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. 2023 Jun 26;74(2):90–98. doi: 10.2478/aiht-2023-74-3684

A new strategy to achieve high antimicrobial activity: green synthesised silver nanoparticle formulations with Galium aparine and Helichrysum arenarium

Nova strategija za postizanje visoke antimikrobne djelotvornosti: zelena sinteza formulacija srebrnih nanočestica pomoću biljnih vrsta Galium aparine i Helichrysum arenarium

Cilem Ozdemir 1,2, Merve Gencer 1, Irem Coksu 3, Tulin Ozbek 1, Serap Derman 3,✉
PMCID: PMC10291498  PMID: 37357883

Abstract

Silver nanoparticles (AgNPs), which have recently gained attention due to their antimicrobial activity, can also be produced by green synthesis. The aims of this study were to (i) characterise green synthesized AgNPs using microwave-assisted aqueous extracts of Galium aparine (G-AgNPs) and Helichrysum arenarium (H-AgNPs) and (ii) investigate the combined antimicrobial effects of the G- and H-AgNPs in different ratios. Nanoparticle formation and reactions were determined with UV-Vis spectroscopy. The G-AgNPs were 52.0±10.9 nm in size, with a 0.285±0.034 polydispersity index (PDI), and a -17.9±0.9 mV zeta potential. For H-AgNPs these characteristics were 23.9±1.0 nm, 0.280±0.032, and -21.3±2.7 mV, respectively. Atomic force microscopy (AFM) and scanning electron microscopy (SEM) confirmed that the particles were monodisperse and spherical. The Fourier transform-infrared spectroscopy (FT-IR) results showed the presence of reducing agents that stabilised the AgNPs. Three different nanoformulations (NF-1, NF-2, and NF-3) were prepared by combining these two synthesised nanoparticles in different ratios and their antimicrobial activity was tested against E. coli, S. aureus, C. albicans, and A. flavus. Our study is the first to show that combining AgNPs from two different biological sources can produce effective nanoformulations with improved antibacterial activity against E. coli and S. aureus. These nanoformulations showed lower minimum inhibitory concentrations (31.25 µg/mL against E. coli with all NFs; 62.5 µg/mL for NF-1 and 125 µg/mL for NF-2/3 against S. aureus) than G-AgNPs (62.5 µg/mL for E. coli) or H-AgNPs (125 µg/mL for S. aureus) alone. Their high combined inhibitory effect against E. coli (NF-1–3) was synergistic and against S. aureus (NF-2 and NF-3) potentially additive. Considering such promising results, we believe our study provides some direction for new research and strategies in antimicrobial therapeutics.

KEY WORDS: A. flavus, antimicrobial nanosystems, C. albicans, E. coli, plant extracts, S. aureus, synergistic effect

Swift and remarkable advances in nanotechnology have made nanomaterials available for many applications in pharmacology, including transport and targeting of drug molecules, development of diagnostic imaging systems, design and production of controlled release systems, and support of plant nutrition (1–5). Nanoparticles can penetrate cells at a high rate thanks to their high surface area/ volume ratio (6), and these properties provide nanoparticles with different biological activities such as antioxidant (7), antimicrobial (8, 9), and anticancer (10). Metallic nanoparticle systems have attracted particular attention in recent years, as, unlike polymeric or lipid nanoparticles, they can be used in antimicrobial treatment, especially due to their surface plasmon resonances (11–14). In this respect silver nanoparticles (AgNPs) stand out (15, 16).

Since chemical nanoparticle synthesis may involve many toxic agents, and physical synthesis is costly (17, 18), more and more attention is being given to the so called green nanoparticle synthesis, which relies on plants, microorganisms, algae, and DNA templates to reduce and stabilise nanoparticle metal ions (19–23). This is particularly true for AgNPs synthesised using plant extracts because of their broad antimicrobial spectrum (24, 25).

In this study, we wanted to see how extracts of immortelle (Helichrysum arenarium) and cleavers (clivers, bedstraw, Galium aparine) would fare in the synthesis of AgNPs in terms of their antimicrobial efficiency, considering that both plants have known therapeutic antimicrobial, antioxidant, and anticancer effects (26–37). In addition, both plants contain compounds that reduce silver and maintain the stability of the formed nanoparticles.

