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. 2020 Jan 2;5(1):386–393. doi: 10.1021/acsomega.9b02867

Vibrational Spectroscopy and Morphological Studies on Protein-Capped Biosynthesized Silver Nanoparticles

Enzo Victorino Hernandez Agressott †, Dominic Blätte ‡, Francisco Afrânio Cunha §,∥, Victor T Noronha †, Richard Ciesielski ‡, Achim Hartschuh ‡, Amauri Jardim de Paula †, Pierre Basílio Almeida Fechine §, Antônio Gomes Souza Filho †, Alexandre Rocha Paschoal †,*
PMCID: PMC6964295  PMID: 31956786

Abstract

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Silver nanoparticles (AgNPs) have a large number of applications in technology and physical and biological sciences. These nanomaterials can be synthesized by chemical and biological methods. The biological synthesis using fungi represents a green approach for nanomaterial production that has the advantage of biocompatibility. This work studies silver nanoparticles (AgNPs) produced by fungi Rhodotorula glutinis and Rhodotorula mucilaginosa found in ordinary soil of the Universidade Federal do Ceará campus (Brazil). The biosynthesized AgNPs have a protein-capping layer involving a metallic Ag core. The focus of this paper is to investigate the size and structure of the capping layer, how it interacts with the Ag core, and how sensitive the system (core + protein) is to visible light illumination. For this, we employed SEM, AFM, photoluminescence spectroscopy, SERS, and dark-field spectroscopy. The AgNPs were isolated, and SEM measurements showed the average size diameter between 58 nm for R. glutinis and 30 nm for R. mucilaginosa. These values are in agreement with the AFM measurements, which also provided the average size diameter of 85 nm for R. glutinis and 56 nm for R. mucilaginosa as well as additional information about the average size of the protein-capping layers, whose found values were 24 and 21 nm for R. mucilaginosa and R. glutinis nanoparticles, respectively. The protein-capping layer structure seemed to be easily disturbed, and the SERS spectra were unstable. It was possible to identify Raman peaks that might be related to α-helix, β-sheet, and protein mixed structures. Finally, dark-field microscopy showed that the silver cores are very stable, but some are affected by the laser energy due to heating or melting.

1. Introduction

Nanoparticles are systems commonly considered to have a size of approximately 1–100 nm; the design, synthesis, and manipulation of this type of system are made through nanotechnology. The small size of these materials makes them attractive for applications in a wide range of areas. Nanoparticles, based on metals, such as Au, Pt, Pd, and Ag, are used in health care products, cosmetics, and food, as well as in environmental and biomedical sciences, chemical industries, space industries, and catalysis.1,2

Several routes and chemical methods are used for the synthesis of nanoparticles (NPs) from metal salts. However, most of them include the use of toxic solvents that generate waste harmful to the health and environment and result in high energy consumption in routes that are generally complex and multistep. A promising approach to achieve this goal is to explore the wide range of natural resources available through the so-called green synthesis. In this context, the use of fungi and bacteria for the synthesis of silver nanoparticles (AgNPs) has been achieving rising interest over the last years. Among the biogenic processes for the production of metallic NPs, those mediated by fungi present high efficiency, besides simplicity and low cost.3,4 Fungi cultures, when compared to bacteria, require simpler nutrients, produce a large amount of biomass, and are easily handled. In addition, most of the fungi used to produce AgNPs are nonpathogenic to humans and the presence of a capping protein layer involving the metallic core makes these particles potentially biocompatible.5,6

