Ipomea carnea-based silver nanoparticle synthesis for antibacterial activity against selected human pathogens

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Ipomea carnea-based silvernanoparticle synthesis for antibacterialactivity against selected humanpathogensS.C.G. Kiruba Daniel a , B. Nazeema Banu b , M. Harshiny c , K.Nehru d , P. Sankar Ganesh b , S. Kumaran b & M. Sivakumar aa Department of Nanoscience and Technology, Anna University ofTechnology, Tiruchirappalli 620 024, Indiab Department of Biotechnology, Periyar Maniammai University,Vallam, Thanjavur 613 403, Indiac Division of Nanotechnology, Department of Electronics andCommunication Engineering, Periyar Maniammai University,Vallam, Thanjavur 613 403, Indiad Department of Chemistry, Anna University of Technology,Tiruchirappalli 620 024, India

Version of record first published: 02 Jul 2012

To cite this article: S.C.G. Kiruba Daniel, B. Nazeema Banu, M. Harshiny, K. Nehru, P. SankarGanesh, S. Kumaran & M. Sivakumar (2012): Ipomea carnea-based silver nanoparticle synthesis forantibacterial activity against selected human pathogens, Journal of Experimental Nanoscience,DOI:10.1080/17458080.2011.654274

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Journal of Experimental Nanoscience2012, 1–13, iFirst

Ipomea carnea-based silver nanoparticle synthesis for antibacterial activity

against selected human pathogens

S.C.G. Kiruba Daniela, B. Nazeema Banub, M. Harshinyc, K. Nehrud, P. Sankar Ganeshb,S. Kumaranb and M. Sivakumara*

aDepartment of Nanoscience and Technology, Anna University of Technology, Tiruchirappalli 620 024,India; bDepartment of Biotechnology, Periyar Maniammai University, Vallam, Thanjavur 613 403, India;cDivision of Nanotechnology, Department of Electronics and Communication Engineering,Periyar Maniammai University, Vallam, Thanjavur 613 403, India; dDepartment of Chemistry,Anna University of Technology, Tiruchirappalli 620 024, India

(Received 20 July 2011; final version received 25 December 2011)

The biosynthesis of silver nanoparticles (AgNps) has a wide range of applications, and here wedevelop a rapid synthesis using the leaf extract of Ipomea carnea. We demonstrated that 100mLof a 1mM silver nitrate solution was reduced to AgNps by 500 mL of I. carnea extract in 5minand that one or more of the chemical constituents present in the extract acted as the reducingagent. Surface plasmon resonance peaks were observed from 410 to 440 nm for AgNpssynthesised using the plant extract, and the peaks showed a characteristic blue shift with variationof pH from 2 to 8. Particle size analysis revealed the size of the AgNps to be from 30 to 130 nm,which was also confirmed by dynamic light scattering, atomic force microscopy and transmissionelectron microscopy. Additionally, the antibacterial effects of the AgNps were evaluated againstselected human pathogens such as Staphylococcus aureus, Bacillus cereus, Bacillus subtilis,Klebsiella pneumoniae, Aeromonas hydrophila, Salmonella typhi, Proteus vulgaris andPseudomonas aeruginosa. Finally, the AgNps were impregnated with a cellulose acetatemembrane to form an antimycobacterial membrane. Antimycobacterial activity against a non-pathogenic Mycobacterium smegmatis showed that the AgNp-embedded membrane system has azone of inhibition of 14mm.

Keywords: silver nanoparticles; Ipomea carnea; cellulose acetate membrane; antibacterial activity

1. Introduction

Nanoparticles are being studied for many applications, including biosensors, labels for cells andbiomolecules, anti-microbial agents and cancer therapeutics [1–4]. Silver nanoparticles havewide industrial applications in electrocatalysis, chemical sensors, catalysis and optical devices[5–8]. Recently, the synthesis of silver nanoparticles has been reported using several methods:such as chemical, gamma-irradiation, thermal decomposition, photochemical and biosyntheticusing microbes and plant resources [9–13].

