface roughness leading to higher frictional drag and fuel consumption of ships. One possible solution is the incorporation or release of antimicrobial compound from the surface. However, most biocides are environmentally toxic, having a negative effect on nontarget species.2−4 Numerous antifouling methods have been attempted including surface modification through coating with chemically active compounds, mimicking natural antifouling surfaces, and engineering different surface topography.5−18 One of the most effective methods of prevention is to deter the formation of biofilms. Great efforts have been developed in preventing bacterial adhesion/growth via embedding nanoparticles, surface grafting of polymeric brushes, hydrogels, and antifouling self-assembly monolayer.19−24 One approach is to create superhydrophobic/hydrophobic surfaces by entrapment of air in micro- and nanosized pores on the surface when the surface is immersed in liquids. This solid−gas interface has the ability to © XXXX American Chemical Society

prevent microorganisms from adhering onto the surface albeit for a short period as organisms will eventually displace the gas bubbles layer.7 In the past decade, applications of electrical potential for prevention the formation of biofilms have gained much attention. Various possible mechanisms such as the electrochemical production of hydrogen peroxide, radical generation, alternating pH, temperature changes, and electroosmotic flow have been proposed.25−28 Results from the applications of high intensity [kV] electric field have also shown changes in biological membranes organization, disruptions of metabolic processes, deformations of the shape of the cell, and production of toxic substances where cells are damaged.29−34 On the contrary, low-intensity [V] electric field has the ability to override the inherent resistance of bacteria to biocides, decrease the concentration of attached bacteria, and decreased viability of bacterial cells and attachment on charged surfaces.27,28,34−40 Received: April 3, 2017 Accepted: July 12, 2017

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DOI: 10.1021/acsami.7b03761 ACS Appl. Mater. Interfaces XXXX, XXX, XXX−XXX

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ACS Applied Materials & Interfaces

Figure 1. Schematic illustration of the proposed antifouling mechanism. When the stainless-steel (SS) substrate is immersed in a medium of E. coli, a layer of air bubbles is formed on the SS substrate via electrochemical gas generation (sample on the left) and a bare SS substrate (control on the right).

Recently, Zhu et al. have reported a biocide-free antifouling method.41 The method is based on the disturbance of charge around the vicinity of the protected surface via triboelectrificationinduced oscillating electric potential.41 However, one of the drawbacks of this system is its inability to enlarge the protected area and duration. The triboelectric oscillator was limited in the charge that it provides as the protected area increases. This leads to the reduction of the electric potential variation between the electrodes. Today, most of the antifouling solutions are still facing the issues of large surface area coverage and sustainability. Here, we have successfully devised a unique method through incorporation of electrochemical reaction through application of low-voltage square-waveform pulses on the surface to create a sustainable solid−gas interface for antifouling. We show that this solution can prevent the adhesion of 99.5% bacteria on the surface. This method has also antimicrobial activity. It killed bacteria (Escherichia coli) that pre-adhered on the surface. The solid−gas interface has the ability to create a dry environment that retards the growth of bacteria. To the best of our knowledge, this is the first report on using electrochemical reaction to create a continuous gas bubble layer on a surface that prevents bacterial adhesion and growth.

MHads + H 2O + e− ↔ H 2 + M + OH− (Heyrovsky Step) −

2MHads + 2e ↔ H 2 + 2M

RESULTS AND DISCUSSION A solid−gas interface can be formed when a superhydrophobic/ hydrophobic surface is immersed in an aqueous solution.42 This interface has the ability to prevent microorganisms from adhering onto the surface.7 We hypothesized that sustaining a continuous layer of dry air bubbles by electrochemical gas generation at the substrate/medium interface will lead to effective resistance to biofouling (Figure 1). To determine the range of electrochemical reaction potential of the SS substrate in LB medium, we performed a linear cyclic voltammetry test. Generally, hydrogen evolution reaction undergoes two reaction steps on SS.43,44 When the potential is applied, the Volmer step (eq 1) is the initial adsorption of hydrogen protons on the surface. The adsorbed hydrogen will either react with the solvated hydrogen proton (Heyrovsky step, eq 2) or combined with adjacent adsorbed surface hydrogens to form the hydrogen molecule (Tafel step, eq 3).43−47 (Volmer Step)

(Tafel Step)

(3)