The production of silver nanoparticles by fungi Rhodotorula mucilaginosa (Rm) and Rhodotorula glutinis (Rg) was previously accomplished by Cunha et al.11,14 These fungi have a wide range of application, e.g., in food and biodiesel industries. In the latter, they are used to convert glycerol derivative into carotenoids, which are important antioxidants.5−7 It should be noted that this type of fungi could be found in a wide variety of environments, such as fruits, wood, water, and decaying soils, which makes it relatively easy to obtain them for cultivation in laboratories and for storage. The feeding of fungi with sucrose or glucose creates enzymes in broth that are easily storable and reusable according to the needs. After separating the fungus from the enzyme broth, silver nitrate is added to the broth and the stabilization of the nanoparticle is achieved by the formation of a thin layer of protein cover that involves the Ag nucleus in a mechanism that has been investigated for different fungi.14,15 These microorganisms possess the capacity to carry out the reduction of metal ions to metallic nanoparticles due to the secretion of a large number of enzymes (generally proteins); the said protein layer generates compartments capable of providing structural, spatial, and chemical controls for the stabilization and generation of nanoparticles.12,15 The AgNPs created by the fungi Rm and Rg are very stable (we have AgNPs in perfect conditions that have been stored for many months). When compared with other nontoxic alternative methods (e.g., plants and bacteria), Rm and Rg fungi-based methods generate a much larger amount of biomass.7−14 Plants might be used, but this method requires a place (e.g., orchards) and a continuous maintenance; it occupies a larger space, and thus, it is more time-consuming; bacteria culture might not be healthy because many of them can be very dangerous for human beings. It should be noted that it is not a straightforward answer to say which method of green synthesis is the best; there are many variables involved that will depend more on the protocols, materials, resources, and biological organisms that we have at hand. Finally, the use of Rm and Rg fungi is very convenient for this work because they are available in abundance in the campus soil of UFC. For more details, see Cunha et al.11,14

Despite the physicochemical and biological characterization commented above, information about the physical, chemical, and optical properties of the nanoparticles is still missing. In this work, we go a step further by performing a joint microscopic–spectroscopic–optical investigation of these nanoparticles. Atomic force and scanning electron microscopy techniques were employed to obtain physical information about the core and the protein layer. Statistical and comparative studies were made using the data provided by these techniques. Chemical and optical analyses of the AgNPs were carried out through surface-enhanced Raman spectroscopy (SERS), photoluminescence (PL) spectroscopy, and dark-field scattering. Together, they give us a greater approach on the study of the properties and characteristics of AgNPs synthesized by Rm and Rg fungi.

2. Experimental Details

Synthesis processes mediated by fungi R. glutinis and R. mucilaginosa were made according to the procedure and reported by Cunha et al.14 and Noronha et al.13 The synthesis process in the laboratory is relatively fast; at the beginning, it takes a few days to prepare the culture and to biosynthesize the NPs, but after that the AgNPs are stored in a well-sealed container in deionized water in a dark, dry place at room temperature. AgNPs can be stored for months (we have AgNPs stored for 12 months in perfect condition) and, therefore, can be used repeatedly for applications and/or characterizations. To use them, one just has to take the desired amount of the stored AgNPs, sonicate, and dilute; this takes only a few hours and large quantities can be prepared if necessary. Further details on the biogenic synthesis are given elsewhere.10−14 A summary of the whole process is illustrated in Figure 1.

Figure 1.

Figure 1

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Summary of the synthesis process and deposition of the samples for the AFM, SEM, and Raman characterizations.

For the Raman and AFM measurements, 10 mL of the suspension of the stored nanoparticles was taken and sonicated for 20 min after addition of 10 mL of deionized water (i.e., diluted AgNP suspension). With a micropipette, one drop was deposited onto a 0.2 mm-thick glass substrate and left to dry covered for 48 h at room temperature. An objective lens of 100×/NA = 0.90 was used in the optical microscope that was conjugated to a Raman spectrometer (WITec alpha300). Spectra were acquired in a time series with an acquisition time of 1 s using a green laser (532 nm) with a power of 10 mW. For AFM characterizations, an Asylum Research MFP-3D-BIO atomic force microscope was used in the tapping mode. For SEM characterization, one drop of the diluted AgNP suspension was deposited on a silicon substrate (Si). The SEM characterization was carried out using a Quanta 450 FEG microscope (FEI). The photoluminescence (PL) emission spectra were measured for individual particles by a confocal microscope using a CW diode laser at 473 nm for excitation together with a laser line filter and a 490 nm long-pass filter in the detection path. Dark-field scans were recorded using broadband (300 nm to 2.5 μm), incoherent illumination at a shallow angle and an NA 0.7 microscope objective to collect the elastically scattered light only. A pinhole in the detection allowed to select the light, scatter off an individual particle, and record its spectrum. Additionally, we illuminated the particles by a HeNe laser at 633 nm (∼5 mW) to test the influence of laser heating and plasmon resonance. The scattered light was either sent to an APD single-photon counter or to a spectrometer, and a 550 nm short-pass filter was included in the optical path to remove the laser light.