Ipomea carnea is a fast-growing noxious weed of negligible economic value. However, itpossesses polyphenols and alkaloids that can be utilised as reducing agents in the synthesis ofnanoparticles. The antimicrobial properties of nanoparticles are well established, and amechanism of inhibition has been proposed by several researchers [14–17]. Silver is used

*Corresponding author. Email: [email protected]; [email protected]

ISSN 1745–8080 print/ISSN 1745–8099 online

� 2012 Taylor & Francis

http://dx.doi.org/10.1080/17458080.2011.654274

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traditionally as a disinfecting agent in medicine and as a culinary agent [18]. AgNps arebiosynthesised and widely used in medicine due to their remarkable physical, chemical andbiological properties stemming from their large surface area and high reactivity. AgNps interactwith a pathogen’s nucleic material and hinder respiratory enzymes, thus eliminating pathoge-nicity [19].

This study describes the synthesis of silver nanoparticles using the weed I. carnea and theirantibacterial activity against selected human pathogens (both Gram-positive and Gram-negative) and one non-pathogenic bacterium, Mycobacterium smegmatis. An attempt was madeto fabricate a silver nanoparticle-impregnated cellulose acetate (CA) membrane, and themembrane was tested against M. smegmatis, which is analogous to M. tuberculosis. Thismembrane can be used as a mask to prevent infection among healthcare workers involved withtuberculosis (TB) patients.

2. Materials and methods

All chemicals were obtained from Sigma–Aldrich (USA) and used as received. A UV-visspectrophotometer (JASCO V-650, Japan) containing double beams in identical compartmentsfor reference and test solutions and fitted with a 1 cm path length quartz cuvette was used forthis study.

The FT–IR spectra were recorded using a FT–IR (Perkin Elmer, USA) spectrophotometer.The particle size of synthesised AgNps was analysed using a particle size analyser (NanotracUltra DLS, USA). The topography of the AgNps was analysed using an atomic forcemicroscope (AFM; Veeco – di Innova, USA) with a silicon nitride tip and spring constantranging from 0.01 to 0.1N/m. The size and shape of the AgNps were analysed using atransmission electron microscope (TEM; JOEL JEM SX 100, Japan) operating at 100 keV. TheI. carnea-stabilised AgNps were prepared for TEM measurement by placement of a drop ofnanoparticles on carbon-coated copper grid followed by drying under vacuum.

2.1. Preparation of plant extract and synthesis of nanoparticles

Fresh I. carnea leaves were cut and washed with Milli-Q water (18.2MV cm�1 resistivity). Theextraction procedure was as follows: 20 g of leaves was added to 100mL of Milli-Q water andboiled for 60min. The broth extract was decanted and kept at 4�C for further use. The leafextract was then mixed with enough 1mM silver nitrate to give the desired solution (0.5% v/v,1% v/v, 2% v/v, 5% v/v and 10% v/v) and allowed to react at room temperature. The effectof pH on the resulting solution of AgNps and plant extract was also evaluated.

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2.2. Fabrication of silver nanoparticle-impregnated membrane

CA was dissolved in dimethylformamide and continuously stirred with freeze-dried AgNps(5 mg/mL) for 4 h and casted as CA membrane (1 cm2) using the phase inversion technique. TheAgNp-impregnated CA membrane was then periodically washed with Milli-Q water to removetrace solvents that also interfere with bacterial growth.

2.3. Antibacterial activity of biosynthesised silver nanoparticles

All the glassware, media and reagents used were sterilised in an autoclave at 121�C for 20min.For the antibacterial assays, Bacillus cereus (MTCC 6840), Bacillus subtilis (MTCC 8114),Proteus vulgaris (MTCC 425), Stapyhlococcus aureus (MTCC 9542), Pseudomonas aeruginosa(MTCC 2488), Aeromonas hydrophila (MTCC 1739), Klebsiella pneumoniae (MTCC 4032) andSalmonella typhi (MTCC 734) strains were obtained from Institute of Microbial Technology(IMTECH), Chandigarh, India, and subcultures were prepared using reviving nutrient broth.The bacterial suspension was prepared by growing a single colony overnight in nutrient brothand adjusting the turbidity to 0.5 McFarland standards.

2.3.1. Growth curve studies

The bactericidal activity of the silver nanoparticles was tested by growth inhibition studies.Sterile Erlenmeyer flasks containing 100mL nutrient broth and the desired amount of AgNpswere inoculated with 1mL of the freshly prepared bacterial suspension. The flasks were thenincubated in a rotary shaker at 150 rpm at 37�C. Bacterial growth was monitored on an hourlybasis for 24 h by measuring the absorbance at 600 nm using a UV-visible spectrophotometer. Acontrol flask containing nutrient broth and bacteria but devoid of AgNps was also monitored.

