Preparation of antimicrobial gold and silver nanoparticles from tea leaf extracts

Accepted Manuscript Title: Preparation of Antimicrobial Gold and Silver Nanoparticles from Tea Leaf Extracts Authors: Satoaki Onitsuka, Toshiyuki Hamada, Hiroaki Okamura PII: DOI: Reference:

S0927-7765(18)30666-0 https://doi.org/10.1016/j.colsurfb.2018.09.055 COLSUB 9658

To appear in:

Colloids and Surfaces B: Biointerfaces

Received date: Revised date: Accepted date:

11-5-2018 10-9-2018 21-9-2018

Please cite this article as: Onitsuka S, Hamada T, Okamura H, Preparation of Antimicrobial Gold and Silver Nanoparticles from Tea Leaf Extracts, Colloids and Surfaces B: Biointerfaces (2018), https://doi.org/10.1016/j.colsurfb.2018.09.055 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

This manuscript includes 4787 wards, 6 figures, and 2 tables.

Title: Preparation of Antimicrobial Gold and Silver Nanoparticles from Tea Leaf Extracts

Authors: Satoaki Onitsuka*, Toshiyuki Hamada, and Hiroaki Okamura

Affiliations: Department of Chemistry and BioScience, Graduate School of Science and

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Engineering, Kagoshima University, 1-21-35 Korimoto, Kagoshima 890-0065, Japan

Corresponding Author: Satoaki Onitsuka. Department of Chemistry and BioScience, Graduate

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School of Science and Engineering, Kagoshima University, Korimoto 1-21-35, Kagoshima 8900065, Japan; Tel: +81-99-285-8115; Fax: +81-99-285-8115; E-mail: [email protected]

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Graphic Abstract

Highlights •

Gold and silver nanoparticles were synthesized using Camellia sinensis extracts.

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Stable Au and Ag NPs were obtained by the extracts derived from used tea products.

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NP-dyed cotton cloths had a strong antimicrobial activity against the bacteria.

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Abstract: Gold and silver nanoparticles were prepared from the green tea and black tea extracts of the leaves of Camellia sinensis. The metal nanoparticle solutions were obtained by reacting HAuCl4 or AgNO3 aqueous solutions with aqueous NaHCO3 and tea leaf extracts, which were

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obtained from used tea leaves at low temperature, under ambient conditions. The nanoparticles were stable at room temperature and had a uniform particle size (Au: ~10 nm, Ag: ~30 nm).

Nanoparticle-immobilized cotton cloths were then prepared, which displayed high antibacterial activity and a characteristic color, thereby showing potential application as antimicrobial

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pigments. This study provides a means of utilizing used tea leaves, which would otherwise be

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considered waste products.

1. Introduction

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Antimicrobial activity

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Keywords: Gold nanoparticles; Silver nanoparticles; Camellia sinensis; Tea products;

Tea is one of the oldest and most widely consumed beverages in the world. Although there are many varieties of tea products, all of them are made from leaves, leaf buds, and leaf stalks of

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the plant Camellia sinensis. Two major varieties of C. sinensis, var. sinensis and var. assamica, are grown for commercial use. Green tea is made predominantly from C. sinensis var. sinensis, while

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black tea is made from either variety. Tea leaves contain a number of biologically active organic compounds such as polyphenols, tannins, caffeine, proteins, and amino acids [1–4]. Polyphenols, particularly flavonoids such as

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catechins, comprise 30% of the dry weight of fresh tea leaves [5]. Although the total polyphenol content in green tea and black tea is similar, the compounds differ due to varying degrees of oxidation. Compounds in green tea exhibit lower oxidation levels due to the inhibition of oxidase activity upon heating. However, compounds in black tea are completely oxidized, e.g., catechins are oxidized to theaflavins and thearubigins. Consequently, catechins constitute 80%–90% of the total flavonoid concentration in green tea. In contrast, catechins in black tea constitute only

20%~30% of the total flavonoid concentration, while theaflavins and thearubigins account for 10% and 50%~60% thereof, respectively. The flavonoid content is of significance as this class of compounds exhibits antioxidant, antibacterial, and antiviral activities, which are well established in the literature [6, 7]. Indeed, various commercially available hygiene products contain green tea essence as the high flavonoid content imparts antibiotic and odor-eliminating properties.