3. Results and Discussion

The SEM technique is a versatile tool that has already been successfully employed to characterize fungal AgNPs.16−19Figure 2 presents SEM images on a silicon substrate of the biosynthesized nanoparticles. The images show AgNPs with different sizes and spherical shapes, although irregular spheres are also present. For both Rg- and Rm-AgNPs, it is possible to observe isolated nanoparticles and agglomerates. However, nanoparticles synthesized by the fungus R. glutinis (Figure 2a) tend to form aggregates on the Si substrate, while those synthesized by R. mucilaginosa (Figure 2b) appear well-isolated. The histograms shown in Figure 2c,d were constructed with 115 AgNPs, which allowed to calculate the average size of 58 nm for Rg-AgNPs and 30 nm for Rm-AgNPs. Cunha et al.14 obtained higher values for Rg-AgNPs (108 nm) and Rm-AgNPs (119 nm) using dynamic light scattering (DLS) to analyze the same samples considered here. This difference can be attributed to the fact that the protein layer covering the silver core could be invisible in SEM and/or to aggregates in the solution used for the DLS experiment.

Figure 2.

Figure 2

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(a) R. glutinis AgNP SEM image and (c) size histogram. (b) R. mucilaginosa AgNP SEM image and (d) size histogram.

Additional characterization was performed by employing atomic force microscopy (AFM) in the intermittent contact mode (tapping). Figure 3a,b shows the AFM topography for Rm- and Rg-AgNPs, respectively. Just like in the SEM images above, AFM confirms that the nanoparticles synthesized by the fungus R. glutinis tend to agglomerate (Figure 3b). Figure 3e,f shows a histogram of the particle sizes for Rm- and Rg-AgNPs, respectively, made with 80 particles taken from the topography images. Due to the agglomeration of the Rg-AgNPs, their histogram has larger values for the nanoparticle sizes than those for Rm-AgNPs. The mean sizes calculated from AFM topography are ∼56 and ∼85 nm for Rm- and Rg-AgNPs, respectively.

Figure 3.

Figure 3

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Atomic force microscopy measurement images of the nanoparticles; the left column images refers to the R. mucilaginosa sample, while the right column refers to R. glutinis. (a, d) AFM topography images; (b, e) AFM phase images; and (c, f) size histograms of the topography images.