2.3.2. Zone of inhibition studies – disc diffusion method

A disc diffusion method was used to evaluate the antibacterial activity of silver nanoparticlesagainst selected human pathogens. A bacterial inoculum of 100 mL with 14� 107CFU (colonyforming units) in their respective log phase were smeared on Mueller–Hinton agar plates.Various concentrations of AgNps (0, 2, 5 and 7 mg) suspended in DMSO were loaded on a 6mmdiameter disc. The discs were placed on the agar plates and incubated at 37�C for 18 h. The zoneof inhibition (ZOI) was measured by standard methods. This assay was performed in triplicateand average results were tabulated.

2.3.3. Minimum inhibitory concentration

The minimum inhibitory concentration (MIC) of AgNps was determined for each of the testorganisms. The test organisms were inoculated in 5mL of nutrient broth and incubated at 37�Cfor 3–4 h. Various concentrations of AgNps (0, 2, 5, 7 and 10 mg) were added to the tubes at theinitial log phase of the organism to arrest the growth. Optical density at 620 nm was read foreach of the test organisms inoculated with the nanoparticles prior to plating on nutrient agar.The plates were incubated at 37�C for 24 h and the total number of colonies was counted todetermine the inhibitory efficacy of the AgNps.

2.3.4. Antimycobacterial studies of silver nanoparticle-impregnated membrane

The disc diffusion assay was carried out using a AgNp-impregnated CA membrane to determinethe mycobactericidal activity of AgNps against the Gram-positive bacterium M. smegmatis.

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A bacterial inoculum of 100 mL with 14� 107CFU in their respective log phase were smeared onMueller–Hinton agar plates. The AgNp-impregnated CA membrane was cut into a disc shapewith 6mm diameter and placed at the centre of the agar plate. A CA membrane without AgNpswas used as a control. The plates were incubated at 37�C for 18 h. The ZOI was measured bystandard methods.

3. Results and discussion

3.1. UV-visible spectroscopy studies

UV-visible absorption spectroscopy is one of the main tools to confirm the formation ofnanoparticles in aqueous solutions. A plant extract of 0.5mL causes a colour change fromtransparent (aqueous silver nitrate solution) to reddish brown within 5min, indicating theformation of AgNps (Figure 1). Noble metal nanoparticles exhibit a specific surface plasmonresonance (SPR) characteristic to each metal. The SPR peak obtained for AgNps varies from410 to 440 nm, in the range of Mie scattering, which confirms the formation of AgNps [20].Increasing the volume ratio of I. carnea extract to silver nitrate solution increases the formationof AgNps, which is evident from the increase in intensity/absorbance of the SPR peak(Figure 2). pH variation studies were conducted (pH 2, 4, 5, 6 and 8) with 1% v/v of leaf extractmediating AgNp synthesis. As the pH increased from 2 to 8, different SPR peaks appearedshowing a characteristic blue shift, indirectly revealing that increasing pH reduces the size of theparticle (Figure 3), which was in accordance with an earlier report [21]. At pH 5 with 1mL ofleaf extract, the desired size (60–70 nm) nanoparticle was obtained, and hence pH 5 was set asoptimum for the synthesis of AgNps.

3.2. Particle size analysis

The particle size of the synthesised AgNps was analysed using a dynamic light scattering (DLS)particle size analyser, an AFM and a TEM. The DLS particle size analysis was carried out usinga standard analysis time, and the size of AgNps was found to vary between 30 and 130 nm(Figure 4). Topographic images from AFM analysis showed the presence of uniformlydistributed AgNps with similar shape and size, between 25 and 150 nm, as seen in Figure 5.

Figure 1. (Colour online) Colour change from transparent to orange and then to reddish brown when ICleaf extract is added to 1mM silver nitrate solution.

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The transmission electron micrograph (Figure 6) showed the nanoparticle size range to bebetween 20 and 140 nm, coinciding with the range obtained from both the DLS and AFManalyses. Thus, the DLS, AFM and TEM analyses gave similar results for the size range of thenanoparticles.

3.3. FT–IR studies and reducing mechanism

FT–IR analysis was carried out to evaluate functional group changes in the constituents ofI. carnea extract before and after the addition of silver nitrate solution (Figure 7). There was asignificant change in the wave number of free hydroxyl groups and phenolic groups (3350 cm�1),suggesting that alkaloids with polyphenols may be involved in the reduction of silver nitrate andfurther stabilisation of AgNps. Interestingly, there was also a significant change in the wave

Figure 3. SPR variations of synthesised silver nanoparticles adjusted to different pH exhibiting blue shift.

