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«Janus»-like Cu-Fe bimetallic nanoparticles with high antibacterial activity
Materials Letters 242 (2019) 187–190
Contents lists available at ScienceDirect
Materials Letters journal homepage: www.elsevier.com/locate/mlblue
«Janus»-like Cu-Fe bimetallic nanoparticles with high antibacterial activity O.V. Bakina ⇑, E.A. Glazkova, N.V. Svarovskaya, N.G. Rodkevich, M.I. Lerner Institute of Strength Physics and Materials Sciences of Siberian Branch of Russian Academy of Sciences, Russian Federation
a r t i c l e
i n f o
Article history: Received 4 December 2018 Received in revised form 16 January 2019 Accepted 18 January 2019 Available online 24 January 2019 Keywords: Bimetallic nanoparticles Electric explosion of wires «Janus»-like nanoparticles Antibacterial activity
a b s t r a c t The search of new efficient antibacterial agents for biomedical applications is subject of researchers special attention. Bimetallic nanoparticles containing biologically active metals are prospective antibacterial agents. The «Janus»-like Cu/Fe nanoparticles prepared by electrical explosive of wires were found to exhibit high antibacterial activity comparable with that of Ag nanoparticles and exceed the antibacterial activity of Fe and Cu monometallic nanoparticles and their mixture. MIC values of bimetallic Cu/Fe particles are 3.91–250 mg/ml. This strong antibacterial activity is due to the synergistic bactericidal Cu2+ and Fe3+ ions released from Cu/Fe bimetallic nanoparticles. Cu/Fe nanoparticles are a promising material for antibacterial protection technologies and for fighting drug-resistant bacterial strains. Ó 2019 Elsevier B.V. All rights reserved.
1. Introduction Bimetallic nanoparticles (BNPs) including those obtained from immiscible metals are of great interest today. The reason of the interest is that BNPs exhibit new properties caused by the mutual influence of the particles components. There are a sufficient number of papers devoted to production of BNPs having antibacterial properties due to presence of silver as the particle core or shell. However, the use of nanoparticles containing silver is limited because of their pronounced cytotoxicity and genotoxicity [1]. While the applying of BNPs containing biologically active metals, such as Cu and Fe is prospective [2]. Cu/TiO2 colloid dispersion exhibited enhanced antibacterial activity due to the synergetic antibacterial effect of Cu and TiO2 by the generation of reactive oxygen species and the migration of copper ions [3]. Cu/Zn BNPs exhibited synergetic antibacterial effects resulted from the relatively slower release of Cu nanoparticles and faster release of Zn nanoparticles [4]. Authors [5] have shown pronounced antibacterial activity of Fe nanoparticles in conjunction with other biologically active metals against microorganisms. Authors [6] have shown that ZnO nanoparticles alloyed with Fe efficiently suppressed the growth of E. coli while being non-toxic for mammalian cells. The same effect was observed for sea urchin-like ZnO/Fe nanoparticles [7]. «Janus»-like Cu/Fe BNPs should be expected to exhibit antibacterial effect based on the ability of Cu2+ ions to ⇑ Corresponding author at: 2/4, pr. Akademicheskii, Tomsk 634021, Russian Federation. E-mail address: [email protected] (O.V. Bakina). https://doi.org/10.1016/j.matlet.2019.01.105 0167-577X/Ó 2019 Elsevier B.V. All rights reserved.
change the permeability of bacterial membranes, and Fe3+ ions to penetrate into the bacterial cell and bind with its components [8]. Here, the electrical explosion of wires (EEW) is a facile and promising method to obtain stable BNPs with different component ratios [9,10]. Hence in this work the antibacterial activities of «Janus»-like Cu/Fe BNPs against bacterial strains have been studied. The effects of varying the Cu/Fe molar ratio on the antibacterial properties have been investigated and the results are discussed in this paper. 2. Materials and methods Cu/Fe BNPs were obtained by the simultaneous electrical explosion of twisted wires (iron and copper) in argon medium [9]. The surface of the particles is covered by a thin oxide layer. The mass ratio of copper and iron in the nanoparticles was regulated by varying the wire diameters. The obtained Cu/Fe nanoparticles were characterized by transmission electron microscopy (JEOL 2000FX, JEM, Japan), X-ray diffraction (DRON-7, Russia), low-temperature nitrogen adsorption (Katakon, Russia). The concentration of Cu and Fe was measured by voltammetric stripping method (Voltammetric analyzer STA, Russia). The error in concentrations was not more 3 %. Escherichia coli ATCC 25922, Staphylococcus aureus ATCC 6538, Pseudomonas aeruginosa ATCC 9027 and MRSA ATCC 43300 were used to detect antimicrobial activity of nanoparticles. For the determination of the minimum inhibitory concentrations (MIC) values 150 ml of the Muller-Hinton broth and 20 ml of aqueous dispersions of nanoparticles were added in each well of disposable 96-well plates. The plates were then inoculated with
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the tested bacteria at a concentration of 106°CFU/ml. The MIC values were determined after 16 h of incubation at 37 °C using the Multiskan FC microplate spectrophotometer (Thermo Fisher Scientific, USA).