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Metal nanoparticles (NPs) have different physical properties from bulk metal, metal ions, and metal atoms. Gold and silver NPs are of particular interest due to the ease of preparation and

interesting optical properties. There are two methods for the preparation of metal NPs: 1)

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destruction of bulk metal; 2) synthesis from metal atoms, clusters, and smaller particles. Au NP

colloidal solutions are obtained by reduction of Au(III) particles, followed by protection of the metal surface with a surfactant, and they show a red color based on the surface plasmon resonance absorption. In addition, functional Au NPs are accessible by ligand exchange reactions

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with functionalized molecules, and can be used as optical materials, sensors [8–12], catalysts [13,

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14], etc. Similarly, Ag NP colloidal solutions are obtained from Ag(I), using alcohols and amines as the reducing and/or the protecting agents. However, many of the surfactants and reactants

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employed in these procedures are harmful to humans and the environment, and thus, a “green”

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preparation method for metal NPs is required.

Interestingly, green and black tea extracts contain both a reductant and a surfactant, so they

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have been used in the “green” preparation of metal NPs. Recently, some examples using a variety of tea extracts of C. sinensis have been reported [15–19]. Vilchis-Nestor et al. have reported the preparation of Au and Ag NPs using green tea aqueous extracts under ambient conditions and in the absence of harmful chemicals and solvents [20]. Microwave irradiation is also effective in

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the rapid synthesis of Au [21] and Ag [22] NPs. In another study, green tea extracts have been used in the preparation of Ag NPs, which are employed in the colorimetric sensing of cysteine

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[23]. Ag NPs prepared from green tea extracts display antibacterial activity [24–26], yet are nontoxic to human and mouse cells [26]. Similarly, black tea aqueous extracts have been used in the preparation of Au [27] and Ag [27–30] NPs. In these reactions, the black tea extracts also

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serve as both a reductant and a surfactant under ambient conditions. Begum et al. suggested that the main biomolecules responsible for the synthesis of the NPs are polyphenols or flavonoids in the tea leaf [27]. Moulton et al. investigated the production of Ag NPs using pure (–)-epicatechin, a kind of tea flavonoids, in the much same way as black tea extracts [28]. They also confirmed that the Ag NPs are nontoxic, as determined during the evaluation of mitochondrial function to assess cell viability and membrane integrity in human keratinocytes.

Oolong tea [31], a semi-fermented Chinese tea, and Pu-erh tea, [32], a microbial fermented Chinese tea, have also been used in the synthesis of Ag NPs. The author’s group works toward the development of functional nanomaterials by the assembly of functional organic molecules onto metal NPs. In this paper, a highly reproducible preparation method for stable Au and Ag NPs, using green and black tea extracts, is reported. The reported

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method is characterized by the use of tea leaf waste at low temperatures. The resulting NPs, which displayed antimicrobial activity, were immobilized on the cotton cloths. The dyed cloths

also displayed strong antimicrobial activity against the bacterial strains Staphylococcus aureus

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and Klebsiella pneumoniae. It was expected the increase in functionality due to the assemblage of functional compounds derived from tea extracts on NPs surface.

2. Experimental

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2.1. General

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Hydrogen tetrachloroaurate(III) tetrahydrate HAuCl4•4H2O was obtained from Kanto Chemical Co., Inc. and used as received. Silver nitrate AgNO3, and solvents were purchased from FUJIFILM

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Wako Pure Chemical, Ltd. and used as such. Deionized water was used throughout this

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investigation and was produced using a G-10C unit (Organo Corporation). Green tea was purchased from Sawadaen, Co., Ltd., Japan. Black tea was purchased from Mitsui Norin Co., Ltd.,

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Japan. Bleached cotton cloths were purchased from Daiei Co. Ltd., Japan. UV-Vis absorption spectra were recorded on a JASCO V-550 using a glass cell with a path length of 1 mm. Transmission electron microscopy (TEM) images of NPs were obtained by using a JEOL JEM-2100F. Scanning electron microscope (SEM) images were obtained by using a HITACHI High-

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Technologies SU-70. The size distribution histogram and the average particle diameter were

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obtained by measuring about 200 particles in each of these samples.

2.2. Preparation of tea extracts Green tea water extracts were prepared by adding 50 g of green tea leaves to 500 mL of water

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and allowing them to infuse for over 24 h at ~0 °C in the refrigerator. Filtration through filter paper afforded the 1st extract. An additional 500 mL of water was added to the collected used tea leaves, under the same conditions. Subsequent filtration afforded the 2nd extract. The procedure was repeated three times to afford the 3rd, 4th, and 5th extracts. Black tea water extracts were obtained using an analogous approach. Similarly, green and black tea alcohol extracts were obtained using the aforementioned protocol, but water was replaced with an

alcohol. Methanol and ethanol were used as extracting solvents.