Figure 2. UV-visible spectroscopy of silver nanoparticles synthesised with different concentrations of I.carnea leaf extracts (v%) in 1mM silver nitrate solution.

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number corresponding to sulphonic groups (650 cm�1). Earlier work using GC–MS to reveal thephytochemistry of I. carnea reported the presence of calystegine B2, calystegine C1 andswainsonine alkaloids as major chemical constituents [22]. Thus, polyphenols may be involved inreducing silver nitrate to AgNps (Figure 8).

3.4. Antibacterial activity

3.4.1. Pattern of bacterial growth inhibition

The growth kinetics of the bacteria is shown in Figure 9. Growth was inhibited in the initialstages, and in media containing AgNps, there was no obvious visible growth after the fourthhour. In the control experiment, we observed typical lag, log and death phases at the 4th, 13thand 26th hour, respectively. All organisms showed a typical inhibitory point after the addition ofsilver nanoparticles. The growth curves of B. cereus, B. subtilis, S. aureus, K. pneumoniae,A. hydrophila, P. vulgaris, S. typhi and P. aeruginosa showed similar results. There was anincrease in growth from the lag to log phase and a constant pattern of growth in the succeedingstationary phase.

3.4.2. Disc diffusion method

The antibacterial activity of the synthesised silver nanoparticles was studied by a qualitative discdiffusion assay on both Gram-positive and Gram-negative bacteria. Table 1 shows the diameter

Figure 5. Atomic force microscopy image viewed at 2D and 3D showing uniform-sized green-synthesisedAg nanoparticles.

Figure 4. DLS particle size analysis of green-synthesised silver nanoparticles having a size range from 30to 130 nm.

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of the ZOI for each organism. After 18 h of incubation at 37�C, the nutrient agar platescontaining various concentrations of nanoparticles exhibited a ZOI of around 11–15mmdiameter (Figure 10). Control plates devoid of nanoparticles did not exhibit any inhibitionzones. Bacterial inhibition may be due to the release of free radical from the surface of the AgNpthat attacks the membrane lipids and then lead to a breakdown of membrane function [23].Previous studies, using a 6mg/mL nanoparticle concentration, have found the ZOI to bebetween 12 and 13.6mm for both ciprofloxacin-resistant and non-resistant strains ofP. aeruginosa [24], but our results, using around 7 mg of nanoparticles, gave a much largerZOI of about 15mm.

Bacillus cereus, B. subtilis, S. typhi, P. aeruginosa and A. hydrophila showed a ZOI of 13mmwhen 7.0 mg of silver nanoparticles were loaded onto the disc. Staphylococcus aureus showed aZOI of 14mm. Klebsiella pneumoniae and P. vulgaris showed a ZOI of 15mm (Figure 10). Whensilver nanoparticles with an average size of 22.5 nm prepared by bacterial reduction wereemployed, Escherichia coli showed an inhibition zone of around 9mm (10mg nanoparticle

Figure 7. FT–IR analysis of green-synthesised silver nanoparticles when compared with IC leaf extract.

Figure 6. Transmission electron microscopy image of green-synthesised silver nanoparticles taken at100,000�.

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Figure 9. Growth kinetics of different microorganisms in the presence and absence of biosynthesised silvernanoparticles.

Figure 8. Schematic representation of mechanism of reduction and stabilisation of silver nanoparticles byI. carnea leaf extract.

Table 1. ZOI (mm) against different bacterial strains and at different concentrations of silvernanoparticles.

Human pathogens

ZOI (mm) at various concentration of silver nanoparticles

2mg 5mg 7mg

B. cereus 10.5� 0.28 12.6� 0.23 13.1� 0.44B. subtilis 11� 0.28 12.2� 0.48 13.1� 0.44S. aureus 10.1� 0.32 12� 0.28 14.1� 0.26P. aeruginosa 11� 0.23 13.1� 0.50 14� 0.17P. vulgaris 10� 0.34 12� 0.28 13.06� 0.4A. hydrophila 11� 0.17 13� 0.28 14.4� 0.31K. pneumonia 11.06� 0.34 13� 0.28 14.9� 0.48S. typhi 11.2� 0.38 13.03� 0.37 15.1� 40.0

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per disc) [25]. In a different antimicrobial study using chemically synthesised, uncapped silvernanoparticles of 3 nm average size, a ZOI of around 14–15mmwas reported forE. coli strains [26].However, this study also used discs with higher nanoparticle loading (100 mg) and fewer bacteria(103–104CFU). In this study, the average particle size was about 50 nm, and we observed anenhanced antibacterial activity even at a higher number of bacterial colonies (107CFU) at a muchlesser nanoparticle concentration (7 mg per disc). Thus, the effective inhibition observed in ourstudies is in agreement with earlier reports [25,26].

