Journal of Molecular Liquids 263 (2018) 187–192
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Short Communication
Photocatalytic degradation of organic dyes and antimicrobial activity of silver nanoparticles fast synthesized by flavonoids fraction of Psidium guajava L. leaves Lu Wang, Fangju Lu, Yan Liu, Yanan Wu, Zhenqiang Wu ⁎ School of Biology and Biological Engineering, South China University of Technology, Guangzhou 510006, PR China
a r t i c l e
i n f o
Article history: Received 9 November 2017 Received in revised form 4 April 2018 Accepted 30 April 2018 Available online 02 May 2018 Keywords: Nanocomposites Antimicrobial activity Photocatalytic degradation Psidium guajava L. leaves Flavonoids
a b s t r a c t A novel and ecofriendly procedure was developed for the synthesis of silver nanoparticles (FAgNPs) with the reduction of AgNO3. The flavonoids fractions (FF) of Psidium guajava leaves (PGL) were used as a green reducing and capping agent. Results showed that FF from PGL rapidly could synthesize into regular spheres and stable silver nanoparticles within 10 min. The average particle size of synthesized FAgNPs was 15–20 nm, with maximum absorbance wavelength at 420 nm. Moreover, FAgNPs exhibited a strong inhibition against the selected microorganisms, especially Alcaligenes faecalis, Escherichia coli and Aspergillus niger. Importantly, FAgNPs also possessed good catalytic degradation potency for organic dyes, namely, methyl orange and Coomassie brilliant blue G250, under solar or UV irradiation. Overall, FAgNPs have good potential application prospects in the development of anti-bacterial materials and for the photocatalytic degradation of certain toxic dyes or chemicals, thereby paving the way for waste treatment and environmental bio-remediation. © 2018 Elsevier B.V. All rights reserved.
1. Introduction Psidium guajava L. leaves (PGL), used as herbal tea or a source of functional beverages in many countries, contain various bioactive compounds, including flavonoids, polyphenols, and saponins [1]. In the present work, PGL was used as a renewable bio-resource to produce bio-based functional materials. Nanotechnology is one of the most interesting and challenging fields in biomedical, waste treatment and environmental bioremediation research due to its unique and attractive physiochemical properties. Metal nanoparticles show improved properties based on idiographic characteristics, such as a higher surface-tovolume ratio and small size compared with the bulk material made from metal [2]. Although many conventional methods, such as microwave-irradiation, electro-irradiation, and strong chemical reductants, are used to synthesize nanoparticles, these methods are expensive and employ strong chemical reagents that can be very harmful to human health [3]. Currently, microbial or plant extracts have been developed to synthesize silver nanoparticles. Khamhaengpol and Siri, (2017) reported that using tissue extract of weaver ant larvae, silver nanoparticles could be synthesized within 48 h [4]. Ravichandran et al., (2016) reported the synthesis of silver nanoparticles using Atrocarpus altilis leaf extracts within 24 h [5]. Das et al., (2012) reported
⁎ Corresponding author. E-mail address:
[email protected] (Z. Wu).
https://doi.org/10.1016/j.molliq.2018.04.151 0167-7322/© 2018 Elsevier B.V. All rights reserved.
a green chemical synthesis of silver nanoparticles (AgNPs) through the reduction of silver nitrate by a fungal strain of Rhizopus oryzae with 72 h [6]. These new methods are convenient and ecofriendly but timeconsuming. In the present work, the flavonoids fraction (FF) from Psidium guajava L. leaves (PGL) are reported as promising reductants for the rapidly and eco-friendly synthesis of benign and stable silver nanoparticles. Silver nanoparticles are a relatively new material to be used as antimicrobial agents. The antimicrobial activity of the nanoparticles can be applied for disinfection in waste water treatment factories, to prevent bacterial colonization, to eliminate microorganisms on medical and silicone rubber gaskets and to protect and transport food and textiles. Synthetic organic dyes in waste water are generally released from plastic, paper, leather, cosmetic, textile and pharmaceutical industries. Removing these non-biodegradable organic chemicals from the environment and industrial waste is a challenging problem. Many techniques have been routinely used for degrading dyes, such as activated carbon sorption, electro-coagulation and microbial treatments [7]. However, these techniques show insignificant degradation effects on certain toxic dyes. Recently, silver nanoparticles have been applied in the catalytic degradation of methylene blue and eosin Y [8]. Due to the high surface area of silver nanoparticles, they exhibit a strong degrading activity on dyes [9]. In this study, the antimicrobial activity and the photocatalytic degradation of methyl orange (MO) and Coomassie brilliant blue G250 (CBB G-250) were investigated in the presence of the synthesized FAgNPs.
