Synthesis, characterisation and antimicrobial activity

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Apr 2, 2015 - and iron-doped zinc oxide nanoparticles, Journal of Experimental Nanoscience, DOI: ... Keywords: antimicrobial activity; ZnO NPs; XRD; TEM; FTIR. 1. ..... metal oxide and/or transition metals increases the surface defects.

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Synthesis, characterisation and antimicrobial activity of manganese- and iron-doped zinc oxide nanoparticles a

a

b

Neha Sharma , Savita Jandaik , Sanjeev Kumar , Mansi Chitkara

c

c

& Inderjit Singh Sandhu a

Department of Biotechnology, Shoolini University, Bajhol, Post Office Sultanpur, Solan, HP 173212, India b

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Department of Physics, Goswamy Ganesh Dutta Satnam Dharma (GGDSD) College, Panjab University, Sector 32, Chandigarh, India c

Nanomaterial Research Laboratory, Chitkara University, Punjab, India Published online: 02 Apr 2015.

To cite this article: Neha Sharma, Savita Jandaik, Sanjeev Kumar, Mansi Chitkara & Inderjit Singh Sandhu (2015): Synthesis, characterisation and antimicrobial activity of manganeseand iron-doped zinc oxide nanoparticles, Journal of Experimental Nanoscience, DOI: 10.1080/17458080.2015.1025302 To link to this article: http://dx.doi.org/10.1080/17458080.2015.1025302

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Journal of Experimental Nanoscience, 2015 http://dx.doi.org/10.1080/17458080.2015.1025302

Synthesis, characterisation and antimicrobial activity of manganese- and iron-doped zinc oxide nanoparticles Neha Sharmaa, Savita Jandaika*, Sanjeev Kumarb, Mansi Chitkarac and Inderjit Singh Sandhuc a

Department of Biotechnology, Shoolini University, Bajhol, Post Office Sultanpur, Solan, HP 173212, India; Department of Physics, Goswamy Ganesh Dutta Satnam Dharma (GGDSD) College, Panjab University, Sector 32, Chandigarh, India; cNanomaterial Research Laboratory, Chitkara University, Punjab, India b

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(Received 11 November 2014; final version received 24 February 2015) The present work reports study on antimicrobial activity of pure and doped ZnO nanocomposites. Polyvinyl pyrrolidone capped Mn- and Fe-doped ZnO nanocomposites were synthesised using simple chemical co-precipitation technique. The synthesised materials were characterised using transmission electron microscope (TEM), X-ray powder diffraction (XRD), energy dispersive X-ray fluorescence (EDXRF), Fourier transform infrared (FTIR) spectroscopy and ultraviolet (UV) visible spectroscopy. The XRD and TEM studies reveal that the synthesised ZnO nanocrystals have a hexagonal wurtzite structure with average crystalline size »7 14 nm. EDXRF and FTIR study confirmed the doping and the incorporation of impurity in ZnO nanostructure. The antimicrobial activities of nanoparticles (NPs) were studied against fungi, grampositive and gram-negative bacteria using the standard disc diffusion method. The photocatalytic activities of prepared NPs were evaluated by degradation of methylene blue dye in aqueous solution under UV light irradiation. Experimental results demonstrated that ZnO NPs doped with 10% of Mn and Fe ions showed maximum antimicrobial and photodegradation efficiency in contrast with that of the 1% loading. The enhancement in antimicrobial effect and photocatalytic degradation is attributed to the generation of reactive oxygen species due to the synergistic effects of Mn and Fe loading. Keywords: antimicrobial activity; ZnO NPs; XRD; TEM; FTIR

1. Introduction Pathogenic microbial contaminations and eradication of organic pollutants have been a major threat to mankind as well as to the environment. Therefore, the development of more efficient material with enhanced antimicrobial and photocatalytic activity is of great significance. Despite the great progress in antimicrobial development, many infectious diseases like intracellular infections are difficult to treat.[1,2] Major reasons of difficulty are transportation through cell membranes, low activity in the cells, antimicrobial toxicity to healthy tissues and acquired resistance of infectious microbes.[3 6] To address these issues, nanoscale materials have been emerged up as novel antimicrobial agents. Nanoparticles (NPs) are ideal forms of antimicrobial agents because these materials exhibit large surface *Corresponding author: Email: [email protected] Ó 2015 Taylor & Francis