2.3. Synthesis of Au and Ag NPs Method A: To a solution of the tea extract (900 µL) was added 10 mM aqueous HAuCl4 solution (100 µL) at ambient temperature, affording the Au NPs with a final metal concentration of 1 mM.

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Method B: To adjust the pH of the solution, aqueous NaHCO3 solution was added to the reaction mixture. To a mixture of a 10 mM aqueous NaHCO3 solution (800 µL) and the tea extract (1 mL) was added 10 mM aqueous HAuCl4 solution (200 µL) at ambient temperature. The final metal

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concentration was 1 mM.

Ag NPs were synthesized using methods A and B, but HAuCl4 was replaced with a 10 mM aqueous AgNO3 solution.

Samples for TEM imaging were prepared by drying a drop of the NP solutions on carbon-coated

2.4. Dyeing of cotton cloths using Au and Ag NPs

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copper grids at room temperature.

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The bleached cotton cloths were sterilized in boiling water and dried before use. To a mixture of

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10 mM aqueous NaHCO3 solution (80 mL) and 100 mL of each tea extract was added 10 mM aqueous HAuCl4 or AgNO3 solution (20 mL) at ambient temperature. Immediately afterwards,

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three sheets of A4-size cotton cloths were dipped in the NP colloid solutions for over 24 h at ambient temperature and then air-dried. Subsequently, the cloths were washed with water, dried again, and dyed with a mixed color of NPs and tea products. Samples for SEM imaging were prepared by drying a drop of the NP solutions on carbon

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conductive adhesive tape at room temperature. In addition, a fiber which was sleaved the dyed

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cotton cloth was applied to a carbon conductive adhesive tape and a SEM image was taken.

2.5. Antimicrobial activity of NP-dyed cotton cloths Antimicrobial fabric tests on the dyed cloths were conducted according to the JIS L 1902:2008

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method [33] and commissioned to the Japan Food Research Laboratories. Test and control samples were cut into the recommended amount of 0.4 g of dyed cloth which was sterilized by autoclaving. S. aureus (NBRC 12732) and K. pneumoniae (NBRC 13277) were used as Grampositive and Gram-negative test bacteria, respectively. The test bacteria were grown in a liquid culture medium. The inoculum with 105 cells/mL was standardized by dilution in a 1:20 nutrient broth. Test and control samples were inoculated with the test bacteria, in triplicate, and then

placed in a sealed vial in an incubator for 18 h at 37 °C. The viable bacteria counts were determined immediately after inoculation and following incubation.

3. Results and discussion 3.1. Characterization of NPs

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In previous studies [20–32], the extracts were obtained by boiling the tea leaves in water, and the fresh extracts were then used in the synthesis of NPs. However, the use of such extracts in

Method A (for both green tea and black tea), led to the formation of a black precipitate,

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(although the solution turned a characteristic color, based on the surface plasmon resonance of

both Au and Ag NPs). It has been suggested that this is due to the presence of compounds that cause aggregation, and the extraction of these compounds must therefore be avoided. When the extraction temperature was reduced, the stability of the NPs was improved. Various

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extraction conditions were tested, revealing that the extracts prepared at 0 °C, yielded the most

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stable NPs for all tea products and metal sources. Surprisingly, the stability of the NPs increased with each latter of the extraction. This result suggested that a highly soluble compound in tea

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leaves causes aggregation of NPs, while tea leaves contain large amounts of essential compounds

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for NP preparation. The extraction conditions are important from the perspective that they also affect the antioxidant properties and taste of the tea extracts [34–36]. In addition, Tsai et al.

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revealed that green tea leaf waste is a good source of useful catechins [37]. Üstündağ et al. also evaluated the value-added potential of black tea waste as a source of antioxidant and antimicrobial phenolic compounds [38]. In this study, it was revealed that waste tea leaves are useful source reagent for the preparation of metal NPs. The pH levels in the reaction mixture

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were controlled by the aqueous NaHCO3 solution, which also served to reduce the reaction time and enhance the stability of the NPs.