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2. Materials and methods
2.5. Synthesis and characterization of FAgNPs
2.1. Plant materials and chemicals
Five millilitres of 5 mg/mL separated flavonoids solution (pH = 9) was added to 100 mL of 1 mM AgNO3 solution with stirring at room temperature for 30 min [12–14]. The mixture was centrifuged at 12,000 rpm for 15 min to collect the FAgNPs. The reduction of the Ag+ to Ag0 was monitored at different time intervals using UV–visible spectroscopic analysis in the range of 200 to 700 nm (UV-2802SH, UNICO, Shanghai, China), a scanning electron microscope equipped with energy dispersive X-ray spectroscopy (SEM-EDX), a transmission electron microscope (TEM) (JEM-2100F, JEOL), a Fourier transform infrared spectrometer (FT-IR, Shimadzu, Japan) between 400 and 4000 cm−1 and an X-ray diffractometer (XRD, D8 Advance, Bruker).
Psidium guajava L. leaves (PGL) were provided by Jiangmen Nanyue Guava farmer cooperatives (Guangdong, China). Silver nitrate (AgNO3, N99.8%) were purchased from Tianjin Kemiou Chemical Reagent Co., Ltd. (Tianjin, China). Individual flavonoid standards, Methyl orange (MO), Coomassie brilliant blue G-250 (CBB G-250), Ampicillin, and Penicillin were purchased from Sigma-Aldrich (St. Louis, MO, USA). Formic acid and acetonitrile solvents were purchased from Fisher Scientific (HPLC grade, 99.9%, Waltham, MA, USA). 2.2. Microorganisms The antimicrobial activity of FAgNPs was evaluated using a panel of strains that included laboratory control strains obtained from the School of Biology and Biological Engineering, South China University of Technology. Gram-negative and Gram-positive bacteria, as well as one fungus, were used in the present study. The Gram-negative bacteria included Escherichia coli and Alcaligenes faecalis. The Gram-positive bacteria included Bacillus aryabhattai and Bacillus subtilis. The fungus used was Aspergillus niger. 2.3. Extraction and purification of flavonoids fraction from Psidium guajava L. leaves One hundred grammes of the dried PGL powder was soaked in 1 L ethanol solution (70%, v/v, Tianjin, China) for 1 h. Extraction of composites from the leaf residues was performed using ultra-sound at 320 W for 30 min. The suspension was filtered through filter paper with pore size of 0.45 μm. The crude extracts were evaporated to dryness under vacuum. The separation and purification of the flavonoids fraction was performed using an AB-8 macroporous resin eluted with a gradient of ethanol and water (0:100, 30:70, 50:50, 70:30, 100:0, v/v) [10]. The optimum dynamic adsorption and desorption conditions of AB-8 macroporous resin were as follows: pH value of sample solution was 5, the flow rate was two bed volume (BV)/h and the gradient of ethanol and water was 70:30 (v:v), respectively. The collected eluents, which are a bright yellow transparent solution, were concentrated by rotary evaporation and freeze-dried. The flavonoids fraction (2.4%, w/w) was obtained by this method. 2.4. HPLC-ESI-TOF/MS analysis of flavonoids fraction The flavonoid compounds were identified by HPLC-ESI-TOF/MS method. The HPLC-ESI-TOF/MS system was comprised of an HPLC system (1200, Agilent, Santa Clara, CA, USA) equipped with a diode array detector (Waters 2998, Milford, MA, USA) and an ultra-high resolution TOF mass detector (maXis, Bruker, Billerica, MA, USA). A Zorbax Eclipse Plus C18 column (250 mm × 4.6 mm, 5 μm, Agilent) was used for flavonoid separation with an instant working temperature at 30 °C. The mobile phase included a 0.1% formic acid aqueous solution (v/v, solution A) and a acetonitrile solution (solution B) at a constant flow rate of 0.8 mL/min with the following gradient program: 0–5 min, 15% solution B; 5–10 min, 15–20% solution B; 10–20 min, 20–25% solution B; 20–30 min, 25–35% solution B; 30–40 min, 35–50% solution B; 40–50 min, 80% solution B; and 50–55 min, 15% solution B. Conditions for MS operation were: 4 kV electrospray voltage with temperature, 6.0 L/min N2 flow rate and voltage of 350 °C and ±40 V in the vaporizer. The mass spectra of each peak were recorded in either positive ion mode within the range of the ion abundance from 100 to 1000 (m/z). A dwell time of 500 ms was recorded under a selected ion-monitoring mode. The mass spectra and distribution patterns of ion fragmentation were used for similarity comparison with standardized data [11].
