Cu₂O@Co/N-doped carbon as antibacterial catalysts for oxygen reduction in microbial fuel cells

Abstract

Biofouling and sluggish kinetics on the cathode surface reduce the power generation of microbial fuel cells (MFCs). In this work, ZIF-derived Cu₂O@Co/N-doped carbon (Cu₂O@Co/NC) was used as an antibacterial oxygen reduction reaction (ORR) catalyst for MFCs. As an antibacterial agent on the cathode surface, Cu₂O can inhibit the excessive growth of biofilms, facilitate the diffusion of OH⁻ ions, and reduce the electron transfer resistance in ORR. The interaction between Cu₂O and Co/NC was studied by charge density analysis. Charge redistribution can promote the adsorption of O₂ molecules, resulting in enhanced ORR activity. The Cu₂O@Co/NC cathode demonstrated superior ORR activities due to a half-wave potential of 0.80 V and an onset potential of 0.89 V versus RHE. The corresponding MFCs gained a maximum power density of 1100 mW m⁻² after 450 h of operation, which was higher than that of Co/NC (739 mW m⁻²) and similar to that of commercial Pt/C (1067 mW m⁻²). Our work provides a strategy to achieve high power density of MFCs by combining the advantages of Cu₂O and Co/NC catalysts.

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Environmental significance

Biological sludge easily blocks the pores of the catalytic layer on the surface of cathode electrodes after long-term operation of microbial fuel cells. Bacterial contamination increases the charge transport impedance and hinders ion diffusion, reducing the power generation and wastewater degradation of the devices. We report ZIF-derived Cu₂O@Co/NC as an antibacterial oxygen reduction catalyst for antibacterial effect and efficient power generation in microbial fuel cells. Cu₂O as an antibacterial component can inhibit the excessive growth of biofilms on the surface of the cathode catalyst, thereby maintaining the diffusion channel of OH⁻ ions and reducing the electron transfer resistance. The Cu₂O@Co/NC cathode can ensure low overpotentials due to efficient ion diffusion and fast electron transfer, including a higher half-wave potential, onset potential and lower Tafel slope. The antibacterial mechanisms might include the induction of oxidative stress, prevention of cell replication and disruption of cell membrane integrity.

Introduction

Microbial fuel cells (MFCs) convert chemical energy into electricity via the degradation of organics using electroactive microorganisms to realize resource regeneration.^1,2 MFCs, as bioelectrochemical hybrid systems, have been used in electricity generation, wastewater treatment, biohydrogen generation and biosensing.³ Oxygen reduction reaction (ORR) processes slow down due to the effect of cathode biofouling, further limiting the power generation of MFCs. In general, the colonization of biofilms blocks the channels of the cathode layer, thereby increasing the charge transfer resistance and hampering the diffusion of ions. The aerobic-respiring bacteria consume dissolved oxygen, resulting in the lowering of dissolved oxygen concentrations and the reduction of reaction kinetics as the biofilm thickness increased.^4–7 Therefore, the hazard of biofouling prevents the MFCs from sustaining high power output for long periods of operation. Some methods such as physical cleaning, chemical cleaning, electric field and surface modification methods are used to mitigate biofouling.⁸ However, physical scraping requires regular treatment and chemical washing easily causes the catalyst layer to fall off. The mitigating biofouling methods based on electric fields are usually limited by the complexity of energy consumption and operating environments. Therefore, we hope to prevent biofouling by the antibacterial treatment of the cathode surface.

Cu₂O is widely used as an antifouling coating to prevent biofouling on marine facilities owing to its high efficiency for antibacterial effects.^9,10 The sterilization principle is based on the release of copper ions and the production of reactive oxygen species to inhibit bacterial growth.¹¹ Although Cu₂O can be used as a biocide to reduce the population of fouling organisms on the cathode surface, the low ORR activity of Cu₂O makes it unsuitable for use as an ORR catalyst alone. Cobalt-based zeolitic imidazole framework (ZIF) catalysts have been considered as star electrocatalysts due to their large specific surface area, uniform nitrogen doping and adjustable structure.^12,13 In particular, ZIF-derived Co-based catalysts possess Co–N active sites for ORR.¹⁴ If Cu₂O and Co/NC are combined, it would be possible to design and prepare highly active ORR catalysts that inhibit the growth of biofilms.