In this respect, high-efficiency extraction of plant components is the most crucial step in the green synthesis of AgNPs, and microwave-assisted extraction (MAE), which has earned it popularity in recent years, is more efficient and quicker than traditional extraction methods. In addition, MAE is a suitable for large-scale and small-scale systems (38).

To sum up, the aims of our study were to: (i) to synthesise and characterise two different AgNPs using the microwave-assisted aqueous extracts of G. aparine and H. arenarium (G-AgNP and H-AgNP, respectively) and (ii) to investigate the antimicrobial activity of combined nanoparticles at different ratios. To the best of our knowledge, this combination has not been investigated.

MATERIALS AND METHODS

Materials

Silver nitrate was purchased from Sigma-Aldrich (St. Louis, MO, USA). Müller Hinton broth, Müller Hinton agar, Sabouraud dextrose broth, and Sabouraud dextrose agar were purchased from Merck (Darmstadt, Germany). The plants H. arenarium and G. aparine were purchased commercially in dry form (Arpas Arifoglu Marketing Distribution and Trade Inc.). E. coli (ATCC number: 25922), S. aureus (ATCC number: 25923), C. albicans (ATCC number: 10231), and A. flavus (ATCC number: 204304) were obtained from the Yıldız Technical University Molecular Biology and Genetics Department, Laboratory of Microbiology (Istanbul, Turkey). Ultra-pure water was obtained from the Millipore MilliQ Gradient system (Millipore Corporation, Bedford, MA, USA).

Preparation of plant extracts

We opted for a fast, efficient, and environmentally friendly MAE method using water, a non-toxic and reliable solvent, instead of chemical solvents (39). To prepare the aqueous extract, 4.5 g of powdered H. arenarium and G. aparine leaves were mixed with 100 mL of distilled 18.2 MΩ/cm water (4.5% w/v) and boiled for 5 min. To remove plant residues, the extracts were first centrifuged (NF 800R, Nuve, Istanbul, Turkey) at 4025 g and 25 °C for 20 min and then filtered through Whatman filter paper No. 1 and were kept at 4 °C for further tests.

Nanoparticle synthesis optimisation

The synthesis of G-AgNPs and H-AgNPs was optimised by trial and error, using different parameters such as pH (6–10), temperature (25–80 °C), AgNO3 concentration (0.1–2 mmol/L), and reaction time (0–240 min). The optimum green synthesis parameters for G-AgNPs were pH 8, temperature 70 °C, AgNO3 concentration 1 mmol/L, and reaction time 4 h. Interestingly, the optimum synthesis parameters for H-AgNPs were different: pH 9, temperature 60 °C, AgNO3 concentration 1 mmol/L (as in G-AgNPs), and reaction time 3 h. G-AgNPs and H-AgNPs analysed in this study were synthesised under these optimal conditions for biological activity.

To synthesise H-AgNPs 1 mL of aqueous H. arenarium extract was added dropwise to 20 mL of AgNO3 solution in the 1:20 ratio (v:v) at 60 °C to obtain a concentration of 1 mmol/L. The pH of the mixture was then adjusted to 9 with 1 mol/L NaOH using a pH-meter (HANNA instruments HI 2211 pH/ORP Meter). The mixture was stirred on a magnetic stirrer at 60 °C for 3 h. To synthesise G-AgNPs, 1 mL of aqueous G. aparine extract was added dropwise to 20 mL of AgNO3 solution in the 1:20 ratio (v:v) at 70 °C to reach a concentration of 1 mmol/L, and the pH of the mixture was then adjusted to 8. The mixture was stirred on a magnetic stirrer at 70 °C for 4 h.

The reaction was followed with a UV-Vis spectrophotometer (UV-1700, Shimadzu, Kyoto, Japan). The produced particles were collected by centrifugation at 9056 g and 25 °C for 30 min (Nüve NF 800R), washed three times with ultrapure water to remove unreacted plant residues and silver nitrate, and then lyophilised. All lyophilised nanoparticles were stored at -80 °C until further analysis. NF-1, NF-2, and NF-3 nanoformulations (NF) were prepared by combining G-AgNPs and H-AgNPs as follows: 1000 µg/mL G-AgNP + 1000 µg/mL H-AgNP (NF-1), 500 µg/mL G-AgNP + 1500 µg/mL H-AgNP (NF-2), and 1500 µg/mL G-AgNP + 500 µg/mL H-AgNP (NF-3).