2.6. Antimicrobial activity assays The antimicrobial activity of the FAgNPs was assessed against selected Gram-positive bacteria, Gram-negative bacteria and fungus using the agar well diffusion method [12]. For comparison, the antimicrobial activities of FF and the silver nitrate solution were used as the controls. Ampicillin and Penicillin were used as the positive controls. The antibacterial activity was evaluated by the size of the diameter in the inhibition zone. 2.7. Photo-catalytic activities assays MO and CBB G-250 dyes were selected to evaluate the photocatalytic degradation potency of synthesized FAgNPs. The degradation experiments for MO were performed in a chamber with 8 light tubes (40 W/tube, China, light intensity was 0.015 W cm−2, wavelength around 450 nm). The experiments for CBB G-250 were performed under UV irradiation in a chamber with 2 UV light tubes (40 W/tube, light intensity was 0.02 W cm−2, wavelength around 365 nm). Prior to the experiment, 20 mg of FAgNPs was added to 50 mL of MO or CBB G-250 solution (10 mg/L, Fisher Scientific). The mixture was first stirred constantly for approximately 30 min in darkness to ensure equilibrium of FAgNPs in the organic dye solution. During the reaction, the MO mixture was kept under solar irradiation in a Pyrex glass beaker and stirred constantly for 10 h, and the CBB G-250 mixture was kept under UV irradiation in a Pyrex glass beaker and stirred constantly for 6 h. The absorption spectrum of the mixture was measured periodically using a UV–Vis spectrophotometer (Shimadzu, UV-2450, Japan) after centrifugation to monitor the degradation of MO or CBB G-250 solution. The degradation efficiency of MO or CBB G-250 was calculated based on Eq. (1): Degradation efficiency ð%Þ ¼
C 0 −C t 100 C0
ð1Þ
C0 represented the concentration of dyes before degradation. Ct represented the concentration of dyes after degradation. 3. Results and discussion 3.1. Identification of flavonoid compounds HPLC-ESI-TOF/MS was used to identify the flavonoid components separated from the PGL extracts. During the HPLC-ESI-TOF/MS analyses, the mass error tolerance was 4 ppm, representing a systematic error in the measurements. As shown in Fig. 1A and Table 1, Peak 1 could be confirmed to be rutin based on the parent ion at m/z of 611.4210 [M + H]+ which produced two main ions at 303.0510 [C15H10O7 + H]+ and 465.1002 [C21H20O11 + H]+. Peak 2 was identified as isoquercitrin by the parent ion m/z of 465.1002 [C21H20O12 + H]+ and produced two main ions at 303.0501 [C15H10O7 + H]+ and 163.1221 [M-C15H10O7 + H]+. Three isomers of quercetin glucoside (Peak 3, 4, and 5) were
L. Wang et al. / Journal of Molecular Liquids 263 (2018) 187–192
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7 5 2 34
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40
Time (min)
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Absorbance
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O
OH
O
R1 2 3 4 5 6
R1=rhamnose, R2 =glucose
OH
R1 =glucose R1 =xylopyranose R1 =arabinopyranose R1 =arabinofuranose R1 =rhamnose
HO
HO
OH
O
OH
O
HO
HO HO
O O
7
400
450
500
550
600
650
700
Wavelength (nm)
O
O
R2 1
OH
O
HO
Fig. 2. UV–Vis spectra spectrum of synthesized FAgNPs at different time intervals.