time. Due to surface tension, liquid copper strives to take the energetically favourable spherical shape. So the formation of a «Janus» particle occurs (Fig. 2). 3.2. Antimicrobial activity of Cu/Fe nanoparticles
3. Results and discussion 3.1. Characteristics of the Cu/Fe bimetallic nanoparticles In case of simultaneous electric explosion of iron and copper wires in the argon atmosphere the spherical 63–72 nm particles formed regardless of the wire diameter ratio. In Fig. 1 we show cake-graph together with microphotographs and X-ray diffraction patterns of the as-prepared samples. In the X-ray diffraction patterns of the BNPs (Fig. 1), the main reflexes correspond to the phases of Fe and Cu. The ratio of peak heights correlates with the mass ratio of copper and iron. According to EDAX-TEM analysis data, iron and copper are non-uniformly distributed over the volume of particles (Fig. 2). There are areas enriched with one of the components, the phase boundary between Fe and Cu domains is clearly visible. Langlois et al. observed the formation of similar structures for Ag-Cu nanoparticles [11]. The morphology of these structures can be classified as classified Janus, quasi-Janus and ball-and-cup [12]. Regardless of the components ratio the nanoparticles are formed from the liquid phase [13]. For both Cu/Fe and Cu/Pb nanoparticles [9], the following mechanism of formation is possible. The products of the explosion of Cu and Fe wires, from which Cu/Fe BNPs are formed, cool down in a non-uniform manner. The metal with a higher melting point temperature (iron) crystallizes the first and then the metal with a lower melting point temperature (copper) crystallizes while the products are cooling. The liquid copper may be staying on the surface of the iron core for some
The antibacterial activity of Cu/Fe nanoparticles is determined by a standard serial microdilution method (Fig. 2). Water suspensions of monometallic Fe and Cu nanoparticles and their mixture show significantly lower antimicrobial activity against all bacterial strains as compared with bimetallic nanoparticles. MIC values of iron or copper nanoparticles are 125–500 mg/ ml, while MIC values of bimetallic Cu/Fe particles are 3.91– 250 mg/ml (Fig. 3). Cu72/Fe28 nanoparticles suppress the growth of gram-positive bacteria more efficiently than Cu28/Fe72. The MIC value for Cu72/Fe28 was 3.91 mg/ml for S. aureus and 31.25 mg/ml for MRSA, which was two times lower than the Cu28/Fe72. However, the antibacterial activity of Cu28/Fe72 BNPs against gram-negative E. coli and P. aeruginosa is higher than that of Cu72/Fe28 and Cu50/Fe50. Copper nanoparticles are widely known as antibacterial agents. The mechanism of their action is based on the ability to be adsorbed to a bacterium cell wall leading to the destruction of the cell membrane. The destruction of cell membrane of E. coli was demonstrated by the atomic force microscopy [14]. The increased antibacterial activity of nanoparticles due to the copper loading in the samples is expected. Iron and copper are known to form a galvanic couple which leads to the dissolution of iron and the formation of Fe3+ ions. The ions kill bacteria by binding biological molecules which results in protein denaturation, DNA damage and the disruption of enzyme functions [15]. The authors [16] observed the destruction of E. coli cell membranes exposed to iron nanoparticles, Fe3+ ions binding with intracellular oxygen or hydrogen peroxide. Therefore, we assume not only
Fig. 1. (a) Cake-graphs illustrating composition based on chemical analysis, (b) TEM images, (c) XRD-analysis of Cu/Fe BNPs and (d) particle size distribution.