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to volume ratio and high reactivity in comparison to bulk form.[7,8] Many NPs have antimicrobial properties and used to control drug-resistant microbial populations.[9] Various inorganic metal oxide NPs viz., ZnO, MgO, TiO2 and SiO2 exhibit considerable antimicrobial activities and used in therapeutics, diagnostics and nanomedicine-based antimicrobial agents.[7,10 12] Inorganic NPs show greater effectiveness on resistant strains of microbial pathogens, less toxicity, heat resistance and provide mineral elements essential to human cells.[13 15] Ariga et al. proposed the new concept of bioinspired nanoarchitectonics as emerging drug delivery systems.[16] The polymer-based NP drug delivery system can also be designed to improve the pharmacokinetics and bio distribution of the drug.[17] Nakanishi et al. have summarised the biological applications, especially cell growth, sensing, and control using nanoarchitectures of nanocarbons.[18] Wang et al.[19] proposed that nanodiamond epirubicin drug delivery complex is capable of killing chemoresistant cancer stem cells and preventing secondary tumour formation in liver cancer. It has been noticed that compound naphthalocyanine encapsulated in water soluble polymer dendrimer can be used to kill the tumour and cancer cells in ovarian cancer.[20] The applications of nanomaterials in the food processing and shipping industries have also been reported in literature.[21] Among metal oxide NPs, ZnO NPs have many significant features such as chemical and physical stability, high catalytic activity, effective antibacterial activity as well as intensive ultraviolet (UV) and infrared (IR) adsorption.[22,23] In addition to this, ZnO NPs are most efficient photocatalysts used in the photodegradation of environmental organic pollutants and toxic.[24,25] The most common technique used to produce defects in pure ZnO NPs is based on the choice of synthesis methods,[26,27] use of composite photocatalysts [28,29] and the doping of pure ZnO with suitable metal ion impurities.[30,31] Various transition metal ions [32 35] have been used to increase the interfacial charge transfer kinetic of ZnO nanostructures. ZnO NPs have wide range of applications. It is found in paints, cosmetics, plastic and rubber manufacturing, electronics and pharmaceuticals. It is also widely used to treat a variety of skin conditions, in products such as baby powder, antidandruff shampoos and antiseptic ointment.[36] It is also a component in tape used by athletes as a bandage to prevent soft tissue damage during workouts.[37] These materials have been successfully used for water disinfection and purification.[38] The present work reports the antimicrobial and photocatalytic activities of Mn- and Fe-doped ZnO NPs synthesised using chemical coprecipitation method.

2.

Experimental

2.1. Materials Following bacteria and fungus were used in the present study. Bacteria: Staphylococcus aureus, Escherichia coli, Klebsiella pneumoniae, Salmonella typhi, Pseudomonas aeruginosa, Bacillus subtilis. Fungi: Candida albicans, Aspergillus fumigatus, Cryptococcus neoformans, Trichophyton mentegrophytes. Clinical isolates (C) of bacteria and fungi were procured from Gian Sagar, Medical College, Rajpura, Punjab. Standard cultures (S) of bacteria and fungi were procured from Institute of Microbial Technology, Chandigarh.

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2.2. Preparation of pure and doped ZnO NPs The polyvinyl pyrrolidone (PVP) capped pure ZnO NPs and doped with Fe (1% and 10%) and Mn (1% and 10%) were prepared using bottom-up wet chemical precipitation technique through hydrolysis and oxidising process. In a typical synthesis of Mn-doped ZnO nanocrystals, 1.0 M ZnCl2, 0.1 M MnCl2.4H2O, 2.0 M NaOH and 2% PVP were prepared separately in deionised water. The Zn and Mn precursor solutions were mixed in the stoichiometries proportion under vigorous stirring. 4 ml of 2% PVP solution was added to total 50 ml volume, before dropwise addition of 1.0 M ZnCl2 solution into 2.0 M NaOH solution. Likewise, the Fe-doped ZnO NPs were prepared using 1.0 M ZnCl2, 0.1 M FeCl3 and 2.0 M NaOH precursor solutions in the stoichiometries proportion. The resulting precipitates were filtered, thoroughly washed and then dried in air at ambient temperature to obtain NPs in powder form. Finally, the synthesised powder was calcined in a muffle furnace at 600  C for 2 h under normal atmospheric conditions.

2.3. Characterisation 2.3.1. X-ray diffraction (XRD) analysis The crystalline size of pure and doped ZnO NPs has been determined from XRD spectra recorded using powder XRD (PAN-Analytic) set-up equipped with 3050/60 goniometer and Cu anode X-ray tube. The XRD scans for the powder samples were performed in the 2 (range 20 80 ) keeping step size 0.001 for the Cu K X-ray radiation  (λ D 1.5418 A). 2.3.2. Transmission electron microscopy (TEM) Formation and particle sizes of the synthesised materials were confirmed from TEM by placing a drop of the NPs dissolved in methanol on carbon coated grids and air drying. TEM images were taken using Hitachi (H-7500) TEM facility available at Punjab University, Chandigarh, India, at an accelerating voltage of 160 kV with magnification of £30 K and £30 K.

2.3.3. Fourier transform infrared (FTIR) spectroscopy The presence of various chemical functional groups and the formation of pure ZnO NPs doped with Fe (1% and 10%) and Mn (1% and 10%) are also supported by FTIR spectra of NPs encapsulated with potassium bromide (KBr) salt. The characteristic IR absorption was recorded in the frequency range of 4000 4500 cm¡1 using a TAG FTIR spectra.

2.3.4. Ultraviolet Visible (UV Vis) spectroscopy The optical absorption measurements were carried out using UV Vis absorption spectrophotometer (Systronic PC based Double Beam Spectrophotometer: 2202). For UV Vis absorption studies 0.01 g of pure and doped ZnO NP powder was dispersed in 10 ml of methanol solution, and further used for characterisation.