rate of formation of FAgNPs was much higher than that reported previously [4,5], which indicates that FF could be applied as a successful and highly efficient material for synthesis of silver nanoparticles. 3.3. Physicochemical characteristics of FAgNPs
OH
OH
Quercetin
8
Kaempferol
Fig. 1. HPLC chromatograms (A) and the chemical structures (B) of the separated flavonoids fraction from Psidium guajava L. leaves. FSM, Flavonoids standard mixture; SFF, Separated flavonoid fraction. 1 Rutin, 2 Isoquercitrin, 3 Quercetin-3-O-β-Dxylopyranosid, 4 Quercetin-3-O-α-L-arabinoside, 5 Avicularin, 6 Quercitrin, 7 Quercetin, 8 Kaempferol.
characterized by the parent ion m/z of 435.0901 [M + H]+ and produced two main ions at 303.0490 [C15H10O7 + H]+ and 133.2510 [MC15H10O7 + H]+. Based on the standard, peaks 3, 4 and 5 were identified to be quercetin-3-O-β-D-xylopyranoside, quercetin-3-O-α-Larabinopyranoside and avicularin, respectively. Peak 6 can be identified as quercitrin by the parent ion m/z of 449.0984 [C21H20O11 + H]+ and produced the main ion at 303.0501 [C15H10O7 + H]+. Peak 7 was confirmed to be quercetin by the main ion at 303.0501 [C15H10O7 + H]+. Additionally, peak 8 can be identified as kaempferol by the main ion at 287.0234 [C15H10O6 + H]+. The chemical structures of identified flavonoids compounds were presented in Fig. 1B. 3.2. Quick synthesis of FAgNPs A very rapid reaction was observed when the FF and AgNO3 solution were mixed at room temperature. The reaction mixture quickly turned a dark colour within 10 min. The visual observations were confirmed by the UV–vis absorption measurements of the reaction solution. As seen from the spectral recordings, the absorbance feature at 420 nm, indicative of elemental silver, reaches a maximum after 10 min (Fig. 2). The
Fig. 3A displays the FTIR spectra of flavonoids powder and its synthesized FAgNPs. Several characteristic peaks were observed. The flavonoids showed major absorption peaks at 669 cm−1, 1367.78 cm−1, 1657.39 cm−1 and 3349.34 cm−1 corresponding to \\C_C, \\C_O, \\C\\O and \\OH groups' stretching vibration, respectively. The synthesized FAgNPs showed characteristic bands at 670.43 cm−1, 2936.75 cm−1, 1069.31 cm−1, 1321.32 cm−1, 1626.43 cm−1, and 3273.46 cm−1, respectively. On comparing the FTIR spectra of FF and FAgNPs, a shift in the absorption peaks of the \\OH, \\C\\O and \\C_O groups was observed, confirming that the flavonoid compounds capped the FAgNPs surface [15]. The XRD pattern of FAgNPs showed five prominent diffraction peaks at 2θ = 32.89°, 38.63°, 44.82°, 63.45°, and 76.48°, in accordance to the (122), (111), (200), (220), and (311) planes of the face-centred cubic structure (JCPDS file No. 087-0717) of silver, respectively. Based on calculations using the Debye–Scherrer formula, the size of synthesized FAgNPs was estimated to be approximately 20 nm (Fig. 3B). This finding is consistent with the results measured by TEM. The FAgNPs possessed a narrow particle-size distribution of 15 to 20 nm and a low polydispersity index of 0.424 (Fig. 3C). The zeta potential value of FAgNPs was −19.37 mV (Fig. 3D), confirming the reasonable stability of the synthesized silver nanoparticles [16]. The SEM images clearly showed a uniform spherical shape with smooth surface of the synthesized FAgNPs (Fig. 4A). The particles had an average size of 15 to 20 nm, same as the result measured by TEM (Fig. 4B). The purity and composition of the FAgNPs, as analysed by EDX, showed high characteristic signals of elemental Ag in FAgNPs at approximately 3 keV followed by C and O (Fig. 4C). The C and O element signals may be attributed to the flavonoids compounds covering the
Table 1 Identification of flavonoids compounds of PGL using HPLC-TOF-ESI/MS method. Peak No.