Nanoparticle characterisation

The formation of nanoparticles was first confirmed visually based on the change in the colour of the reaction solution from yellow to brown. Analytically it was confirmed from the intensity of surface plasmon band absorption of nanoparticle solutions measured in the wavelength range of 200–800 nm at 25±0.1 °C using a UV-Vis spectrophotometer (UV-1700, Shimadzu). All measurements were made at a 1:10 dilution of the samples. For the blank we used ultrapure water.

The average size (hydrodynamic diameter) and polydispersity index (PDI) of nanoparticles were measured with dynamic light scattering (DLS), and the zeta potential with electrophoretic light scattering (ELS) using a Zetasizer Nano ZS (Malvern Instruments, Worcestershire, UK) equipped with a 4.0 mV He–Ne laser (633 nm) (7). Measurements were carried out in triplicate, at 25±0.1 °C, using the 0.8872 cP viscosity and 1.330 refractive indexes for the solutions and dielectric constant of 79 f(ka) 1.50 (Smoluchowski value). The number of runs and run durations were chosen automatically. All samples were diluted to a 1:10 ratio with distilled water before measurement.

The functional groups involved in both plant powders (G. aparine and H. arenarium) and the synthesised AgNPs (G-AgNPs and H-AgNPs) were determined using a Fourier transform-infrared (FT-IR) spectrophotometer (Shimadzu) (8). The analysis was performed in universal attenuation total reflectance (ATR) mode at 25±0.1 °C with a scanning spectrum of 800–3500 cm-1 wavenumber with 32 scans per sample and resolution of 4 cm-1.

The surface morphology, topography, size, and size distribution of AgNPs were determined with both atomic force microscopy (AFM) (Shimadzu SPM 9600) and scanning electron microscopy (SEM) (FEI QUANTA 450 FEG, Thermo Fisher Scientific, Waltham, MA, USA). AFM images were taken with the force constant of 0.02–0.77 N/m, tip height 10–15 nm, and silicon lever in contact mode (40). Freeze-dried powdered nanoparticles were fixed on metallic studs with double-sided conductive tape, then coated with gold under vacuum and analysed with SEM (7).

Antimicrobial activity measurement

The antimicrobial activity of G-AgNPs and H-AgNPs alone and in nanoformulations (NF-1, NF-2, and NF-3) was tested against E. coli (ATCC 25922), S. aureus (ATCC 25923), C. albicans (ATCC 10231), and A. flavus (ATCC 204304) in vitro using the broth microdilution method, which is a quantitative method. The results were obtained by spectrophotometric measurements (OD600 nm) and the standard plate counting method, as described by the Clinical & Laboratory Standards Institute (CLSI) standard (41, 42).

We prepared stock solutions of AgNPs and nanoformulations at a concentration of 2 mg/mL and serial dilutions in the range of 1–0.03125 mg/mL. 100 µL of the prepared samples were added to six wells each of the 96-well microplate. Microorganism suspension (106 CFU/mL) was added to each well to adjust the final volume in the wells to 200 µL. Microplates containing bacteria were incubated at 37 °C and microplates containing fungi at 28 °C for 16–18 h. After incubation, we determined minimum inhibition concentrations (MIC) and minimum bactericidal or fungicidal concentrations (MBC or MFC, respectively) by spectrophotometry (OD600 nm) and standard plate counting.

Statistical analysis

For statistical analysis we used the SPPS software version 22 (SPPS Inc., Chicago, IL, USA). All data are expressed as means ± standard deviations (SD) of three independent measurements. Statistical differences in MIC and colony counts between control and treated groups were analysed with the two-way analysis of variance (ANOVA) and significance set to p<0.05.

RESULTS

Figure 1 shows colour changes in the solution colour, which is attributed to the localised surface plasmon resonance (SPR) of metal nanoparticles (43–46). UV-Vis spectroscopy confirmed the formation of AgNPs with the characteristic SPR peak at 418 nm and 406 nm wavelengths for G-AgNPs and H-AgNPs, respectively.

Figure 1.