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In the synthesis of the Au NPs using green tea water extract under the optimized conditions in Method B, the color of the reaction mixture immediately turned red (Fig. 1a, solid line). The TEM image of the Au NP colloidal solutions showed the formation of spherical Au NPs with a uniform

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particle size of 8.5 ± 2.5 nm (Fig. 2a). The use of 10 mM aqueous AgNO3 solution yielded the Ag NP colloidal solutions under the same conditions (Fig. 1b, solid line), with a larger particle size of 18.9 ± 4.4 nm (Fig. 2b).

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Fig. 1. UV-Vis absorption spectra of NPs. a) Au NPs from green tea water extract (solid line) and black tea water extract (dashed line). b) Ag NPs from green tea water extract (solid line) and

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black tea water extract (dashed line).

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rate of particle size (%)

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Fig. 2. TEM images and corresponding size distribution histograms of NPs. a) Au NPs from green

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tea water extract. b) Ag NPs from green tea water extract.

In the case of black tea water extracts, Method B using the 3rd extract also yielded the corresponding Au and Ag NP colloidal solutions (Fig. 1, dashed line) with a uniform particle size

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of 11.0 ± 4.2 nm or 34.4 ± 9.6 nm, respectively (Fig. 3c and d). Black tea or AgNO 3 produced larger NPs compared to green tea or HAuCl4. It is noteworthy that all NP colloidal solutions were stable for more than a month, in addition to being condensable and redispersible. In fact, these NPs solutions were storable in a refrigerator, and UV-Vis absorption spectra of the stored solutions were hardly any change.

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tea water extract. d) Ag NPs from black tea water extract.

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Fig. 3. TEM images and corresponding size distribution histograms of NPs. c) Au NPs from black

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Although alcohols are a kind of harmful solvent, methanol and ethanol were also used as

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extraction solvents. In this case, the above-described method may be applicable to the preparation of Au and Ag NPs. However, the characteristic colors based on the surface plasmon

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resonance of the NPs were difficult to determine in the absorption spectra. This was due to the masking of the plasmon absorption band of the NPs by the absorption band of the pigments (such as chlorophylls or theaflavins) in the tea products. TEM analysis of the prepared NP colloidal solutions revealed the formation of spherical NPs (Fig. 4 and 5). From the 5th green tea

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methanol extract, Au and Ag NPs were obtained with sizes of 11.5 ± 3.4 nm and 17.5 ± 7.1 nm, respectively (Fig. 4e and f). The 3rd black tea-methanol extract gave Au and Ag NPs having sizes

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of 10.8 ± 2.9 nm and 12.1 ± 5.9 nm, respectively (Fig. 5g and h). In this case, the size and particle size distribution of the Ag NPs was larger than those of the Au NPs. All the colloidal solutions

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prepared using alcohol extracts also possessed high stability.

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diameter (nm) rate of particle size (%)

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Fig. 4. TEM images and corresponding size distribution histograms of NPs. e) Au NPs from green

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tea MeOH extract. f) Ag NPs from green tea MeOH extract.

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Fig. 5. TEM images and corresponding size distribution histogram of NPs. g) Au NPs from black tea MeOH extract. h) Ag NPs from black tea MeOH extract.

3.2. Antimicrobial activity of NP-dyed cotton cloths Since ancient times, the microbicidal activities of silver and green tea catechins have been known. Therefore, it was envisaged that the prepared NPs would possess dual functionality, derived from

both the metal and tea product. Thus, the antibacterial activity of the NPs was established. Bleached cotton cloths were dyed using the NP colloidal solutions, and they displayed the colors of the NPs and the pigments in the tea products. The attachment of Au and Ag NPs on the cloths was confirmed by SEM. SEM images of Ag NPs with green tea extract also showed the generation of Ag NPs (Fig. 6i). The size and particle size distribution of the NPs, as determined by SEM, were

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similar to the results of TEM. In addition, the attachment of Ag NPs on the cloth was verified by SEM images of the cotton fiber that had been dyed with the Ag NPs solution (Fig. 6j). In this case,

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Ag NPs of the same size as in the colloidal solution were observed.

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Fig. 6. SEM images of NPs. i) Ag NPs from green tea water extract. j) Ag NPs on the cotton fiber.