The resulted cyclic voltammogram (Figure 2a) shows the hydrogen evolution reaction at electric potential range below −1 V and hydrogen proton adsorption regions between −0.2 and −0.8 V, which is in accordance with previous studies on SS.44 To create a solid−gas interface on the SS surface, an electrical potential of −3 V was applied as hydrogen evolution reaction occurring < −1 V. Due to the complex mechanism of bubbles formation/detachment and displacement of gas bubbles by microorganism, a square-waveform potential pulse was maintained throughout the experiment. Gas bubbles (Figure 2b) could be visually observed on the surface of the SS substrate after applying an electric potential of −3 V for 5 s. Two experimental setups were prepared for each experiment. The first setup consisted of a SS substrate (sample) and Pt and Ag wires connected to a potentiostat. The other setup consisted of only SS substrate (control). Both substrates were immersed in a medium containing E. coli for 16 h to allow substantial biofilm formation at 37 °C. One of the SS substrates underwent the square-waveform-pulsed electrochemical treatment cycle as shown in Figure 2c. Figure 2d shows the chronoamperometry during the electrochemical treatment of the different substrates under the experimental conditions. The sample or substrate with a biofilm substrate exhibited higher current when compared to the clean substrate. We attribute this finding to the presence of E. coli on the surface which enhanced the HER performance as shown by Logan et al.48 To assess the antifouling properties of the sample, we performed the plate count method (PCM) (see Experimental Section). The graph in Figure 3a reports the normalized bacterial growth (E. coli) obtained from PCM under an electrical potential of −3 V. The plot shows a reduction of 99.5% in the bacterial growth on the sample substrate when compared to the control. Optical microscope images of the crystal violet stained bacteria on the surface in Figure 3b1,b2 display a minute amount of E. coli adhered on the sample substrate when compared to the control substrate. Figure 3b3,b4 are fluorescent microscopy images of the Live/Dead assay of the sample and control substrates, respectively. The green florescent dye indicates the presence of live

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H 2O + M + e− ↔ MHads + OH−

(2)

(1) B


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Figure 2. (a) Linear sweep cyclic voltammetry (CV) curves of SS substrate in LB at 50 mV/s scan rate. (b) Microscopy image of the SS substrate surface after applying an electric potential of −3 V for 5 s. (c) Voltage−time curves of the of the square-waveform potential pulses on the SS substrate. (d) Chronoamperometry curves of the electrochemical treatment cycle on the different sample substrates under different experimental conditions.

E. coli, whereas the red fluorescent dye represents dead E. coli. The control substrate displayed a higher intensity of green florescent dye than did the sample substrate (Figure 3b3,b4). Overall, the results from the three different experiments are in agreement with each other and are consistent. From these three experimental systems, it is evident that the gas bubbles obtained through the electrochemical reaction have successfully created a solid−gas interface, which has antifouling ability of reducing extensive the amount of E. coli adhering onto the surface. Hydrogen evolution reaction consists of two reactions. In order to ascertain that the antifouling activity is due to the solid− gas interface, we conducted a replicate experiment at −0.8 V potential. At this potential, only the Volmer step (eq 1) occurs. Hydrogen is adsorbed on the surface of the substrate when a potential is applied and therefore gas bubbles cannot visually be observed at this potential. Figure 3c shows the normalized bacterial growth obtained from PCM under an electrical potential of −0.8 V. A greater number of E. coli attached onto the surface of the sample when compared to the control. Both optical (Figure 3d1,d2) and fluorescent (Figure 3d3,d4) microscopy images from crystal violet and Live/Dead assay stained surfaces show higher amounts of E. coli (normalized bacteria growth count) adhered on the substrate when subjected to potential of −0.8 V compared to that on the control. The increase in the bacterial counts may be due to the change in the surface free energy and the increase in the concentration of positive ion in the diffuse layer. When −0.8 V is applied to the sample, hydronium ions adsorb onto the surface