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2.3.5. Photocatalytic measurements The photocatalytic activities of NPs were examined by studying the degradation of methylene blue (MB) dye aqueous solution under UV exposure. The photocatalytic studies under UV light were performed using UV-photoreactor equipped with two 18 W UV tubes (Orial made 66001). The photocatalytic reaction under UV light were carried out with »112 mg nanopowder mixed with 250 ml of 32 ppm MB dye solution in a glass reactor with surface area 200 cm2. The aqueous suspension was put under constant stirring in dark for 1 h, so that the MB dye atoms were adsorbed on the surface of nanocrystals. The stable suspension was then exposed to the UV radiation with continuous magnetic stirring. About 10 ml of suspension solutions was sampled at different time intervals and centrifuged. The supernatant after centrifugation was analysed by the UV-Vis spectrophotometer. The rate of decolourisation of the test contaminant was noticed from the optical absorption spectra. The degradation efficiency (e) of dye is calculated from the equation eD

C0 ¡ C £100 C0

(1)

where C0 is the initial concentration of the dye and C is the concentration after UV photons irradiation. The photocatalytic process of MB can be expressed as apparent pseudo-first-order kinetic equation: ln

C0 D kt C

(2)

where k is the apparent pseudo-first-order rate constant, C0 is original MB concentration and C is MB concentration in aqueous solution at time t.

2.4. Determination of antimicrobial activity 2.4.1. Disc diffusion assay Antibacterial and antifungal activities of the synthesised NPs were evaluated by the standard disc diffusion method described by Bauer et al. [39] and modified according to clinical and laboratory standards institute guidelines.[40] The chosen concentration range was 1mg/ml to 100 mg/ml in methanol and activity was determined by measuring the zone of inhibition.

2.4.2. Determination of MIC, MBC and MFC Minimum inhibitory concentration (MIC) of the NPs for various bacteria was calculated by Broth micro dilution reference method (CLSI M7-A7) [41] after determination of minimum effective antibacterial concentration from the disc diffusion method. The MIC of NPs for filamentous fungi was done by Broth micro dilution reference method (CLSI M38-A2) [42] and for yeast by (CLSI M27-A3).[43] Resazurin reagent was used as indicator. The lowest concentration that prevented colour change was taken as a minimum inhibitory concentration. Maximum bactericidal concentration (MBC) and

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maximum fungicidal concentration (MFC) were determined by plating a particular volume of sample from the wells in the microtitre plate on the nutrient agar and sabouraud dextrose agar plates of bacteria and fungi, respectively.

3. Results and discussion 3.1. Characterisation

DD

0:9λ b cos u

where b is full width half maxima of the diffraction peak, u is the Bragg peak angle and λ is the wavelength of Cu Ka radiation. The average crystalline sizes calculated using the Scherrer formula for ZnO nanomaterial doped with different contents of Mn and Fe impurities are given in Table 1.

ZnO doped with 10% Mn

ZnO doped with 10% Fe

Intensity (a.u.)

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3.1.1. X-ray diffraction (XRD) analysis The XRD patterns for pure and doped ZnO powder samples are shown in Figure 1. All recorded reflections support the hexagonal wurtzite structure of ZnO with lattice parameters a D b D 3.249 A and c D 5.206 A. The average crystalline size (D) of the synthesised NPs was calculated using the Scherrer’s formula,[44]

Pure ZnO

39

52

Angle (2θ) Figure 1 . X-ray diffraction of pure and doped ZnO NP.

65

78

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Table 1. Decolourisation rate constants of MB dye using ZnO photocatalysts doped with Mn and Fe impurities under UV exposure. Decolourisation under UV light Samples Pure ZnO ZnO doped with 1% Mn ZnO doped with 10% Mn ZnO doped with 1% Fe ZnO doped with 10% Fe

Crystalline size (nm)

Rate constant (k) in min¡1

Correlation co efficient (R2 value)

13 7 10 12 14

6.09E-4 1.79E-3 3.38E-3 4.24E-3 6.65E-3

0.556 0.943 0.961 0.979 0.970

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3.1.2. Transmission electron microscopy (TEM) The particle size and morphology of the synthesised ZnO NPs were analysed from TEM micrographs (Figure 2(a) and 2(b)). The micrographs reveal that the product consists of spherical particles with the average size »9 15 nm, which is in good agreement with that estimated by Scherer formula based on the XRD pattern.

3.1.3. Fourier transform infrared (FTIR) spectroscopy The presence of various chemical functional groups and the formation of PVP capped ZnO NPs are also supported by FTIR spectra (Figure 3) in KBr matrix. Similar spectra were obtained for the undoped ZnO as well as for the Mn- and Fe-doped ZnO samples. The absorption peaks in the range of 400 700 cm¡1 could be attributed to the ZnO stretching modes.[45] Also observed were weak absorption peaks in the range of 1100 1600 cm¡1 corresponding to the OH bending mode,[46] C OH plane bending and C OH out-ofplane bending.[47] We observed a broad band in the 2900 3700 cm¡1 region, which can

Figure 2. Transmission electron micrograph showing pure and doped ZnO NP.

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(a) Pure Zno

(c) ZnO doped with 10% Fe

4000

3500

3000

2500

1500

2000

1000

500

-1

Wave number (cm )

Figure 3. FTIR spectra of pure and doped ZnO NP.

be explained as overlapping O H stretching modes and C H stretching modes. Another major characteristic peak is due to PVP capping agent and coupling agent (KH-570) used in the IR spectroscopy.