Retention time (min)
λmax (nm)
Molecular ion (m/z)
MS2(m/z)
Mw
Compounds
Reference
1 2 3 4 5 6 7 8
16.15 17.82 19.39 20.15 20.79 21.59 33.15 38.21
256, 354 254, 360 256, 356 257, 356 257, 353 256, 351 254, 371 254, 365
611.4210 [M + H]+ 465.3610 [M + H]+ 435.0901 [M + H]+ 435.0930 [M + H]+ 435.0940 [M + H]+ 449.1098 [M + H]+ 303.0516 [M + H]+ 287.0891 [M + H]+
465.1002, 303.0510, 309.1121 303.0501, 163.1221 303.049, 133,1412 303.0509,133.2510 303.0511 303.0512, 147.1232 303.0516 287.0891
610 465 434 434 434 448 302 286
Rutin Isoquercitrin Quercetin-3-O-α-L-arabinofuranoside Quercetin-3-O-β-D-xylopyranoside Avicularin Quercitrin Quercetin Kaempferol
Standard Standard Standard Standard Standard Standard Standard Standard
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their activity, ultimately killing the bacteria. Due to the different properties of the cell wall structure, such as thinner peptidoglycan layer of Gram-negative bacteria, silver nanoparticles can more easily reach the cytoplasm or interact with the cell membrane, causing damage of the membrane or proteins [19]. Hence, Gram-negative bacteria were observed to be significantly more sensitive to the silver nanoparticles than were the Gram-positive bacteria (p b 0.05).
surface of FAgNPs. The possible synthesis pathway of FAgNPs is shown in Fig. S1 [17]. 3.4. Antimicrobial activity As observed in Fig. 5, FF does not exhibit any inhibitory activity against selected strains compared to AgNO3 or FAgNPs. FAgNPs exhibited improved antibacterial activity against the selected strains, leading to larger clear zones on the plates. Although AgNO3 also exhibited strong inhibition against the selected strains, AgNO3 cannot be widely applied in biomedical or waste water treatment fields due to its high toxicity. Silver nanoparticles showed improved properties based on idiographic characteristics, such as higher surface-to-volume ratio and small size, compared with the AgNO3 solution. A 100 μg/mL dose of FAgNPs exhibited a good inhibitory activity against A. faecalis and A. niger. It showed no significant difference in antimicrobial activity against E. coli compared with the same concentration of ampicillin (p = 0.137). However, compared with the same concentration of penicillin, FAgNPs displayed significant difference in antimicrobial activity against A. niger, (p b 0.05). Based on the results described by Wang et al. (2018), with the increasing of the concentration of AgNPs, the antimicrobial activity against A. niger was significantly improved [18]. A few studies have established the antimicrobial mechanisms of chloramphenicol, aminoglycosides, tetracyclines, penicillin and glycopeptides. However, regarding the antimicrobial mechanism of silver ions or silver nanoparticles, no consistent basis has been accepted. Previous studies have demonstrated that AgNPs could strongly bind to proteins, different enzymes and non-enzyme proteins, including chaperones, porins, or periplasmic peptide-binding proteins, thereby inhibiting their activities [16]. FAgNPs probably bind to the cellular and membrane proteins following transportation through the compromised cell wall and inhibit
A
Fig. 6A presents the UV absorption spectra for degradation of MO by solar irradiation in the absence of FAgNPs. The maximum absorption peak of MO was found to appear at 464 nm. This maximum absorption peak at 464 nm decreased gradually with the extension of exposure time under solar irradiation. From Fig. 6B, it can be concluded that the blank experiments performed with solar irradiation in the absence of any FAgNPs did not show degradation ability of MO. Control experiments performed with FAgNPs in the dark exhibited nearly no change in degradation of MO. As demonstrated, FAgNPs possess good catalytic degradation potency for MO under solar irradiation. Fig. 6C shows the UV absorption spectra of CBB G-250 by UV irradiation in the absence of FAgNPs. The characteristic absorption peak of CBB G-250 at 585 nm was used for monitoring the catalytic degradation process. With the extension of exposure time, the UV absorption spectra of CBB G-250 at 585 nm showed a progressive decline. From Fig. 6D, it can be observed that the degradation of CBB G-250 did not progress with UV irradiation in the absence of FAgNPs. Experiments performed with FAgNPs without UV irradiation displayed nearly no change in degradation rate of CBB G250. Importantly, the experiments performed with FAgNPs and UV irradiation possessed good catalytic degradation potency for CBB G-250. Ghosh et al. (2002) reported that silver nanoparticles can act as efficient
B
100
2400
(111)
2000
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3349.34
1367.78
Flavonoids FAgNPs
670.43
30
Intensity (counts)
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3273.46
50
2936.75
60
1657.39
70
1321.32
669.37
80
1626.43
1087.57
90
1069.31
% Transmitance
3.5. Photo-catalytic activity on degradation of organic dyes
1600
(122)
1200 (200)
800
(220)
0 10
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C 14
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12 10 8 6 4 2 0 0.1
(311)
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Size (d, nm) Fig. 3. (A) XRD pattern, (B) FTIR spectra, (C) size distribution and (D) zeta potential analysis of synthesized PAgNPs.