In this work, ZIF-derived Cu₂O@Co/N-doped carbon (Cu₂O@Co/NC) was synthesized to provide Co–N active sites for ORR. Fast mass transport channels of Co/NC resulted from porous carbonized nanocubes. Electron distribution was studied using density functional theory (DFT) calculations to understand the effects of interface. The ORR activity can be estimated by half-wave potential, onset potential and Tafel slope. The antibacterial effect reduced the accumulation of biofilms to facilitate the electron transfer and OH⁻ ion diffusion transport of MFCs. The polarization and power density curves of MFCs were further used to verify the performance of Cu₂O@Co/NC as an antibacterial ORR catalyst.

Experimental section

Computational methods

Spin-polarized DFT calculations were performed using the Vienna Ab initio Simulation Package (VASP). The generalized gradient approximation (GGA) with the Perdew–Burke–Ernzerhof (PBE) functional was implemented to evaluate electron exchange correlation and projector augmented wave potentials were used to describe ion-electron interactions.¹⁵ The cut-off energy was set to 500 eV and the convergence threshold was conducted as 10⁻⁶ eV and 0.02 eV Å⁻¹ for energy and force, respectively. The interaction between neighboring slabs was avoided with a vacuum space of 16 Å. The k-point mesh was selected as 3 × 2 × 1 in the structure optimization using the Monkhorst–Pack method. The adsorption energy (ΔE) is defined as follows:

ΔE = E_T − E_O2 (1)

where E_T is the initial energy of substrates and E_O2 is the energy of O₂.

Materials

2-Methylimidazole, cetyltrimethylammonium bromide (CTAB), cobalt nitrate hexahydrate (Co(NO₃)₂·6H₂O), cupric sulphate pentahydrate (CuSO₄·5H₂O), L-ascorbic acid (AA) and sodium hydroxide (NaOH) were used in the experiments. Carbon cloth (WOS1009) was gained from Carbon Energy Technology Ltd of Taiwan. Electrolytic cells were obtained from Lambert Scientific Instrument Ltd (Beijing, China).

Synthesis

Synthesis of Co/NC: first, 10 mg of CTAB was dissolved in 20 mL ultrapure water with stirring. Then, 0.58 g Co(NO₃)₂·6H₂O was added into this solution with stirring to form a pink solution. The pink solution was poured into 2-methylimidazole (9.08 g)/ultrapure water (140 mL) with constant stirring for 30 min at ambient temperature to obtain a purple precipitate. The purple precipitate was centrifuged and washed six times with ethanol and then dried in a vacuum chamber at 60 °C overnight to obtain ZIF-67. Finally, ZIF-67 was annealed at 550 °C under a N₂ atmosphere for 2 h to obtain Co/NC.

Synthesis of Cu₂O@Co/NC: Cu₂O@Co/NC was prepared by a liquid-phase reduction method (Fig. S1†). First, 0.20 g Co/NC was mixed with 50 mL ultrapure water and dispersed under ultrasonication for 10 min. Then, 0.32 g NaOH was dissolved into 50 mL ultrapure water and mixed with the above-mentioned solution with stirring to form a homogeneous solution. Next, 1.00 g CuSO₄·5H₂O was introduced to this solution to form Cu(OH)₂ precipitates. Finally, 0.70 g AA was added and stirred for 1 h for the reduction of Cu(OH)₂ to Cu₂O. The precipitates were washed with ethanol followed by vacuum-drying at 60 °C overnight.