The AFM tapping operation mode is particularly interesting for this work since it is sensitive to different compositions through the phase image. Besides the cantilever amplitude, the movement of the probe can be characterized by its phase relative to a drive oscillator. The phase signal changes when the probe finds regions of different compositions; thus, phase imaging is a powerful tool that is sensitive to the rigidity/smoothness of the surface, i.e., a dissipative force between the tip and the sample surface. This allows the mapping of surfaces to identify constituents with different hardnesses and/or to find different materials involved. Figure 3c,d shows AFM phase images for Rm- and Rg-AgNPs, correspondingly. Importantly, the contrast of these images demonstrates the existence of a solid nucleus (i.e., Ag) for each nanoparticle with a wrapping layer (i.e., protein) involving it. The donut-shaped aspect in the phase images is not present in the corresponding spots of the topography images shown in Figure 3a,b. These images show a profile made by considering a horizontal line crossing the nanoparticles that is indicated by the arrows with an FWHM of ∼21 nm attributed to the protein-capping layer width. It should be noted that this value is the experimental minimum limit for the NP considered since the measured profile is a convolution of the tip diameter with the layer width. Using this method, it is possible to estimate the width of the protein layer biosynthesized by fungi to be approximately 24 nm for Rm-AgNPs and 21 nm for Rg-AgNPs, while the diameters of the solid core of the particle are estimated to around 37 nm and 71 for Rm- and Rg-AgNPs, respectively. The Rg nanoparticles tend to agglomerate; this can induce errors in the estimation of the real sizes of Rg-AgNPs, even though the values obtained here have good agreement with the literature.13Table 1 summarizes the analysis of the AFM and SEM measurements.

Table 1. AgNP Sizes According to the AFM Analysis.

AgNPs Rm-AgNPs Rg-AgNPs
AFM topography, particle diameter (nm) average; SD 56; s ≈ 6 85; s ≈ 7
AFM phase, protein layer thickness (nm) average; SD 24; s ≈ 2 21; s ≈ 2
AFM phase, protein solid core diameter (nm) average; SD 37; s ≈ 2 71; s ≈ 7
SEM image, particle diameter (nm) average; SD 30; s ≈ 3 58; s ≈ 9
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Photoluminescence (PL) spectroscopy is an effective technique to study the optical properties of silver nanoparticles to evaluate potential applications of materials, such as in photonics. PL emission spectra are shown in Figure 4 for excitation with a blue laser (λ = 473 nm, 2.62 eV). The spectra shown in Figure 4a,b were acquired for different nanoparticles, but all of the spectra for the same Rg or Rm fungus species are similar, with a very broad peak at 570 nm. Similar spectra have been reported in the literature for AgNPs stabilized in soluble starch20 as well as for AgNPs biologically synthesized by fungi.21 Variations in the emission wavelength could come from size deviations,22,23 but this was not observed in the spectra shown in Figure 4a,b, indicating homogeneity in the sizes of the NPs analyzed.

Figure 4.

Figure 4

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Photoluminescence measurements for (a) R. glutinis and (b) R. mucilaginosa.

SERS is an extension of Raman spectroscopy that explores the enhanced local fields at metallic nanostructures, thus allowing for the detection of very small amounts of sample.24 Representative Raman spectra of the AgNPs acquired with a green laser (2.33 eV) are shown in Figure 5c,d. The spectra have well-defined peaks and improved sensitivity due to the SERS effect. The most characteristic bands are associated with the CONH group, referred to as amides I to VII, with the vibrational assignments according to Table 2. Most of the peaks shown in Figure 5c,d are in the region from 1200 to 1700 cm–1 and could be assigned to C–O stretching, N–H bending, and C–N stretching.25 Thus, considering that amide II has a very weak Raman signal, the peaks could be related mostly to amides I and III. It is not possible to classify the proteins according to their secondary structures, i.e., α-helix, β-sheet, and protein mixed structures (α/β, α + β), based on the obtained Raman spectra due to the large amount of peaks distributed in a wide range of frequencies. These peaks might be related to α-helix or β-sheet structures. However, narrow and relatively intense Raman bands are found between 500 and 900 cm–1 both in M3 and G3 spectra and this can be associated with protein mixed structures.25,26

Figure 5.

Figure 5

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(a) Time series Raman spectra in a single point of Rm-AgNPs and (b) Rg-AgNPs with an acquisition time of 0.1 s per spectrum. (c) Selected Raman spectra of the sample Rm-AgNPs indicated in the lines M1, M2, and M3 of image (a). (d) Selected Raman spectra of the sample Rg-AgNPs indicated in the lines G1, G2, and G3 of image (b).

Table 2. Raman Shift of AgNPs Produced by R. glutinis and R. mucilaginosa.