O.V. Bakina et al. / Materials Letters 242 (2019) 187–190
189
Fig. 2. (a) EDAX-TEM images of Cu50/Fe50 nanoparticles.
Fig. 3. Antibacterial activities by Cu/Fe, Cu and Fe nanoparticles and their mixtures and corresponding images representation of MBC of nanoparticles (250 lg/ml).
copper nanoparticles are responsible for the high antibacterial activity of Cu/Fe BNPs, but Fe3+ ions as well. The Cu/Fe BNPs under investigation exhibit antibacterial activity comparable with silver-based nanocomposites considered the most efficient antibacterial agents. For instance, according to Ref. [17] the MIC value for binary Fe3O4-Ag 20 nm nanostructures against E. coli was 120 mg/ml. For Ag/ZnO nanocomposites of less
than 100 nm in size, the MIC value against E. coli was 100 mg/ml, and 200 mg/ml against P. aeruginosa. The authors [18] have shown MIC for Ag/TiO2 nanoparticles to be 130 and 208 mg/ml, and for Ag particles (20 nm in size) to be 13 and 16 lg/ml against E. coli and S. aureus, respectively. These data indicate a significant inhibitory effect of bimetallic Cu/Fe nanoparticles whose MIC values are close to those of antibiotics against all tested microorganisms [19].
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4. Conclusion The antibacterial effect of Cu/Fe BNPs towards to four bacterial strains has been studied. The nanoparticles have been found to have high antibacterial activity against both Gram-negative and Gram-positive bacteria, including the antibiotic-resistant MRSA strain. Cu/Fe BNPs are prospective as antibacterial medications for wound treatment and expected alternative to silvercontaining nanomaterials with pronounced cytotoxicity and genotoxicity. Conflict of interest None. Acknowledgements The synthesis and characterization of nanoparticles were produced under the financial support of the Russian Science Foundation (Project No. 17-19-01319). The antimicrobial activity was financially supported by the Fundamental Research Program of the State Academies of Sciences for 2016–2020. References [1] P.V. Asha Rani, G.L.K. Mun, M.P. Hande, S. Valiyaveettil, Cytotoxicity and genotoxicity of silver nanoparticles in human cells, ACS Nano 3 (2009) 279– 290. [2] R. Parimaladevi, V. Poornima Parvathi, S. Sowmiya Lakshmi, M. Umadevi, Synergistic effects of copper and nickel bimetallic nanoparticles for enhanced bacterial inhibition, Mater. Lett. 211 (2018) 82–86. [3] S. Chen et al., Synergistic antibacterial mechanism and coating application of copper/titanium dioxide nanoparticles, Chem. Eng. J. 256 (2014) 238–246. [4] M. Ashfaq, N. Verma, S. Khan, Copper/zinc bimetal nanoparticles-dispersed carbon nanofibers: a novel potential antibiotic material, Mater. Sci. Eng. 59 (2016) 938–947.