Electrochemical measurements

Electrochemical tests were conducted using a CHI760E workstation in a three-electrode system, in which a glassy carbon electrode was used as the working electrode, a Pt foil as the counter electrode and Hg/HgO as the reference electrode, respectively. All of potentials in electrochemical tests were converted to the reversible hydrogen electrode (RHE) according to the following equation:

E_RHE = E_Hg/HgO + 0.059 pH + 0.098 (2)

For the rotating disk electrode (RDE), the electron transfer number was calculated from the Koutecky–Levich (K–L) equation as follows:¹⁶

B = 0.62nFC₀D₀^2/3V^−1/6 (4)

where j, j_L, and j_K are the measured current density, diffusion limited current density and kinetic current density, respectively, w is the angular velocity of rotation, n represents the electron transfer number, F is the Faradic constant (96 485 C mol⁻¹), C₀ is the bulk concentration of O₂ (1.2 × 10⁻⁶ mol cm⁻³), D₀ is the diffusion coefficient of O₂ in solutions (1.9 × 10⁻⁵ cm² s⁻¹), and V is the kinematic viscosity (0.01 cm² s⁻¹).

Antibacterial activity

Escherichia coli (ATCC 25922) was selected as the antibacterial model to conduct in vitro antibacterial tests. A LB liquid medium and a solid medium were prepared in advance for sterilization. The bacterial solution was diluted to 106 CFU mL⁻¹ with a sterile PBS solution, and then 0.1 mL dilute bacterial solution was inoculated on the LB solid medium. Following this, 20 μL catalyst solution with a concentration of 0.1 g mL⁻¹ was dropped on a 8 mm filter paper affixed on the medium. The blank control group was dropped the same volume of sterile water. The culture dish was placed in a 37 °C incubator for 24 h. The antibacterial activity of the catalyst was characterized by measuring the diameter of the inhibition circle. The tests were repeated three times to ensure the accuracy of the results.

Assembly and operation of MFCs

The air cathode was composed of a catalyst layer, a collector layer (100 mesh titanium mesh) and a gas diffusion layer. First, 90 mg acetylene black, 150 μL 60% polytetrafluoroethylene (PTFE) and 3 mL ethanol were sonicated for 30 min followed by coating on one side of a titanium mesh (3 cm × 3 cm) uniformly. The gas diffusion layer was obtained by heating it to 370 °C for 20 min, which contributed to the diffusion of O₂. Then, 36 mg catalyst, 30 mg acetylene black, 50 μL 10% PTFE and 2 mL ethanol were sonicated for 30 min to prepare a catalyst ink. Another side of the titanium mesh was coated with 4 mg cm⁻² catalyst as the catalyst layer for subsequent assembly. The anode was made of carbon cloth (2 cm × 3 cm) after pretreatment. The bacterial solution for inoculation was derived from the long-term stable operating dual-chamber MFC. MFCs were operated with an external resistance of 1000 Ω at a constant temperature of 30 °C. The anode electrolyte was renewed when the output voltage dropped below 50 mV. The electrolyte contained CH₃COONa (0.5 g L⁻¹), NaH₂PO₄·2H₂O (2.76 g L⁻¹), Na₂HPO₄·12H₂O (11.4 g L⁻¹), NH₄Cl (0.3 g L⁻¹) and KCl (1.3 g L⁻¹). The output voltage was recorded every 5 min using a data acquisition instrument (USB-5936, Aertai, China). Power density curves and polarization curves were measured by varying the external resistors.

Results and discussion

DFT calculations

DFT calculations were carried out to investigate the effects of Cu₂O on the ORR activity of Co/NC. The Co/NC model consisted of 6 Co,7 N, and 53 C atoms. The Cu₂O@Co/NC model was established based on the Co/NC model by adding Cu₂O (48 Cu, 24 O atoms) (Fig. S2a,†1a). The effects of Cu₂O on the interface charge were described by the charge density difference. Interfacial interaction induced by Cu₂O can be observed from electron accumulation and depletion (Fig. 1b). Charge redistribution was induced by strong interfacial interaction to activate catalyst activity. Interfacial charge distribution between Cu₂O and Co/NC was further clarified by the Bader charge analysis quantitatively (Fig. S2b,†1c). Co atoms lost more electrons (0.02–0.04e) and N atoms obtained less electrons (0.09–0.13e) owing to the interaction of Cu₂O and Co/NC. The charge distribution around Co atoms presented a “claw” shape in Fig. S2c.† Losing more electrons of Co atoms indicated that the valence state of Co atoms on Cu₂O@Co/NC was more positive than Co/NC. Oxygen adsorption energy was used to evaluate the O₂ adsorption capacity of catalysts. The lower O₂ adsorption energy of Cu₂O@Co/NC (−1.48 eV) than that of Co/NC (−1.29 eV) implied the stronger oxygen adsorption capacity of Cu₂O@Co/NC (Fig. 1d). Compared with Co/NC, Cu₂O@Co/NC had an affinity towards O₂ recognized as essential to the ORR process. Projected density of states (PDOS) and density of states (DOS) were used to analyze the electronic structure changes of the models. The calculated d-band center of Co for Cu₂O@Co/NC (−1.70 eV) was shifted positively than Co/NC (−1.85 eV) (Fig. 1e). The closer the d-band center was to Fermi level, the stronger the binding force between the adsorbate and the substrate.¹⁷ The optimized d-band center by introducing Cu₂O enhanced the intrinsic ORR catalytic activity. The increase in electronic states near the Fermi level of Cu₂O@Co/NC was beneficial to promote electron transfer (Fig. 1f). Hence, the enhanced oxygen absorption and electron transfer accelerated the ORR process.