and are reduced to hydrogen (Volmer step, eq 1). Once the potential is turned off, adsorbed hydrogen may desorb from the surface. This process will increase the surface free energy. Bacterial adhesion will be favored as it reduces the surface free energy.49 In addition, the increase in the concentration of positive ions in the double layer near the surface due to the application of potential might be an additional driving force to attract more E. coli toward the surface region. The generation of hydrogen peroxide for antimicrobial and bacterial detachment by low voltage electrochemical reaction has been previously reported.50 In this reported experiment, 1.5 V potential was applied on a conductive polymer membrane for a prolong time. This method reduced the number of bacteria only by 80%, and the formation of biofilm resumed when the potential was removed. We have carried out the experiment with a positive bias potential of 5 V. Under this condition, oxygen gas bubbles are likely generated. A physical bubble layer is observed. Results (Figure S1) show that there was no detectable bacteria on the sample substrate relative to that on the control. This shows the effectiveness of the gas bubble layer; however, it is not advisible to apply positive bias potential on the substrate as it will oxidized the substrate and corrosion will occur. To determine the antimicrobial ability of our approach, a biofilm was preformed on both; the sample and the control. Both substrates were immersed in the E. coli inoculum and incubated at 37 °C for 16 h. The substrates were washed three times with 2% (v/v) LB/PBS solutions to remove excess E. coli which were not adhered onto the surface. The substrates were reimmersed in C


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Figure 3. Normalized bacteria growth (E. coli) (%) obtained from plate count methods (PCM) on control substrate (without potential) and sample substrate (with potential) immersed for 16 h: (a) bare SS substrate @ −3 V) in E. coli inoculum [n = 9; p = 0.0003], (c) bare SS substrate @ −0.8 V in E. coli inoculum [n = 9; p = 0.03], (e) biofilm grown SS substrate @ −3 V in 2% (v/v) LB/PBS medium (n = 9; p = 0.0001). Optical microscopy image (100×) of crystal violet stained SS control substrate (without potential) immersed for 16 h in (b1). (d1) E. coli inoculum; (f1) 2% (v/v) LB/PBS medium and sample substrate (with potential); (b2) bare SS substrate @ −3 V in E. coli inoculum; (d2) bare SS substrate @ −0.8 V in E. coli inoculum; (f2) biofilm grown SS substrate @ −3 V in 2% (v/v) LB/PBS medium. Fluorescence microscopy image (100×) of Live/Dead assay stained SS control substrate (without potential) immersed for 16 h (b3) in (d3) E. coli inoculum; (f3) 2% (v/v) LB/PBS medium and sample substrate (with potential); (b4) bare SS substrate @ −3 V in E. coli inoculum; (d4) bare SS substrate @-0.8 V in E. coli inoculum; (f4) biofilm grown SS substrate @ −3 V in 2% (v/v) LB/PBS medium. In fluorescence microscopy images: red indicates dead E. coli; green indicates live E. coli.

2% (v/v) LB/PBS solutions for 16 h at 37 °C. The sample underwent square-waveform-pulsed potential (−3 V) electrochemical treatment as described above. PCM was performed after serial dilution on the scrapped E. coli biofilm on the substrates. The plot in Figure 3e shows the results of the normalized

bacteria growth (E. coli) (%) obtained from PCM under an electrical potential of −3 V. No bacteria were detectable on the sample substrate when compared to those on the control. Optical microscope images of the crystal violet stained surfaces in Figure 3f1,f2 shows that numerous E. coli adhered on both the D


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ACS Applied Materials & Interfaces sample and the control. There was much lesser E. coli attached on the sample as compared to the control. This is consistent with previous reports on detachment of E. coli when an electric potential is applied.27,40,50 The degree of detachment is not as significant as reported previously. This might be due to the short duration of the potential pulses applied in our experiment. Fluorescence microscopy images (Figure 3f3,f4) using Live/ Dead assay show red fluorescent for the sample substrate and green fluorescence for the control. This indicates that the E. coli which adhered on the sample substrate were dead, whereas E. coli which adhered on the control were alive. These results are in agreement with the data obtained from the PCM. E. coli that preadhered on the sample either detached from the surface or died leading to no bacterial growth after the electrochemical treatment. Previous electrochemical studies investigating microbial attachment and antimicrobial activity to surfaces ascribed the differences in attachment behavior prior to electrostatic repulsive forces and hydrogen peroxide effect.27,40,50 In our experimental design and approach, electrostatic interactions between the surface and bacteria were minimized since short potential pulses were applied. Hydrogen peroxide generation does occur in our working potential. It is assumed that these mechanisms can be ruled out in our system. We have deduced a possible explanation for the antimicrobial effect in our experiment. Hydrogen evolution reaction occurs when potential of −3 V was applied to the substrate. Hydrogen first adsorbs on the surface (Volmer step,eq 1) followed by the formation of hydrogen gas molecules (Heyrovsky or Tafel Step).51 The hydrogen gas nucleates into gas bubbles. The bubbles grow larger due to coalescence of smaller bubbles in the vicinity. Bubbles which exceed surface tensions forces are detached from the surface.52,53 Those gas bubbles that remain on the surface serve as voids which create an effective separation layer between the surface and the surrounding. These voids are relatively dry due to the low solubility of water in hydrogen. The E. coli adhered on the surface are therefore encapsulated within the void, which creates an arid environment where the growth of E. coli is eliminated.54 This work provides an effective antifouling and antimicrobial solution. To make this technique accessible to a large variety of applications, we repeated the experiments with a nickel foil. The results from this experiment (Figure S2a) show a reduction of 95% in the bacterial count as compared to that of the control. This proves the effectiveness of this technique and the fact that it is applicable to other conductive surfaces. We propose two new mechanisms for antifouling and antimicrobial effects. It correlates with the fundamental of HER with a solid−gas interface for antifouling and dry environment for antimicrobial effect. This method is not limited by the requirement of electric potential. It could be used by solar panels in tropical environment where it is self-sustainable. It could also be applied to nonconducting surfaces via coating of photocatalytic catalysts where photocatalytic/photoelectrochemical reaction occurs when the surface is exposed to light.