3.1.4. Ultraviolet Visible (UV Vis) spectroscopy Figure 4 shows the UV Vis absorption spectra of pure ZnO and ZnO doped with 10% Mn and Fe impurities. The absorption peaks of pure ZnO, Mn- and Fe-doped ZnO NPs are 399, 378 and 389 nm, respectively. It has been noticed that the position of absorption spectra in case of doped ZnO nanomaterial shifts towards the lower wavelength side with

2.2

Pure ZnO ZnO doped with 10% Fe ZnO doped with 10% Mn

2.0

Absorbance (a.u.)

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Transmittance (a.u.)

(b) ZnO doped with 10% Mn

1.8

1.6

1.4

390

520

° Wave length in (A)

650

Figure 4. UV Vis absorption spectra of pure and doped ZnO NP.

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3.1.5. Photocatalytic measurements Photocatalytic performances of the synthesised nanostructures were evaluated by photodegradation of MB dye under UV light using optical absorption spectroscopy. The sensitised photodegradation curves and plot of Ln (C0/C) versus the UV irradiation time (t) in presence of different photocatalysts are shown in Figure 5(a) and 5(b), respectively. A near linear relationship between Ln (C0/C) and ‘t’ divulges that photodegradation of MB dye follows the pseudo-first-order kinetics. The photocatalytic degradation of MB dye was evaluated from the apparent rate constants (k) calculated from the linear curves using Equation (2). Higher the value of apparent rate constants (k) more will be the photocatalytic performance. The obtained first-order rate constants (k) and degradation efficiency (e) of the synthesised NPs under UV exposure are also listed in Table 1. Degradation efficiency of pure and doped ZnO NPs is also shown in a bar diagram (Figure 6). The experimental results clearly show the significance of Mn- and Fe-doping for the photocatalytic degradation of the MB dye solution. It has been noticed that the MB dye solution degraded to maximum extent (e D 65% and k D 6.65 £ 10¡3 s¡1) in case of ZnO nanocrystals doped with 10% Fe impurity, whereas it degraded to the minimum

(a)

Dye conc. (%)

104

78

52

26

Pure ZnO ZnO doped with 1% Mn ZnO doped with 10% Mn ZnO doped with 1% Fe ZnO doped with 10% Fe 16

32

48

64

80

96

112

Time (minutes) 0.57

0.38

ln(C0/C)

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increasing dopants concentration. This indicates that band gap of pure ZnO material increases with doping concentration. The increase in band gap or blue shift can be explained by the Burstein Moss effect.

Pure ZnO ZnO doped with 1% Fe ZnO doped with 10% Fe ZnO doped with 10% Mn ZnO doped with 1% Mn

(b)

0.19

0.00 16

32

48

64

80

96

Time (minutes) Figure 5. Photodegradation of MB dye by ZnO NPs and doped NPs.

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Degradation efficiency (%)

57

9

Pure ZnO ZnO doped with 1% Mn ZnO doped with 10% Mn ZnO doped with 1% Fe ZnO doped with 10% Fe

38

19

0 0

30

60

90

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Time (in minute)

Figure 6. Degradation efficiency of pure and doped ZnO NP.

extent (e D 9% and k D 6.08 £ 10¡4 s¡1) by pure ZnO photocatalyst after 105-min UV light irradiation.

3.2. Antimicrobial activity 3.2.1. Disc diffusion assay The antimicrobial activity of pure and doped NPs is given in Tables 2 4. It is clear from the tables that ZnO NPs doped with 10% Mn and Fe ions impurities exhibit higher antibacterial activities as compared to 1% loading and pure ZnO. The experiment results indicate that doping in the nanomaterials plays a significant role in the antibacterial activity. Our results are well supported by the earlier studies reported by Sharma et al. [48] and Rekha et al. [49] that transition metal doping in ZnO enhances the antibacterial activity. Thus, in this report, doped ZnO NPs have shown the best antibacterial behaviour compared to ZnO NPs. The antifungal effect of NPs has received only marginal attention and just a few studies on this topic have been published. In case of fungi the activity was reported only against T. mentagrophytes (S) and C. neoformans (C) and no activity was seen in the case of A. fumigatus and C. albicans. Our results showed better antifungal activity against T. mentagrophytes as compared to the earlier work of Kim et al. who reported antifungal effect of Ag NPs on T. mentagrophytes and C. albicans at 1mg/ml.[50] However, in our study no activity has been observed against C. albicans and A. fumigatus. The absence of activity against Aspergillus may be due to the complex cell wall structure with high percentage of chitinous layer. Owing to the chitin layer, OH produced by NPs was not able to cause the destruction of cell wall.[51] Though at high concentration (100 mg/ml) activity against C. neoformans was observed in our study, which is quite least studied. However, the exact mechanism of resistance to the fungus is not known till now. The interaction between NPs and the membrane results changes in the membrane observed as ‘pits’ on the membrane surfaces. The formation of pores subsequently leads to cell death.[52] It may also be the case through which ZnO NPs showed activity against T. mentagrophytes and C. neoformans.