Fig. 1 (a) Cu₂O@Co/NC model. (b) Charge density difference of Cu₂O@Co/NC, the yellow and cyan regions indicate electron accumulation and depletion. (c) Calculated charge of atoms of Cu₂O@Co/NC. (d) O₂ adsorption energy of Co/NC and Cu₂O@Co/NC. (e) PDOS of the Co 3d orbital in Co/NC and Cu₂O@Co/NC. (f) Comparative DOS plots of Cu₂O, Co/NC and Cu₂O@Co/NC.

Characterization

ZIF-67 had a uniform cube shape with a smooth surface (Fig. S3a†). Co/NC maintained the same nanocube-like morphology with a porous and rough surface (Fig. 2a, S3b†). The porous N-doped carbon framework provided accessible active sites and pathways for mass transport. Co nanoparticles were evenly embedded in a N-doped carbon framework. High-resolution transmission electron microscopy (HRTEM) further revealed that the thickness of the carbon layer was about 5 nm (Fig. 2b). The lattice spacing of 0.204 nm was indexed to the (111) plane of metallic Co from the inset image. The carbon layer can avoid the aggregation of Co nanoparticles and further control the size of Co nanoparticles. The interconnected carbon can form a conductive carbon network to promote fast electron transfer. The Co/NC nanocubes were coated by dispersing Cu₂O clusters to protect Co/NC from biofouling (Fig. 2c and d). Meanwhile, the electronic states of Co/NC were modulated by dispersing Cu₂O, optimizing O₂ adsorption energy. Cu₂O and Co/NC were tightly connected by a N-doped carbon backbone (Fig. 2e and f). A distinct interface boundary can be observed between Co/NC and Cu₂O. The identified lattice spacing of 0.243 nm could be attributed to Cu₂O (111) in the HRTEM image. The corresponding elemental analysis showed the distribution of Co, Cu, N and C elements (Fig. 2g). N-doped carbon was distributed uniformly, while Co and Cu₂O were distributed inside and outside, respectively. C and N elements distributed uniformly in the N-doped carbon cubes. Co nanoparticles embedded in the N-doped carbon backbone and concentrated at the center of N-doped carbon cubes. Cu elements coated on the surface of Co/NC.

Fig. 2 (a) TEM and (b) HRTEM images of Co/NC. (c) SEM image of Cu₂O@Co/NC. (d–f) TEM and HRTEM images of Cu₂O@Co/NC. (g) Elemental mapping images of Cu₂O@Co/NC.

The characteristic diffraction peaks of as-synthesized ZIF-67 are completely consistent with those of simulated ZIF-67 (Fig. S4†). All the samples presented broad diffraction peaks at 21.7° and 22.8° due to agraphitic carbon (Fig. 3a). The diffraction peaks at 44.4° and 51.6° were indexed to the (111) and (200) crystal faces of metallic Co (JCPDS No. 01-1255), respectively. The peaks at 36.4°, 42.3°, 61.5°, and 73.5° were assigned to the (111), (200), (220) and (311) lattice planes of Cu₂O (JCPDS No. 05-0667). The peak of Cu₂O (111) showed stronger intensity than that of other planes and the Cu₂O (111) crystal planes provided dominant active sites for ORR, in accordance with the previous reports in the literature.¹⁸ Two obvious peaks at the D band (1370 cm⁻¹) and G band (1590 cm⁻¹) presented the presence of defects and graphitization (Fig. 3b). Cu₂O@Co/NC obtained a balance between carbon defects and graphitization, because the relative intensity of D band to G band (I_D/I_G) value was 1.12.