[5] S.A. Mahdy, Q.J. Raheed, P.T. Kalaichelvan, Antimicrobial activity of zero-valent iron nanoparticles, Int. J. Modern Eng. Res. 2 (2012) 578–581. [6] K. Ravichandran et al., Effect of Fe + F doping on the antibacterial activity of ZnO powder, Ceram. Int. 41 (2015) 3390–3395. [7] J. Ma, A. Hui, J. Liu, Y. Bao, Controllable synthesis of highly efficient antimicrobial agent-Fe doped sea urchin-like ZnO nanoparticles, Mater. Lett. 158 (2015) 420–423. [8] J.H. Byeon, Rapid green assembly of antimicrobial nanobunches, Sci. Rep. 6 (2016) 27006. [9] M.I. Lerner, A.V. Pervikov, E.A. Glazkova, N.V. Svarovskaya, A.S. Lozhkomoev, S. G. Psakhie, Structures of binary metallic nanoparticles produced by electrical explosion of two wires from immiscible elements, Powder Techol. 288 (2016) 371–378. [10] O.V. Bakina, E.A. Glazkova, A.S. Lozhkomoev, M.I. Lerner, N.V. Svarovskaya, Cellulose acetate fibres surface modified with AlOOH/Cu particles: synthesis, characterization and antimicrobial activity, Cellulose 25 (2018) 4487–4497. [11] C. Langlois, Z.L. Li, J. Juan, D. Alloyeau, J. Nelayah, D. Bochicchio, R. Ferrandod, C. Ricolleaua, Transition from core–shell to Janus chemical configuration for bimetallic nanoparticles, Nanoscale 4 (2012) 3381–3388. [12] R. Ferrando, Symmetry breaking and morphological instabilities in core-shell metallic nanoparticles, J. Phys. Condens. Matter 27 (2015) 013003. [13] A. Pervikov, M. Lerner, K. Krukovskii, Structural characteristics of copper nanoparticles produced by the electric explosion of wires with different structures of metal grains, Curr. Appl. Phys. 17 (2017) 201–206. [14] U. Bogdanovic´, V. Lazic´, V. Vodnik, M. Budimir, Z. Markovic´, S. Dimitrijevic´, Copper nanoparticles with high antimicrobial activity, Mater. Lett. 128 (2014) 75–78. [15] S. Stankic, S. Suman, F. Haquel, J. Vidic, Pure and multi metal oxide nanoparticles: synthesis, antibacterial and cytotoxic properties, J. Nanobiotechnol. 14 (2016) 73. [16] C. Lee, J.Y. Kim, W.I. Lee, K.L. Nelson, J. Yoon, D.L. Sedlak, Bactericidal effect of zero-valent iron nanoparticles on Escherichia coli, Environ. Sci. Technol. 42 (2008) 4927–4933. [17] A. Pachla et al., Synthesis and antibacterial properties of Fe3O4-Ag nanostructures, Polish J. Chem. Techol. 18 (2016) 110–116. [18] N. Niño-Martínez, G.A. Martínez-Castañón, A. Aragón-Piña, F. MartínezGutierrez, J.R. Martínez-Mendoza, F. Ruiz, Characterization of silver nanoparticles synthesized on titanium dioxide fine particles, Nanotechnology 13 (2008) 065711. [19] J.M. Andrews, Determination of minimum inhibitory concentrations, J. Antimicrob. Chemother. 48 (2001) 5–16.
Contents lists available at ScienceDirect
Materials Letters journal homepage: www.elsevier.com/locate/mlblue
«Janus»-like Cu-Fe bimetallic nanoparticles with high antibacterial activity O.V. Bakina ⇑, E.A. Glazkova, N.V. Svarovskaya, N.G. Rodkevich, M.I. Lerner Institute of Strength Physics and Materials Sciences of Siberian Branch of Russian Academy of Sciences, Russian Federation
a r t i c l e
i n f o
Article history: Received 4 December 2018 Received in revised form 16 January 2019 Accepted 18 January 2019 Available online 24 January 2019 Keywords: Bimetallic nanoparticles Electric explosion of wires «Janus»-like nanoparticles Antibacterial activity
a b s t r a c t The search of new efficient antibacterial agents for biomedical applications is subject of researchers special attention. Bimetallic nanoparticles containing biologically active metals are prospective antibacterial agents. The «Janus»-like Cu/Fe nanoparticles prepared by electrical explosive of wires were found to exhibit high antibacterial activity comparable with that of Ag nanoparticles and exceed the antibacterial activity of Fe and Cu monometallic nanoparticles and their mixture. MIC values of bimetallic Cu/Fe particles are 3.91–250 mg/ml. This strong antibacterial activity is due to the synergistic bactericidal Cu2+ and Fe3+ ions released from Cu/Fe bimetallic nanoparticles. Cu/Fe nanoparticles are a promising material for antibacterial protection technologies and for fighting drug-resistant bacterial strains. Ó 2019 Elsevier B.V. All rights reserved.