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The antimicrobial fabric test of the dyed cloths was conducted according to the JIS L 1902:2008 method against S. aureus (NBRC 12732) and K. pneumoniae (NBRC 13277) as Gram-positive and

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Gram-negative bacteria, respectively. In the test against S. aureus, all samples displayed high antimicrobial activity (Table 1). In the examination against K. pneumoniae (Table 2), most samples displayed high antimicrobial activity except for Au NPs with black tea (entry 7). Since antimicrobial activity of NPs is strongly dependent on the size, the smaller dimensions of

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Ag NPs (<30 nm) imparts high activity against S. aureus and K. pneumoniae [39]. Sankar et al. reported that the silver nanopowder (commercially available product) incorporated in cellulose

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pulp has antimicrobial activity [40], however, our products displays higher antimicrobial activity. It was suggested that this was due to the assembly of functional organic molecules such as polyphenols, obtained from tea extracts, onto the NP surface.

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In contrast, Au is considered an inert material in a biological sense. Au NPs are also highly biocompatible and do not display acute cytotoxicity [41]. Green and black teas have antimicrobial activity against S. aureus and show the minimum inhibitory concentration (MIC) of 0.07% and 0.31%, respectively [42]. The activity is mainly attributed to the polyphenols found in tea. In fact, the MIC value of epigallocatechin gallate, the main constituent of tea catechins, is 50~100 μg/mL [43]. However, the extracts and compounds are inactive against Gram-negative

bacteria such as K. pneumoniae [42, 43]. Amazingly, the resultant Au NPs from green tea killed the inoculated bacteria almost entirely (Table 2, entries 3, 5). This may seem surprising, given that the concentration of the antimicrobial compounds in the tea extracts is very small and not sufficient this activity. The observed potent biological activity of the dyed cotton cloths could be attributed to an unusual synergistic effect of the assembled functional organic molecules on the

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surface of the NPs.

4. Conclusions

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We have developed a simple method for the preparation of Au and Ag NPs using the botanical

extracts derived from tea products. In this method, control of extraction conditions is more important, regardless of the tea products. In addition, the resultant NPs can serve as antimicrobial pigments, thus showing scope for application in functional hygiene products. This

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methodology allows for the effective utilization of the nutrients present in used tea leaves.

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Studies are underway to expand the scope of these botanical extracts and to explore their

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ACKNOWLEDGMENT

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application as functional nanomaterials.

We are grateful to Takeshi Tanaka, Evaluation Center of Materials Properties and Function,

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Institute for Materials Chemistry and Engineering, Kyushu University, for the photographing of TEM images. We thank Dr. Tsuyoshi Sawada and Shingo Kubo, Division of Instrumental analysis, Research Support Center, Kagoshima University, for technical support. We also thank Hajime Simodozono, Shimodozono Co., Ltd., Japan, for technical advice. This work was supported by the

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Grants-in-Aid for Scientific Research (No. 23350021, No. 26410096, and No. 17K05838) from the Ministry of Education, Culture, Sports, Science and Technology, Japan, by the Cooperative

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Research Program of the “Network Joint Research Centre for Materials and Devices” (No. 2011287, 2014440, 20161260, 20171299, and 20181302), and public foundation Yonemori-

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Seishinikuseikai, Japan.

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sample solvent

metal

1

2

6.3 × 104

5.1 × 104

control

2b

green tea

H2O

Ag

<20

<20

3b

green tea

H2O

Au

<20

<20

4b

green tea

MeOH

Ag

<20

5b

green tea

MeOH

Au

<20

6b

black tea

MeOH

Ag

<20

7b

black tea

MeOH

Au

8b

control

3 4.7 × 104 <20 <20

SC R

1a

U

material

test institution

IP T

entry

<20

<20

<20

<20

<20

<20

<20

<20

1.7 × 107

9.9 × 106

1.5 × 107

A

N

<20

Immediately after inoculation. b After 18 h. <20: undetected.

A

CC

EP

TE D

a

M

Table 1. Viable cell counts of samples in the antimicrobial fabric test for Staphylococcus aureus

entry

sample material

solvent

test institution metal

1

2

3

3.1 × 104

2.7 × 104

2.9 × 104

control

2b

green tea

H2O

Ag

<20

<20

<20

3b

green tea

H2O

Au

<20

<20

<20

4b

green tea

MeOH

Ag

<20

<20

5b

green tea

MeOH

Au

<20

<20

6b

black tea

MeOH

Ag

<20

<20

7b

black tea

MeOH

Au

2.1 × 107

2.6 × 107

2.3 × 107

8b

control

3.4 × 107

3.8 × 107

3.3 × 107

IP T

1a

A

CC

EP

TE D

M

A

Immediately after inoculation. b After 18 h. <20: undetected.

<20 <20

SC R

U

N

Table 2. Viable cell counts of samples in the antimicrobial fabric test for Klebsiella pneumoniae a

<20