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Table 2. Antimicrobial activity of ZnO NPs against various microorganisms.

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ZnO NPs (mg/ml) Microorganisms

100

50

25

10

1

Bacteria B. subtilis (S) B. subtilis (C) K. pneumonia (S) K. pneumonia (C) S. aureus (S) S. aureus (C) E.coli (S) E.coli (C) P. aeruginosa (S) P. aeruginosa (C) S. typhi (S) S. typhi (C)

30.6 § 0.5 37 § 3 27.3 § 1.5 28.3 § 0.57 35.3 § 1.5 32 § 1 27.6 § 0.57 24 § 1 29 § 1 26.7 § 1.5 31 § 1 28.6 § 1.5

28.6 § 1.5 34.6 § 3.2 27.3 § 1.5 28.3 § 0.57 31.3 § 1.5 30.3 § 0.57 24.6 § 0.57 23 § 2 28 § 1 21.3 § 1.5 30.6 § 1.5 28 § 1

Zones (mm) 24.7 § 1.5 33.3 § 2.1 23.3 § 0.57 21 § 1 24.6 § 2.5 24.3 § 1.5 23 § 2 21.3 § 0.57 24 § 1 19 § 2 28.3 § 0.57 23 § 1

21 § 2 31.3 § 0.57 21 § 2.6 20.6 § 0.57 21.3 § 1.5 20.7 § 1.5 20 § 1 19 § 2 20.6 § 1.5 19.3 § 1.5 27.2 § 1 22.7 § 1.5

21.3 § 3.5 21 § 1 16.7 § 1 18.6 § 2.1 21 § 2 20.3 § 2.1 18.3 § 2.5 18.6 § 2.5 16.6 § 1.1 13.3 § 1.5 23.3 § 1 22 § 2.1

26 § 1.5 10.6 § 1

25 § 1.5 NZ

23 § 2 NZ

20.3 § 1.5 NZ

19.6 § 2.1 NZ

Fungi/yeast T. mentegrophytes (S) C. neoformans (C)

Note: S, standard isolate; C, clinical isolate; NZ, no zone.

In this study, different concentrations of nanoscale Fe- and Mn-doped ZnO and pure ZnO were tested to find out the best concentration that can have the most effective antibacterial property. With an increase in concentration of doping antimicrobial activity increased. Our data are in accordance with the previous studies, dealing with the antimicrobial effects of NPs.[53] If the concentration of doped metals in nano-ZnO increases in culture medium, interaction between oxygen and dehydrogenase enzyme increases too which enhances antimicrobial activity.[54] The increase in antibacterial and photocatalytic activity to increase in dopants concentration degradation is attributed to the generation of reactive oxygen species (ROS) due to coupling or synergistic effects of Mn and Fe loading. The ROS generation is attributed to the creation of photoinduced charge carriers in ZnO NPs and their interactions with oxygen and water molecules on the surface of particles. It is proposed that photogenerated electron migrates to the surface of dopant ions from the conduction band of excited ZnO (Figure 7). Likewise, the photogenerated hole is also transferred to the surface of ZnO NPs. An electron in the conduction band on the catalyst surface can reduce molecular oxygen to superoxide anion. The superoxide anion can then react with H2O to form H2O2, which further forms OH radicals. On the other hand, migrated hole reacts with chemisorbed H2O molecules to form reactive species such as O2¡ and OH radicals. Such an efficient charge separation increases the lifetime of the charge carriers and increases the efficiency of the interfacial charge transfer to adsorbed substrates. The presence of ROS such as O2¡ and OH radicals is the primary cause of cell death and organic matter mineralisation. Another

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Table 3. Antimicrobial activity of Fe-doped ZnO NPs against various microorganisms.

Microorganisms Bacteria B. subtilis (S) B. subtilis (C) K. pneumonia (S) K. pneumonia (C)

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S. aureus (S) S. aureus (C) E. coli (S) E. coli (C) P. aeruginosa (S) P .aeruginosa (C) S. typhi (S) S. typhi (C) Fungi/yeast T. mentegrophytes (S) C. neoformans (C)

ZnO NPs C Fe concentrations (mg/ml)

Doping conc. (%)

100

50

25

10

1

10 1 10 1 10 1 10 1 10 1 10 1 10 1 10 1 10 1 10 1 10 1 10 1

Zones (mm) 43 § 3.5 33.7 § 1.5 37.7 § 1.1 33.6 § 2.1 30.3 § 1.1 32.6 § 1.5 31.3 § 1.2 33 § 1 35.6 § 0.57 33 § 1 33 § 1 34 § 1 31.7 § 1.1 32.3 § 0.57 29.3 § 2.1 32 § 2.1 32.6 § 0.57 33 § 0.57 30.6 § 1.5 30.7 § 2.1 38.6 § 1.5 29 § 1 37.6 § 1.1 38.3 § 1.5

42.6 § 4 31.3 § 0.57 34 § 1 30.1 § 1.1 29.6 § 0.57 30 § 1 30 § 1 30 § 1.7 31.3 § 1.5 31.3 § 1.5 32 § 1 32.3 § 1.5 29.7 § 0.57 31 § 0.57 27 § 1.7 31 § 3.2 31 § 1 30.6 § 0.57 29.6 § 0.57 25.6 § 1.5 37 § 1 27 § 2 35.3 § 1.5 37.7 § 1.5