Fig. 3 (a) XRD patterns of Co/NC and Cu₂O@Co/NC. (b) Raman spectra of Co/NC and Cu₂O@Co/NC. (c) XPS full scan of Cu₂O@Co/NC, (d) Co 2p, (e) Cu 2p, (f) N 1s.

The XPS survey spectrum of Cu₂O@Co/NC demonstrated the presence of C, N, O, Co and Cu elements (Fig. 3c). C 1s can be classified into four different peaks corresponding to C–C/C=C, C–N/C=N, C–O and C=O. The emergence of peaks corresponding to C–N/C=N verified that nitrogen was doped into the carbon matrix. A binding energy of 530.8 eV of Cu₂O@Co/NC could be ascribed to Cu–O, suggesting the presence of Cu₂O (Fig. S5†). The Co 2p spectrum can be deconvoluted to Co 2p_3/2, Co 2p_1/2 and two satellite peaks (Fig. 3d). The characteristic peaks of Co²⁺ (781.0, 796.7 eV), Co⁰ (778.6, 793.9 eV) and satellite peaks (785.8802.8 eV) were identified in the Co 2p spectrum of Cu₂O@Co/NC, while Co²⁺ (780.6, 796.5 eV), Co⁰ (778.3, 793.8 eV) and satellite peaks (784.9, 802.1 eV) can be identified for Co/NC. The presence of Co²⁺ was attributed to the formation of Co–N coordination inherited from ZIF-67, which was ORR active sites.¹⁹ Some of Co²⁺ ions were reduced by the reaction with carbon to form metallic Co. A positive shift in the peak of Co²⁺ revealed that Cu₂O may interact with Co/NC by electron redistribution. The positive shift suggested more electron depletion and higher valence state of Co atoms, which was consistent with DFT calculations. For the Cu 2p region, two peaks located at 932.8 and 952.7 eV could be ascribed to Cu⁺ in agreement with XRD (Fig. 3e). Binding energies of 935.0 and 954.9 eV were ascribed to Cu²⁺, which was accredited to the partial oxidation of Cu₂O.²⁰ The Cu⁺-to-Cu²⁺ ratio was 1.8, suggesting that Cu⁺ was dominant. Two satellite peaks were observed at 943.6 and 963.3 eV. The high resolution of N 1 s can be deconvoluted into four characteristic peaks with four nitrogen species: pyridinic-N (398.6 eV), Co-N (399.1 eV), pyrrolic-N (399.8 eV) and graphitic-N (401.1 eV) (Fig. 3f). The synergistic effect of nitrogen species can enhance the ORR activity.