Figure 10. (Colour online) Antibacterial tests: ZOI seen around different concentrations of green-synthesised silver nanoparticles present wells against different microorganisms and inset showing positivecontrol of ethambutol.

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3.4.3. Minimum inhibitory concentration

The MIC of nanoparticles was evaluated to determine the toxicity of silver. This concentration isreached when there is a decrease in bacterial growth but no accompanying toxicity is observed.For all organisms, 20 mL aqueous AgNps having 10 mg AgNp gave a significant decrease inCFUs (Figure 11). With 40 mL (20 mg AgNps), many fewer colonies were formed. At 100 mL(50 mg AgNps), even fewer CFUs were observed. However, as this last concentration may betoxic to humans, the optimum MIC was determined to be 20 mg.

3.4.4. Antimycobacterial membrane studies

The colour of pure CA membrane was significantly different from the colour of AgNp-impregnated CA membrane (Figure 12). It was found that the silver nanoparticle-impregnatedCA membrane exhibited an inhibition zone of 14mm. No inhibition zone was observed with thepure CA membrane (Figure 13). This clearly demonstrates that the antimycobacterial activityis due to the silver nanoparticles embedded in the membrane and not due to the CA itself.

Figure 11. MIC test against different strains of microorganisms exhibiting varied growth and survivalagainst different concentrations of biosynthesised silver nanoparticles.

Figure 12. (Colour online) (a) CA membrane and (b) CA membrane impregnated with green-synthesisedsilver nanoparticles.

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The development of low fouling membranes or antifouling membranes is an intense area of

research in membrane separation technology [27,28]. The use of nanoparticles in the

manufacture of membranes allows for both a high degree of control over membrane fouling

and the ability to produce desired structures [29–31]. In particular, AgNp-impregnated

nanofibres and nanofibrillar aerogels can be used for antimicrobial membrane synthesis. The

membrane is immersed in silver nitrate and then irradiated with UV light or exposed to sodiumborohydride to reduce the silver nitrate, producing a CA membrane with embedded silver

nanoparticles. The AgNps synthesised in this article showed better results than previous reports

when used to impregnate a CA membrane. Biofouling can be avoided using the bactericidal

properties of silver nanoparticles, and indeed, silver is a typical example of a bactericide that is

used for fouling mitigation in polymeric membranes. Escherichia coli and Staphylococcus aureus

have typically been used as model organisms to evaluate the antimicrobial properties of AgNp-

impregnated CA membranes [32]. However, in this study, we evaluated the antimicrobial

activity of AgNps against M. smegmatis.

4. Conclusion

We have demonstrated a simple, fast and green method to synthesise AgNps using I. carnea. Thesynthesised AgNps were confirmed by UV-visible spectrophotometer. The size, topography and

shape of AgNps were measured using a DLS particle size analyzer, AFM and TEM,

respectively. The reducing mechanism may involve the hydroxyl groups whose presence in the

alkaloids and polyphenols of the extract was confirmed by FT–IR. We also fabricated a CA

membrane impregnated with biosynthesised AgNps and tested it against M. smegmatis. The

results suggest that the weed extract-based synthesis of silver nanoparticles is very efficient

against selected human pathogens and can be used in the fabrication of hospital clothes, gloves

and masks to avoid the spread of infection among healthcare workers.

Acknowledgements

Authors S.C.G. Kiruba Daniel and B. Nazeema Banu have equally contributed to this study. We are verymuch thankful to Anna University of Technology Tiruchirappalli for the funding of Instrument facilities.S.K. sincerely acknowledge the financial assistance from DST Nanomission infrastructure project # SR/NM/PG-05/2008 and Periyar-TBI for instruments facility. B.N.B. acknowledges CSIR for providingSenior Research Fellowship (09/960(002)/2K9-EMR-I).

Figure 13. (Colour online) Antimycobacterial assay: ZOI seen around green-synthesised silvernanoparticles-impregnated CA membrane in a M. smegmatis plate and it is absent around CA membrane.

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