surface and the medium. The antimicrobial function has an effectiveness where there was no bacteria count obtained from the preadhered E. coli on the substrate. This antimicrobial function uses the confinement of bacteria on the surface in a dry environment where growth of E. coli was eliminated. This study also serves as a new viable approach for self-sustainable antifouling and antimicrobial solution due to the renewable gas layer generation with pulse potential applications.

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EXPERIMENTAL SECTION

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ASSOCIATED CONTENT

Bacterial Growth: E. coli. Starter (ATCC#25922) was prepared by incubating a colony of E. coli in 15 mL of LB broth (Merck Millpores) shaking at 120 rpm at 37 °C for 6 h. The E. coli starter was then diluted in LB broth to achieve 5 × 107 cells/mL by UV−vis absorbance reading of 0.3 at a wavelength of 600 nm.55 UV−vis absorption was measured by 1650PC UV−vis spectrophotometer (Shimadzu, Kyoto, Japan). The LB medium served as the electrolyte for the electrochemical experiment. To access the antifouling properties on the surface, E. coli biofilms were scrapped off from the substrate using a sterilized cotton swab. Serial dilutions were performed before performing the plate count method (PCM).56 Crystal Violet Staining. The substrates were immersed in 0.2% crystal violet (Merck, Darmstadt, Germany) for 15 min. They were rinsed three times with ultrapure distilled water. The samples were dried at room temperature and placed under the optical microscope (Carl Zeiss, Axio Vision) for imaging. Live/Dead Assay Kit. QIA76 Live/Dead Double Staining assay kit (Merck Millpores) was used. Substrates were stained in accordance to the manufacturer protocols provided. Fluorescent microscopy images were obtained by fluorescence microscopy (Carl Zeiss, Axio Vision). Electrochemical Reaction. A three-electrode setup controlled by a CH Instruments-750B potentiostat was used with Ag wire as the reference and a platinum wire as counter electrode. A 316 stainless-steel (SS) sheet was used as the working electrode. Electrochemical Procedure. Electric potential (−3 and −0.8 V) was first applied for 5 s (on). It was then turned-off for a duration of 600 s (off). This on/off procedure was repeated throughout the duration of the whole experiment. All potentials applied were referenced to Ag wire. S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acsami.7b03761. Normalized bacteria growth (E. coli) results for experiment conducted with a positive bias potential of 5 V; results for the experiment conducted with nickel foil (PDF)

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AUTHOR INFORMATION

Corresponding Authors

*E-mail: [email protected]. *E-mail: [email protected]. *E-mail: [email protected]. ORCID

Zhichuan J. Xu: 0000-0001-7746-5920 Pooi See Lee: 0000-0003-1383-1623 Meital Reches: 0000-0001-5652-9868

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CONCLUSION In this paper, we have successfully devised a new approach with dual antifouling and antimicrobial functionalities. It has an antifouling performance that prevents 99.5% of E. coli from adhering onto the surface through application of short square-waveform pulses to induce water reduction. Gas bubbles that remain on the surface serve as an effective barrier that separates the substrate

Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This work was supported by the Singapore National Research Foundation under its Campus for Research Excellence and E


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Technological Enterprise (CREATE) programme (NTU-HUJ CREATE Programme), the Israeli Water Authority, and the Rosetrees Trust.

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