43 § 3.5 29.3 § 1.5 34.3 § 0.57 28 § 1 29 § 1 26.6 § 1.2 25.3 § 0.57 25 § 2 30.3 § 1.5 27.3 § 2.1 30.6 § 1.5 31.3 § 2.5 29 § 2 28 § 2.6 23.7 § 1.5 25.4 § 4.3 29.6 § 1.5 25.6 § 1.1 28 § 1 23.3 § 1.5 35 § 1 25.6 § 1.7 33.3 § 1.1 34.6 § 0.57

43.3 § 2.9 26.6 § 2.5 33.4 § 0.57 25.3 § 1.5 27.3 § 1.5 24 § 2 25.6 § 2.1 25.6 § 3.2 29.7 § 1.7 24 § 2.6 30 § 1 29 § 3 27 § 2 26.3 § 3.7 21.3 § 1.5 24 § 4.9 27 § 2.6 23 § 1 27.7 § 2.1 21.3 § 1.5 34 § 1.7 25 § 1.5 32 § 1 32.7 § 1.1

32.6 § 4.6 23.7 § 2.5 32 § 1 20.6 § 2.5 20.3 § 0.57 21.3 § 1.5 21 § 2 21.3 § 0.57 20.3 § 2.5 21.7 § 1.5 20.6 § 1.5 21.6 § 1.5 21 § 1 21.3 § 0.57 19.3 § 0.57 19.3 § 0.57 21.3 § 2.1 21 § 2 19.6 § 1.5 20.3 § 2.1 29.6 § 1.5 24.7 § 1 28.6 § 1.5 23.6 § 1

10 1 10 1

38 § 2.6 35 § 1 11.6 § 1.1 11 § 1.1

37.6 § 1.5 33.3 § 1.5 NZ NZ

32.6 § 1.5 32.6 § 2.1 NZ NZ

31 § 2.6 29.6 § 3.7 NZ NZ

26.6 § 1.5 25.6 § 3.7 NZ NZ

Note: S, standard isolate; C, clinical isolate; NZ, no zone.

possible explanation for this could be the abrasive surface texture of ZnO as doping of metal oxide and/or transition metals increases the surface defects.

3.2.2. Minimum inhibitory concentration (MIC) MIC and MBC/MFC for the NPs were calculated against gram-negative as well as grampositive bacteria and fungal strains (Tables 5 and 6). In this case also doped ZnO NPs were found to be better than pure. Excellent MIC of 0.09 mg/ml against B. subtilis (S) was obtained in the case of 10% Fe doping. Overall, in the present study gram-negative

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Table 4. Antimicrobial activity of Mn-doped ZnO NPs against various microorganisms.

Microorganisms Bacteria B. subtilis (S) B. subtilis (C) K. pneumonia (S) K. pneumonia (C)

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S. aureus (S) S. aureus (C) E. coli (S) E. coli (C) P. aeruginosa (S) P. aeruginosa (C) S. typhi (S) S. typhi (C)

Fungi/yeast T. mentegrophytes (S) C. neoformans (C)

ZnO NPs C Mn concentrations (mg/ml)

Doping conc. (%)

100

50

25

10

1

10 1 10 1 10 1 10 1 10 1 10 1 10 1 10 1 10 1 10 1 10 1 10 1

Zones (mm) 33.6 § 1.1 27.3 § 2.1 37.7 § 0.57 27 § 2 27.6 § 1.5 27.3 § 1.5 28.3 § 1.5 27 § 2.6 37.6 § 1.5 30 § 1 38.3 § 2.5 29.3 § 2.5 29 § 3.6 27.6 § 1.5 27 § 2 26.3 § 1.5 29.3 § 0.57 27.3 § 1.5 29.6 § 1.1 28.7 § 2.8 39.3 § 1.5 28 § 4 29.3 § 3.2 27.6 § 2.5

32 § 2 24.7 § 1.5 36.3 § 2 23.3 § 2.1 27 § 1 26 § 1 27.7 § 1.5 23 § 1.7 35.3 § 1.5 27 § 1 36.3 § 2.1 29.3 § 2.5 27 § 1.7 26 § 1 23 § 1 22.7 § 2.1 28.3 § 2.1 27 § 1.5 29 § 1.7 26.6 § 1.1 36 § 1 26.3 § 2.1 28.7 § 1.5 25.7 § 1.1

30.3 § 1.5 22.3 § 2.1 31.7 § 0.57 22 § 1 24 § 1 23.3 § 2.1 22 § 2 21 § 1 33.3 § 2.3 26.3 § 2.5 33.3 § 0.57 24 § 2.6 15 § 3 25 § 1 22 § 1 21.3 § 1.1 26 § 1 26 § 3.2 26 § 1 26.3 § 1.5 33 § 1 25.3 § 2.1 27.6 § 1.1 24 § 2.6