Figure 1

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UV–Vis absorption spectra of a) G-AgNPs and b) H-AgNPs with different incubation times (0–240 min)

Figure 2 shows that the particles were nanosized and highly monodisperse. Table 1 shows the average particle size, zeta potential, and PDIs of H-AgNPs and G-AgNPs. Because of excessive negative or positive zeta potential values (±30 mV), the electrostatic force between the nanoparticles prevents agglomeration of the NPs (47). These negative zeta potential values may be due to the presence of the stabilising agents (bioorganic components in the extract) acting as silver-reducing agents. Figure 3 shows the range of potentials for both H-AgNPs and G-AgNPs.

Figure 2.

Figure 2

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Particle size distribution of a) G-AgNPs and b) H-AgNPs

Table 1.

Physicochemical properties of H-AgNPs and G-AgNPs

NPs Particle Size (nm) Zeta Potential (mV) Polydispersity Index
H-AgNP 23.9±1.0 −21.3±2.7 0.285±0.034
G-AgNP 52.0±10.9 −17.9±0.9 0.280±0.032
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Figure 3.

Figure 3

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Zeta potential of a) G-AgNPs and b) H-AgNPs

Figures 4a and 4c show the FT-IR spectra of G. aparine and H. arenarium plant powders, respectively. The vibrational stretches in the FT-IR spectrum of G. aparine at 3450, 2921–2848, 1378, and 1010 cm-1 correspond to the O–H stretch of an aromatic alcohol, aliphatic C-H stretch, the C=C stretch in the aromatic ring, and the alcohol C–O stretch, respectively. Despite lower peak intensities, the FT-IR spectrum of G-AgNPs is relatively similar to that of G. aparine (Figure 4b). Phytochemicals in G. aparine are responsible for the formation and stabilisation of G-AgNPs but also coat the surface of the nanoparticles (48).

Figure 4.

Figure 4

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FT-IR spectrum of a) G. aparine, b) G-AgNPs, c) H. arenarium, and d) H-AgNPs

The band at 1650 cm-1 in the spectrum of H. arenarium (Figure 4c) suggests that it may belong to the carbonyl stretch in the amide bond of the proteins, while the band at 1557 cm-1 may belong to the stretching vibrations of conjugated double bonds, indicating the presence of terpenoids or other aromatic plant components. The broad bands between 1100–1000 cm-1 may have formed due to ether interactions, suggesting the presence of flavanones in H. arenarium. The FT-IR spectrum of H-AgNPs (Figure 4d) shows that most of the functional groups in H. arenarium either disappeared or the existing peaks had large shifts in their positions. Compared to the FT-IR spectrum of H. arenarium, it suggests that the reduction, capping, and stabilisation of AgNPs are owed to the aromatic carbonyl, amide, and ether components as well as flavanone, protein, and terpenoid components, as reported elsewhere (22, 49).

Figures 5 and 6 show that most of the synthesised AgNPs have spherical and monodisperse distribution. The sizes of G-AgNPs are between 40 and 60 nm (Figures 5a and 6a), and the sizes of H-AgNPs are between 20 and 30 nm (Figures 5b and 6b). These values correlate with DLS findings.

Figure 5.

Figure 5

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2-D Atomic force microscope images of a) G-AgNPs and b) H-AgNPs. Scan scale: 1×1 µm

Figure 6.

Figure 6

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Scanning electron microscope images of a) G-AgNPs and b) H-AgNPs at 200,000× magnification

Antimicrobial activity of nanoparticles and nanoformulations

Table 2 shows the minimum inhibitory, bactericidal, and fungicidal concentrations of G-AgNPs, H-AgNPs, and their three combinations against E. coli, S. aureus, C. albicans, and A. flavus. G-AgNPs were effective against E. coli and C. albicans, and H-AgNPs against S. aureus and A. flavus, which is evident from the Petri dish images (Table 3).

Table 2.