Electrochemical activity

All samples exhibited obvious oxygen reduction peaks in O₂-saturated 0.1 M KOH, indicating their oxygen reduction activity (Fig. 4a). The comparison of Cu₂O@Co/NC cyclic voltammetry (CV) curves in N₂- and O₂-saturated 0.1 M KOH can clearly distinguish the position of the oxygen reduction peak (Fig. S6a†). The mass ratio of Co/NC and CuSO₄ was 1 : 5, and the sample exhibited the best ORR activity (Fig. S6b†). Co/NC, Cu₂O@Co/NC and Pt/C displayed oxygen reduction peaks at 0.79, 0.80 and 0.87 V and the corresponding peak current densities were 2.35, 2.75 and 3.59 mA cm⁻², respectively. The oxygen reduction peak of Cu₂O@Co/NC was more positive than that of Co/NC, and the electrochemical active area of the CV curve was larger than that of Co/NC. The electrochemical active area was increased due to the presence of Cu₂O. The peak current density of Cu₂O@Co/NC was higher than that of Co/NC, manifesting that the reaction rate of ORR was improved. Linear sweep voltammetry (LSV) was conducted at a rotation speed of 1600 rpm in O₂-saturated 0.1 M KOH (Fig. 4b). Cu₂O@Co/NC showed a more positive onset potential (E_onset, at 0.2 mA cm⁻²) of 0.89 V, and a half-wave potential (E_1/2) of 0.80 V compared with Co/NC (E_onset = 0.82 V, E_1/2 = 0.69 V), which was smaller than 20% Pt/C (E_onset = 1.00 V, E_1/2 = 0.86 V).²¹ Tafel plots were used to reflect ORR kinetics within the mixed kinetic-diffusion controlled region (Fig. 4c).²² The small Tafel slope value indicated fast kinetics for ORR. Cu₂O@Co/NC displayed a lower Tafel slope of 62.99 mV dec⁻¹, whereas Co/NC showed Tafel slopes of 69.94 mV dec⁻¹. The comparison of various ORR catalysts activities is presented in Table S2† and the half-wave potentials of ORR catalysts are presented in Fig. S10.† Cu₂O@Co/NC demonstrated superior ORR activities.^23–28 The oxygen reduction pathway was obtained by different rotation rates (Fig. S7a†). According to the K–L equation, the calculated electron transfer number was 3.4, suggesting that two- and four-electron pathways coexisted and ORR proceeded predominantly via a four-electron reaction pathway (Fig. S7b†). The electrochemical impedance spectrum (EIS) curve of Cu₂O@Co/NC showed a smaller semicircle than that of Co/NC, implying a smaller charge transfer resistance (Fig. 4d, Table S1†). Cu₂O can contribute electrons to oxygen and obtain electrons from the N-doped carbon backbone, accelerating the electron transfer and reducing the charge transfer resistance. The fast ORR process was linked with the optimized binding energy of oxygen resulting from charge redistribution. The tolerance to methanol crossover effects of Cu₂O@Co/NC was obtained by adding 3 M CH₃OH into electrolytes (Fig. 4e). The CV curve of Cu₂O@Co/NC retained the same shape and showed an obvious oxygen reduction peak, while the CV curve of Pt/C completely deformed. The results revealed that Cu₂O@Co/NC had better poison tolerance than that of Pt/C, which played a pivotal role for MFCs. The CV scans of catalysts in the non-Faraday region with different sweep speeds can reflect double-layer capacitance (C_dl) (Fig. S8†). Electrochemical surface areas (ECSAs) were evaluated with C_dl in the potential range without ORR occurring (Fig. 4f). The calculated C_dl value of Cu₂O@Co/NC (15.17 mF cm⁻²) was higher than that of Co/NC (7.62 mF cm⁻²), signaling that Cu₂O@Co/NC possessed more active sites.

Fig. 4 (a) CV curves in O₂-saturated 0.1 M KOH. (b) LSV curves of catalysts in 0.1 M KOH at a rotation speed of 1600 rpm. (c) Tafel plots of catalysts (d) Nyquist curves of Cu₂O@Co/NC, Co/NC and Pt/C. (e) Resistance to poisoning of Cu₂O@Co/NC and 20 wt% Pt/C. (f) Double-layer capacity of the catalysts.

Antibacterial activity

The performance of MFCs is greatly affected by biofouling on the cathode surface due to the increasing internal resistance and impeding mass transport. Cathodes with antibacterial properties can effectively inhibit the formation of biofilms. The inhibition zone method was used to assess the antibacterial activity of cathode catalysts. The bacteriostatic ring diameter of Cu₂O@Co/NC was about 2 mm, while Co/NC did not show any obvious bacteriostatic ring under the same condition (Fig. 5). Cu₂O@Co/NC exhibited good potential to inhibit the formation of cathode biofilms due to the antibacterial effect of Cu₂O.

Fig. 5 Photographs of Escherichia coli (ATCC25922) cultured on a solid medium with 20 μL of 0.1 g mL⁻¹ Cu₂O@Co/NC (a) and Co/NC (b).