1. Introduction Bimetallic nanoparticles (BNPs) including those obtained from immiscible metals are of great interest today. The reason of the interest is that BNPs exhibit new properties caused by the mutual influence of the particles components. There are a sufficient number of papers devoted to production of BNPs having antibacterial properties due to presence of silver as the particle core or shell. However, the use of nanoparticles containing silver is limited because of their pronounced cytotoxicity and genotoxicity [1]. While the applying of BNPs containing biologically active metals, such as Cu and Fe is prospective [2]. Cu/TiO2 colloid dispersion exhibited enhanced antibacterial activity due to the synergetic antibacterial effect of Cu and TiO2 by the generation of reactive oxygen species and the migration of copper ions [3]. Cu/Zn BNPs exhibited synergetic antibacterial effects resulted from the relatively slower release of Cu nanoparticles and faster release of Zn nanoparticles [4]. Authors [5] have shown pronounced antibacterial activity of Fe nanoparticles in conjunction with other biologically active metals against microorganisms. Authors [6] have shown that ZnO nanoparticles alloyed with Fe efficiently suppressed the growth of E. coli while being non-toxic for mammalian cells. The same effect was observed for sea urchin-like ZnO/Fe nanoparticles [7]. «Janus»-like Cu/Fe BNPs should be expected to exhibit antibacterial effect based on the ability of Cu2+ ions to ⇑ Corresponding author at: 2/4, pr. Akademicheskii, Tomsk 634021, Russian Federation. E-mail address: [email protected] (O.V. Bakina). https://doi.org/10.1016/j.matlet.2019.01.105 0167-577X/Ó 2019 Elsevier B.V. All rights reserved.
change the permeability of bacterial membranes, and Fe3+ ions to penetrate into the bacterial cell and bind with its components [8]. Here, the electrical explosion of wires (EEW) is a facile and promising method to obtain stable BNPs with different component ratios [9,10]. Hence in this work the antibacterial activities of «Janus»-like Cu/Fe BNPs against bacterial strains have been studied. The effects of varying the Cu/Fe molar ratio on the antibacterial properties have been investigated and the results are discussed in this paper. 2. Materials and methods Cu/Fe BNPs were obtained by the simultaneous electrical explosion of twisted wires (iron and copper) in argon medium [9]. The surface of the particles is covered by a thin oxide layer. The mass ratio of copper and iron in the nanoparticles was regulated by varying the wire diameters. The obtained Cu/Fe nanoparticles were characterized by transmission electron microscopy (JEOL 2000FX, JEM, Japan), X-ray diffraction (DRON-7, Russia), low-temperature nitrogen adsorption (Katakon, Russia). The concentration of Cu and Fe was measured by voltammetric stripping method (Voltammetric analyzer STA, Russia). The error in concentrations was not more 3 %. Escherichia coli ATCC 25922, Staphylococcus aureus ATCC 6538, Pseudomonas aeruginosa ATCC 9027 and MRSA ATCC 43300 were used to detect antimicrobial activity of nanoparticles. For the determination of the minimum inhibitory concentrations (MIC) values 150 ml of the Muller-Hinton broth and 20 ml of aqueous dispersions of nanoparticles were added in each well of disposable 96-well plates. The plates were then inoculated with
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O.V. Bakina et al. / Materials Letters 242 (2019) 187–190
the tested bacteria at a concentration of 106°CFU/ml. The MIC values were determined after 16 h of incubation at 37 °C using the Multiskan FC microplate spectrophotometer (Thermo Fisher Scientific, USA).
time. Due to surface tension, liquid copper strives to take the energetically favourable spherical shape. So the formation of a «Janus» particle occurs (Fig. 2). 3.2. Antimicrobial activity of Cu/Fe nanoparticles