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A
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6 Ag
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3 Ag
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Fig. 4. SEM micrographs (A), TEM micrographs (B) and EDX spectrum of synthesized FAgNPs (C).
photocatalysts through the electron transfer process due to their large surface area [20]. The UV/solar irradiation struck the valence electrons of FAgNPs, they gained energy and emitted from the valence shell. After emission these highly energetic electrons are used in generation of hydroxyl radicals which are responsible for decomposition of dyes [21–24]. The possible mechanism for degradation of dyes by FAgNPs could be proposed as follows: (1) Efficient absorption of photons by the synthesized F-AgNPs:
hv þ FAgNPs
solar or UV irradation
þ hv
−
þe
Coomassie brilliant blue G-250. These findings suggest that flavonoidmediated synthesized silver nanoparticles can not only prevent microbial colonization but also catalytically degrade toxic or harmful chemical dyes in the presence of solar or UV irradiation, possibly representing a new and efficient method for environmental remediation. Supplementary data to this article can be found online at https://doi. org/10.1016/j.molliq.2018.04.151. Acknowledgements This work was supported by the Science and Technology Project of Guangdong Province, China (2016A020210011 and 2017B020207003) and the Agricultural Science and Technology Research Project of Jiangmen City, China (20150160008347).
(2) Releasing of OH• radicals
þ
hv þ H2 O→OH
(3) Degradation of the organic dyes by successive attack by the OH• radicals
MO þ OH →Hydrazine derivatives þ H 2 O CBB G−250 þ OH →Degradation products þ H2 O
Zone of inhibition (mm)
þ
hv þ OH− →OH
30
Ampicillin
Penicillin
*
**
**
20
*
15 10 5
1 B. aryabhattai
2 B. subtilis
Gram-positive FAgNPs were synthesized rapidly and in an eco-friendly manner by adopting flavonoid compounds from PGL at room temperature and within 10 min of incubation. The FAgNPs possessed good antimicrobial activity and photocatalytic degradation effect on methyl orange and
FAgNPs
25
0 4. Conclusions
AgNO3
FF
3 A. faecalis
E. 4coli
Gram-negative
A. niger 5
Fungus
Strains Fig. 5. Antimicrobial activity of the synthesized FAgNPs. Levels of statistical significance are compared FAgNPs with antibiotic and AgNO3 (*p b 0.05, **p b 0.01, n = 4).
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B
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0h
6h
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0h 0.5 h 1h 3h 6h 10 h
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MO+FAgNPs+Solar irradiation MO+FAgNPs+dark MO+Solar irradiation
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60 50 40 30 20 10 0
450
500
550
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0
1
2
3
4
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Fig. 6. (A) UV–Visible absorption spectra and (B) photocatalytic activity effect of solar irradiation time on degradation of methyl orange (MO); UV–visible absorption spectra (C) and photocatalytic activity effect (D) of UV irradiation time on degradation of Coomassie brilliant blue G-250 (CBB G-250). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)
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