MBC/MFC and MIC values of samples according to the broth microdilution method

Test sample AgNP concentrations used in nanoformulations (μg/mL) MIC μ/mL) by microorganisms MBC/MFC μ/mL) by microorganisms
E. coli S. aureus A. flavus C. albicans E. coli S. aureus A. flavus C. albicans
G-AgNPs 62.5 − − 2000 125 − − −
H-AgNPs − 125 500 − − − − −
NF-1 1000 G-AgNP + 1000 H-AgNP 31.25* 125 500 − 125 250 − −
NF-2 500 G-AgNP + 1500 H-AgNP 31.25* 62.5 500 − 125 125 − −
NF-3 1500 G-AgNP + 500 H-AgNP 31.25* 62.5 500 − 125 125 − −
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*

p<0.05, NFs vs AgNPs. MBC – minimum bactericidal concentration; MFC – minimum fungicidal concentration; MIC – minimum inhibitory concentration

Table 3.

Table 3

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Petri dish images obtained by standard plate counting related to respective MICs. The dilution coefficient for E. coli is 102. There is no dilution for other microorganism. MIC – minimum inhibitory concentration

In turn, all nanoformulations combining H-AgNPs and G-AgNPs were significantly more effective against E. coli than their components alone, with the MIC lowered to 31.25 µg/mL for all three formulations, which points to a synergistic effect. In addition, NF-2 and NF-3 nearly halved the MIC and MBC of H-AgNPs alone against S. aureus, which points to an additive effect. Neither G-AgNPs or H-AgNPs alone or in combination showed antifungal effect, and their bactericidal effects against E. coli did not improve when combined.

DISCUSSION

Cell uptake of nanoparticles depends on particle size and so does their antimicrobial activity, which increases with smaller nanoparticles, as reported by Manoslava et al. (50) and Agnihotri et al. (51). The antimicrobial activity of G-AgNPs and combined nanoformulations against E. coli is higher than against other microorganisms tested in the study, which can be explained by the presence of a fine peptidoglycan layer and porins possessed by Gram-negative bacteria and the action of Ag+ ions released by AgNPs (52–55). The somewhat higher negative zeta potential of H-AgNPs can, in turn, explain the antimicrobial activity against Gram-positive S. aureus and A. flavus (56). Ours and previous studies all seem to suggest that knowing the amount of dissolved Ag+ released from the surface of AgNPs may shed more light on their antibacterial activity or cytotoxicity and we believe that future studies should be determining the amount of released Ag+.

There are two interesting findings that we cannot yet explain. The first is that the combinations of G-AgNPs and H-AgNPs produced the same synergistic antimicrobial effect against E. coli regardless of their ratios. The second is that even though G-AgNPs showed inhibitory effect against C. albicans and H-AgNPs against A. flavus, none of their combinations inhibited C. albicans, yet maintained the inhibitory effect on A. flavus. We believe that further research should also try to explain this seeming paradox.

Despite these limitations of our study, our findings of the synergistic effects of the two synthesised nanoparticles when combined seem to support some earlier reports of improved antimicrobial effects by combinations of AgNPs with tomato, onion, acacia, neem, Eucalyptus globulus, Trichophyton rubrum, or garlic (57–61). One study that combined AgNPs synthesised with the rutin flavonoid and heliomycin antibiotic reported dose-dependent and synergistic antibacterial activity against Aeromonas hydrophila and Pseudomonas fluorescens (62).

In addition, we know that H. arenarium contains quercetin, chlorogenic acid, caffeic acid, and naringenin flavonoids, while G. aparine contains gallic acid, quercetin, tannic acid, and rutin (27, 28, 36). There are many studies showing the antimicrobial activity of these compounds alone (63–65). So, besides the combined effect of AgNPs with these plant components, the synergistic antimicrobial effect of the nanoformulations could be attributed to a synergy between plant components on the surface of AgNPs. This, however, calls for further investigation.

CONCLUSION

Our study is the first to report the antimicrobial activity of nanoformulations containing both G-AgNPs and H-AgNPs and the first to identify their synergism against E. coli. NF-2 and NF-3 were more effective against S. aureus than G-AgNPs and H-AgNPs alone or combined in NF-1. This suggests that the antibacterial effect of H-AgNPs alone against S. aureus is further enhanced by what seems an additive effect of the NF-2 and NF-3 formulations. However, our study also raises a number of questions that need to be clarified by future studies, especially in terms of the mechanism of action involved.

Acknowledgments

This research was supported by the Scientific and Technological Research Council of Turkey (TUBITAK) under grant Nos. 1139B411900718 and 1139B411900634. For this research author Irem Coksu received a doctorate scholarship by the Republic of Turkey, Council of Higher Education.

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