3. Results and discussion 3.1. Characteristics of the Cu/Fe bimetallic nanoparticles In case of simultaneous electric explosion of iron and copper wires in the argon atmosphere the spherical 63–72 nm particles formed regardless of the wire diameter ratio. In Fig. 1 we show cake-graph together with microphotographs and X-ray diffraction patterns of the as-prepared samples. In the X-ray diffraction patterns of the BNPs (Fig. 1), the main reflexes correspond to the phases of Fe and Cu. The ratio of peak heights correlates with the mass ratio of copper and iron. According to EDAX-TEM analysis data, iron and copper are non-uniformly distributed over the volume of particles (Fig. 2). There are areas enriched with one of the components, the phase boundary between Fe and Cu domains is clearly visible. Langlois et al. observed the formation of similar structures for Ag-Cu nanoparticles [11]. The morphology of these structures can be classified as classified Janus, quasi-Janus and ball-and-cup [12]. Regardless of the components ratio the nanoparticles are formed from the liquid phase [13]. For both Cu/Fe and Cu/Pb nanoparticles [9], the following mechanism of formation is possible. The products of the explosion of Cu and Fe wires, from which Cu/Fe BNPs are formed, cool down in a non-uniform manner. The metal with a higher melting point temperature (iron) crystallizes the first and then the metal with a lower melting point temperature (copper) crystallizes while the products are cooling. The liquid copper may be staying on the surface of the iron core for some
The antibacterial activity of Cu/Fe nanoparticles is determined by a standard serial microdilution method (Fig. 2). Water suspensions of monometallic Fe and Cu nanoparticles and their mixture show significantly lower antimicrobial activity against all bacterial strains as compared with bimetallic nanoparticles. MIC values of iron or copper nanoparticles are 125–500 mg/ ml, while MIC values of bimetallic Cu/Fe particles are 3.91– 250 mg/ml (Fig. 3). Cu72/Fe28 nanoparticles suppress the growth of gram-positive bacteria more efficiently than Cu28/Fe72. The MIC value for Cu72/Fe28 was 3.91 mg/ml for S. aureus and 31.25 mg/ml for MRSA, which was two times lower than the Cu28/Fe72. However, the antibacterial activity of Cu28/Fe72 BNPs against gram-negative E. coli and P. aeruginosa is higher than that of Cu72/Fe28 and Cu50/Fe50. Copper nanoparticles are widely known as antibacterial agents. The mechanism of their action is based on the ability to be adsorbed to a bacterium cell wall leading to the destruction of the cell membrane. The destruction of cell membrane of E. coli was demonstrated by the atomic force microscopy [14]. The increased antibacterial activity of nanoparticles due to the copper loading in the samples is expected. Iron and copper are known to form a galvanic couple which leads to the dissolution of iron and the formation of Fe3+ ions. The ions kill bacteria by binding biological molecules which results in protein denaturation, DNA damage and the disruption of enzyme functions [15]. The authors [16] observed the destruction of E. coli cell membranes exposed to iron nanoparticles, Fe3+ ions binding with intracellular oxygen or hydrogen peroxide. Therefore, we assume not only
Fig. 1. (a) Cake-graphs illustrating composition based on chemical analysis, (b) TEM images, (c) XRD-analysis of Cu/Fe BNPs and (d) particle size distribution.
O.V. Bakina et al. / Materials Letters 242 (2019) 187–190
189
Fig. 2. (a) EDAX-TEM images of Cu50/Fe50 nanoparticles.
Fig. 3. Antibacterial activities by Cu/Fe, Cu and Fe nanoparticles and their mixtures and corresponding images representation of MBC of nanoparticles (250 lg/ml).
copper nanoparticles are responsible for the high antibacterial activity of Cu/Fe BNPs, but Fe3+ ions as well. The Cu/Fe BNPs under investigation exhibit antibacterial activity comparable with silver-based nanocomposites considered the most efficient antibacterial agents. For instance, according to Ref. [17] the MIC value for binary Fe3O4-Ag 20 nm nanostructures against E. coli was 120 mg/ml. For Ag/ZnO nanocomposites of less
than 100 nm in size, the MIC value against E. coli was 100 mg/ml, and 200 mg/ml against P. aeruginosa. The authors [18] have shown MIC for Ag/TiO2 nanoparticles to be 130 and 208 mg/ml, and for Ag particles (20 nm in size) to be 13 and 16 lg/ml against E. coli and S. aureus, respectively. These data indicate a significant inhibitory effect of bimetallic Cu/Fe nanoparticles whose MIC values are close to those of antibiotics against all tested microorganisms [19].