31.6 § 2.1 21.6 § 1.1 31.6 § 1.1 21.7 § 2.1 24 § 1 21.6 § 2.5 21.6 § 1.5 21 § 1 29 § 2 21.6 § 2.1 29.7 § 1.5 22 § 2.6 24.6 § 1.1 21 § 2 20.7 § 3 20.3 § 2.1 20.6 § 2.5 20.6 § 1.5 21.7 § 1.5 21 § 2.6 29 § 2.6 23.3 § 1.5 27.3 § 1.5 23.6 § 2.1

26.3 § 0.57 20 § 1 25.6 § 0.57 21 § 1 18.3 § 2.1 16.6 § 2.1 18.6 § 2.5 17.7 § 1.5 24.3 § 1.1 19 § 2 26 § 1.1 17.6 § 2.5 21.3 § 3 19.3 § 1.5 19.3 § 0.57 16.3 § 1.5 18.3 § 1.1 16.6 § 1.5 14.3 § 3 13.7 § 1.5 27 § 2 23 § 1 26.6 § 2.1 22 § 1

10 1 10 1

38 § 2.6 35 § 1 11.6 § 1.1 11 § 1.1

37.6 § 1.5 33.3 § 1.5 NZ NZ

32.6 § 1.5 32.6 § 2.1 NZ NZ

31 § 2.6 29.6 § 3.7 NZ NZ

26.6 § 1.5 25.6 § 3.7 NZ NZ

Note: S, standard isolate; C, clinical isolate; NZ, no zone.

bacterial strains were more sensitive in comparison to gram-positive strains against the NPs tested. Except for 10% Fe which showed more activity towards B. subtilis, a grampositive bacteria. However, all other NPs were more sensitive to S. typhi and P. aeruginosa. Previous studies have also shown good activity of ZnO NPs against gramnegative bacteria.[55,56] More activity towards gram-negative bacteria may be because the cell wall of gram-positive bacteria has more peptidoglycan than gram-negative bacteria cell wall, which is negatively charged, and more ZnO, Fe and Mn ions may get trapped to peptidoglycan in gram-positive bacteria.[57] Whereas in case of gram-negative bacteria

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Valance band Reduction reaction

Band gap

O2

Fermi level

Conduction band OH

Oxidation reaction

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Figure 7. Mechanism of action of doped NP.

there are electrostatic interactions between NPs and cell surface followed by cell morphological changes, increase in cell permeability and their accumulation in the cytoplasm.[58] MIC followed the same pattern as antimicrobial activity. MIC observed in T. mentegrophytes (S) and C. neoformans (C) was 0.33 § 0.14 and 26.6 § 14.4 mg/ml, respectively. MIC values for both the fungal strains were 0.25 § 0.21 and 11.5 § 11.8 mg/ ml in case of 10% Fe doping and 0.33 § 0.14 and 13.5 § 10.9 mg/ml in case of 1% Fe doping, respectively. Similarly, MIC values of T. mentegrophytes and C. neoformans were 0.21 § 0.07 and 9.4 § 5.4 mg/ml, respectively (Table 5) in case of 10% Mn doping. MIC of T. mentegrophytes against 1% doping (s) was 0.25 § 0.24 mg/ml whereas for C. neoformans was 14.5 § 9.5 mg/ml (Table 5). However, less activity of NPs against fungus may be attributed to the complex cell wall structure of the fungus. Table 5. Minimum inhibitory concentration (mg/ml) of pure ZnO and doped ZnO NP against various microorganisms. Microorganisms Bacteria S. aureus (S) S. aureus (C) S. typhi (S) S. typhi (C) K. pneumoniae (S) K. pneumoniae (C) B. subtilis (S) B. subtilis (C) E. coli (S) E. coli (C) P. aeruginosa (S) P. aeruginosa (C)

ZnO

ZnO C 10% Fe ZnO C 1% Fe ZnO C 10% Mn ZnO C 1% Mn

0.31 § 0.01 0.31 § 0.01 0.16 § 0.01 0.16 § 0.01 0.31 § 0.02 0.31 § 0.02 0.21 § 0.06 0.24 § 0.04 0.16 § 0.02 0.28 § 0.03 0.43 § 0.05 0.43 § 0.05

0.22 § .03 0.125 § 0.0 0.17 § 0.04 0.29 § 0.00 0.22 § 0.03 0.23 § 0.03 0.09 § 0.00 0.19 § 0.00 0.11 § 0.00 0.14 § 0.00 0.17 § 0.00 0.14 § 0.09

Fungi T. mentegrophytes (S) 0.33 § 0.14 C. neoformans (C) 26.6 § 14.4

0.25 § 0.21 11.5 § 11.8

Note: S, standard isolate; C, clinical isolate.