Performances of MFCs

The output voltage of Cu₂O@Co/NC was 0.43 V, which was higher than that of Co/NC and comparable to commercial 20 wt% Pt/C (Fig. 6a). The output voltage of Pt/C was highest in the first cycle corresponding to the oxygen reduction activity among the catalysts. The maximum output voltage of Pt/C decreased from 0.46 to 0.42 V after four cycles, while Cu₂O@Co/NC remained stable at about 0.43 V. The voltage of Pt/C dropped rapidly in view of poor poison resistance and inactivation of the Pt/C catalyst. The thicker biofilm formed on the cathode of Co/NC after 450 h operation proved that Cu₂O@Co/NC can inhibit the excessive growth of biofilms (Fig. 6b). The power density and polarization data were obtained when the output voltage was stable after 450 h of operation. The maximum power density observed with Cu₂O@Co/NC was 1100 mW m⁻² at a high current density of 4.46 A m⁻², compared to that of Co/NC (739 mW m⁻²) and Pt/C (1067 mW m⁻²) (Fig. 6c). The maximum power density of Cu₂O@Co/NC was noteworthy compared to those of reported catalysts based on metal carbon material (Table S3†). When the power density reached the maximum, the external resistance was equal to the internal resistance of MFCs. The internal resistance of Cu₂O@Co/NC (280 Ω) was lower than that of Co/NC (440 Ω) and Pt/C (300 Ω). The voltages of Cu₂O@Co/NC, Pt/C and Co/NC decreased with the increase in current density (Fig. 6d). The polarization curves of Cu₂O@Co/NC and Pt/C exhibited similar trends, implying similar electrode catalysis processes. The voltage decreased rapidly at a current density of 2.8 A m⁻² for Co/NC. The voltage decrease was attributed to the internal resistance and hampered OH⁻ diffusion, which was caused by the growth of biofilms on the cathode surface. The open circuit voltage of Cu₂O@Co/NC was the largest. Cu₂O@Co/NC with a high potential and stable power generation benefitted from the high oxygen reduction activity and efficient antifouling property. Cu₂O was oxidized to CuO by O₂, and CuO was reduced to Cu₂O by obtaining electrons in the solution to form a redox cycle, which facilitated electron transfer.

Fig. 6 (a) Output voltages. (b) Biofilm on the cathode surface after 450 h of operation. (c) Power density of the MFCs. (d) Polarization curves of the MFCs.

The mechanisms of bacterial inhibition are proposed as follows: (1) the catalyst can produce reactive oxygen species (O₂⁻˙, OH⁻˙, and H₂O₂) to cause oxidative stress via a Fenton-like reaction, (2) the catalyst may prevent cell replication by binding with DNA or specific proteins and (3) positively charged Cu species can contact with negatively charged groups to destroy membrane integrity and disrupt cell functions.^9,29,30 These mechanisms could help understand the pathways for the contact killing of bacteria by antibacterial catalysts.

Conclusions

In summary, the efficient and stable operation of MFCs attributed to the high efficiency of ORR process. The high ORR activity stemmed from strengthening O₂ adsorption of Cu₂O@Co/NC induced by charge redistribution. Cu₂O@Co/NC showed enhanced half-wave potential, onset potential and low Tafel slope. Cu₂O can effectively inhibit the excessive growth of biofilms, promoting electron transfer and OH⁻ ion diffusion transport in MFCs. Effective electron transfer and OH⁻ ion diffusion transport decreased internal resistance and concentration difference. The possible antibacterial mechanisms of Cu₂O@Co/NC included oxidative stress, prevention of replication and destruction of the membrane integrity of bacteria. Cu₂O@Co/NC as an antibacterial ORR catalyst exhibited a low overpotential and a high power density in MFCs. This work provides a synthetic guidance to design and prepare cathode ORR catalysts with high efficiency and practicality.

Author contributions

All authors have given approval to the final version of the manuscript.

Conflicts of interest

There are no conflicts to declare.

Acknowledgements

This work was financially supported by the Key R&D Program of Ministry of Science and Technology of China (2018YFC1803100), Youth Project of Science & Technology Research Program of Chongqing Education Commission of China (KJQN201901208). We also thank the Big Data Center of Southeast University for providing the facility support on the numerical calculations.

Notes and references

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Footnotes

† Electronic supplementary information (ESI) available. See DOI: https://doi.org/10.1039/d2en00980c

‡ These authors contributed equally to this work.

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