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4. Conclusion The antibacterial effect of Cu/Fe BNPs towards to four bacterial strains has been studied. The nanoparticles have been found to have high antibacterial activity against both Gram-negative and Gram-positive bacteria, including the antibiotic-resistant MRSA strain. Cu/Fe BNPs are prospective as antibacterial medications for wound treatment and expected alternative to silvercontaining nanomaterials with pronounced cytotoxicity and genotoxicity. Conflict of interest None. Acknowledgements The synthesis and characterization of nanoparticles were produced under the financial support of the Russian Science Foundation (Project No. 17-19-01319). The antimicrobial activity was financially supported by the Fundamental Research Program of the State Academies of Sciences for 2016–2020. References [1] P.V. Asha Rani, G.L.K. Mun, M.P. Hande, S. Valiyaveettil, Cytotoxicity and genotoxicity of silver nanoparticles in human cells, ACS Nano 3 (2009) 279– 290. [2] R. Parimaladevi, V. Poornima Parvathi, S. Sowmiya Lakshmi, M. Umadevi, Synergistic effects of copper and nickel bimetallic nanoparticles for enhanced bacterial inhibition, Mater. Lett. 211 (2018) 82–86. [3] S. Chen et al., Synergistic antibacterial mechanism and coating application of copper/titanium dioxide nanoparticles, Chem. Eng. J. 256 (2014) 238–246. [4] M. Ashfaq, N. Verma, S. Khan, Copper/zinc bimetal nanoparticles-dispersed carbon nanofibers: a novel potential antibiotic material, Mater. Sci. Eng. 59 (2016) 938–947.
[5] S.A. Mahdy, Q.J. Raheed, P.T. Kalaichelvan, Antimicrobial activity of zero-valent iron nanoparticles, Int. J. Modern Eng. Res. 2 (2012) 578–581. [6] K. Ravichandran et al., Effect of Fe + F doping on the antibacterial activity of ZnO powder, Ceram. Int. 41 (2015) 3390–3395. [7] J. Ma, A. Hui, J. Liu, Y. Bao, Controllable synthesis of highly efficient antimicrobial agent-Fe doped sea urchin-like ZnO nanoparticles, Mater. Lett. 158 (2015) 420–423. [8] J.H. Byeon, Rapid green assembly of antimicrobial nanobunches, Sci. Rep. 6 (2016) 27006. [9] M.I. Lerner, A.V. Pervikov, E.A. Glazkova, N.V. Svarovskaya, A.S. Lozhkomoev, S. G. Psakhie, Structures of binary metallic nanoparticles produced by electrical explosion of two wires from immiscible elements, Powder Techol. 288 (2016) 371–378. [10] O.V. Bakina, E.A. Glazkova, A.S. Lozhkomoev, M.I. Lerner, N.V. Svarovskaya, Cellulose acetate fibres surface modified with AlOOH/Cu particles: synthesis, characterization and antimicrobial activity, Cellulose 25 (2018) 4487–4497. [11] C. Langlois, Z.L. Li, J. Juan, D. Alloyeau, J. Nelayah, D. Bochicchio, R. Ferrandod, C. Ricolleaua, Transition from core–shell to Janus chemical configuration for bimetallic nanoparticles, Nanoscale 4 (2012) 3381–3388. [12] R. Ferrando, Symmetry breaking and morphological instabilities in core-shell metallic nanoparticles, J. Phys. Condens. Matter 27 (2015) 013003. [13] A. Pervikov, M. Lerner, K. Krukovskii, Structural characteristics of copper nanoparticles produced by the electric explosion of wires with different structures of metal grains, Curr. Appl. Phys. 17 (2017) 201–206. [14] U. Bogdanovic´, V. Lazic´, V. Vodnik, M. Budimir, Z. Markovic´, S. Dimitrijevic´, Copper nanoparticles with high antimicrobial activity, Mater. Lett. 128 (2014) 75–78. [15] S. Stankic, S. Suman, F. Haquel, J. Vidic, Pure and multi metal oxide nanoparticles: synthesis, antibacterial and cytotoxic properties, J. Nanobiotechnol. 14 (2016) 73. [16] C. Lee, J.Y. Kim, W.I. Lee, K.L. Nelson, J. Yoon, D.L. Sedlak, Bactericidal effect of zero-valent iron nanoparticles on Escherichia coli, Environ. Sci. Technol. 42 (2008) 4927–4933. [17] A. Pachla et al., Synthesis and antibacterial properties of Fe3O4-Ag nanostructures, Polish J. Chem. Techol. 18 (2016) 110–116. [18] N. Niño-Martínez, G.A. Martínez-Castañón, A. Aragón-Piña, F. MartínezGutierrez, J.R. Martínez-Mendoza, F. Ruiz, Characterization of silver nanoparticles synthesized on titanium dioxide fine particles, Nanotechnology 13 (2008) 065711. [19] J.M. Andrews, Determination of minimum inhibitory concentrations, J. Antimicrob. Chemother. 48 (2001) 5–16.