Concentration (mg/ml) 0.26 § 0.09 0.19 § 0.026 0.26 § 0.09 0.17 § 0.013 0.13 § 0.04 0.11 § 0.024 0.13 § 0.04 0.16 § 0.00 0.21 § 0.06 0.15 § 0.00 0.21 § 0.06 0.13 § 0.012 0.26 § 0.09 0.19 § 0.00 0.23 § 0.09 0.21 § 0.02 0.16 § 0.01 0.12 § 0.02 0.16 § 0.01 0.18 § 0.01 0.31 § 0.05 0.18 § 0.00 0.31 § 0.05 0.27 § 0.02 0.33 § 0.14 13.5 § 10.9

0.21 § 0.07 9.4 § 5.4

0.27 § 0.021 0.17 § 0.013 0.17 § 0.013 0.17 § 0.0 0.26 § 0.0 0.13 § 0.010 0.19 § 0.026 0.24 § 0.027 0.19 § 0.026 0.27 § 0.022 0.15 § 0.003 0.28 § 0.023 0.25 § 0.24 14.5 § 9.5

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Table 6. Minimum bactericidal/fungicidal concentration (mg/ml) of pure ZnO and doped ZnO NP against various microorganisms.

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Microorganisms Bacteria S. aureus (S) S. aureus (C) S. typhi (S) S. typhi (C) K. pneumoniae (S) K. pneumoniae (C) B. subtilis (S) B. subtilis (C) E. coli (S) E. coli (C) P. aeruginosa (S) P. aeruginosa (C)

ZnO 0.35 § .05 0.31 § .03 0.31 § .03 0.38 § .19 0.35 § .21 0.32 § .03 0.23 § .23 0.29 § .19 0.22 § 0 0.42 § .14 0.52 § .07 0.59 § .19

Fungi T. mentegrophytes (S) 0.61 § 0.07 C. neoformans (C) 28 § 21.6

ZnO C 10% Fe ZnO C 1% Fe ZnO C 10% Mn ZnO C 1% Mn 0.28 § .03 0.30 § .03 0.27 § .04 0.31 § .01 0.24 § .09 0.32 § .10 0.14 § .43 0.21 § .07 0.19 § .19 0.25 § .21 0.21 § .07 0.29 § .19 0.5 § 0 29.2 § 19

Concentration (mg/ml) 0.31 § .04 0.25 § .43 0.34 § .43 0.29 § .19 0.29 § .23 0.17 § .28 0.31 § .25 0.23 § .23 0.35 § .21 0.31 § .14 0.35 § .26 0.27 § .21 0.33 § .07 0.19 § .26 0.36 § .38 0.23 § .28 0.31 § .07 0.19 § .26 0.33 § .23 0.21 § 0 0.30 § .19 0.26 § .23 0.30 § .19 0.35 § .25 0.63 § 0.07 29.2 § 19

0.35 § 0.25 25 § 0

0.25 § .43 0.31 § .28 0.23 § .23 0.24 § .43 0.35 § .25 0.28 § .28 0.26 § .47 0.26 § .28 0.25 § .25 0.29 § .23 0.38 § .38 0.36 § .28 0.35 § 0 41.7 § 14.4

Note: S, standard isolate; C, clinical isolate.

3.2.3. Maximum bactericidal/fungicidal concentration (MBC/MFC) Results of MBC/MFC were on the same line as MIC. The values obtained for MBC were at least the double of the counterpart MIC which suggests the bactericidal nature of NPs. Optimum MBC was obtained for 10% Fe-doped ZnO NP against B. subtilis (S) (0.14 § 0.43 mg/ml) followed by 10% Mn against S. typhi (S) (0.17 § 0.28 mg/ml). Several investigations have suggested the possible mechanisms involving the interaction of NPs with the biological macromolecules. The production of H2O2 from the surface of ZnO is considered as an effective means for the inhibition of bacterial growth.[59] Another possible mechanism is the release of Zn2C ions, resulting in the damage of the bacterial membrane and direct cellular internalisation of ZnO NPs.[60] A recent study suggested the generation of ROS by ZnO NPs may lead to oxidative stress and lipid peroxidation, and as a result NPs get internalised resulting in oxidative DNA damage.[61] NPs are known to deactivate cellular enzymes and DNA by coordinating with the electrondonating groups such as carboxylates, amides, imidazoles, indoles, hydroxyls and so forth. They create pits in bactericidal cell walls, leading to increased permeability and eventually the cell death.[62] The metal ion-based nanomaterials exhibit broad-spectrum biocidal activities towards different bacteria, fungi and viruses.[63] Previous studies of NPs have shown that the greater the size of NPs, the greater the efficacy in inhibiting the growth of bacteria, involving both the production of ROS and the accumulation of NPs.[64] The high rate of generation of surface oxygen species from ZnO leads to the death of the bacteria once it kills/captures the bacteria. The ZnO NPs presumably remain tightly adsorbed on the surface of the leftover/dead bacteria preventing further antibacterial action. However, ZnO NPs continue to release peroxides into the medium

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even after the surface of the dead bacteria is completely covered by ZnO NPs, thereby showing high bactericidal efficacy.

4. Conclusions As clear from the results that a higher percentage of doping leads to a significant rise in antimicrobial potential, still higher content of metal ion doping (including Fe, Mn and others) needs to be studied further. However, based on the findings of present studies, it cannot be denied that Fe-doped ZnO possess an enormous potential as an antimicrobial agent and therefore can be pursued as an important candidate for future studies.

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Acknowledgements The authors are grateful to Shoolini University, Department of Biotechnology, Bajhol, Solan, Himachal Pradesh, India, for support and institutional facilities.

Disclosure statement No potential conflict of interest was reported by the authors.

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