R. glutinis and R. mucilaginosa assignmenta
1600–1690 cm–1 amide I, C=O stretching/hydrogen bonding coupled with COO
1480–1580 cm–1 amide II, N–H groups bending vibrations, C–N stretch
1230–1300 cm-1 amide III, C–N stretch, 30% N–H bend, C–C stretching, C–H flexion
625–770 cm–1 amide IV, OCN bending
640–800 cm–1 amide V, out-of-plane NH bending
540–600 cm–1 amide VI, out-of-plane C=O bending
200 cm–1 skeletal mode
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a

Refs (30−35).

The Raman spectra vary with time for acquisitions at the same sample spot, even for small acquisition times. This fact was investigated in time series measurements in a single spot, in which 100 measurements were made using 0.1 s for each acquisition, with an elapsed time between acquisitions of 1 s due to experimental limitations of the equipment. The acquired spectra are shown in Figure 5a,b for Rm- and Rg-AgNPs, respectively, with selected spectra shown in Figure 5c,d for the indicated orange lines. The peaks at around 500, 900–1000, and 1600 cm–1 might be assigned to a shift of the NH2 twisting, wagging, rocking, and scissoring modes, respectively, indicating an amine–silver interaction.26 Moreover, for both Rm- and Rg-AgNPs, the Raman spectra vanish (or become too weak) after approximately 40 and 55 s, respectively. The stabilization of biogenic AgNPs results from the capping protein structures, usually oligopeptides lying on the surface of the nanoparticle, thus conferring stability and preventing the oxidation of Ag0 to Ag+. Various substances can break this energy balance, leading to the collapse of the nanoparticle. The substances that cause this effect are those that alter the conformation structure of the oligopeptides or alter their load content, destabilizing the protein and consequently the silver nanoparticle. Among these, we can mention oxidizing or reducing agents, lasers, and heat.27,28 These may be some of the facts that can explain the instability of the Raman spectra described above; however, a relevant one to explain the temporal fluctuations may be due to the transfer of electrons that regulate the molecule–metal interaction under the excitation of light. This is particularly relevant for proteins due to the complex landscape and energy range that they possess together with the interlacing of vibrational modes.29

Another possible explanation for the instabilities observed in the Raman spectra might be related to modifications of the silver core, e.g., small changes in its shape, heating, or even melting due to the laser energy transfer. This hypothesis was verified employing a dark-field setup equipped with an additional HeNe laser, as described in the Experimental Details section. Dark-field microscopy is a very useful tool to study metal particles either in the biological or in materials science field.36,37Figure 6c shows a dark-field APD image of Rm-AgNPs by raster scanning a sample region; the bright points indicate the location of Rm nanoparticles. Figure 6a shows the scattered light for the chosen spots indicated in Figure 6c with 1 s of acquisition time for every spectrum. The image shown in Figure 6a is homogeneous, indicating the stability of the nanoparticle under these measurement conditions. Keeping the same experimental conditions, the HeNe laser was turned on and focused on the same sample spot. The acquired spectra thus obtained are summarized in Figure 6b. This figure is similar to Figure 6a up to about 75 s, which can be considered the starting time for a decrease in the scattering intensity. Figure 6d shows three sample spectra after a delayed time of 19, 99, and 166 s of sample exposure to the HeNe laser. It is clear that the peaks weaken their intensities, although they do not alter their positions and/or widths. This is good evidence that, besides the protein conformations, the metallic cores are also affected by the laser. It is important to comment that Rg-AgNPs exhibit a similar behavior. Throughout both sample materials, the degree as to which the scattering spectra were influenced by laser heating was very diverse. A possible cause for this behavior is the diversity in the microscopic shape of the individual particles (cf. Figure 2). Figure S1 of the Supporting Information shows a Raman time series measurement on the exact same samples used to acquire Figure 6 but on different particles. Due to experimental limitations, we cannot have Raman and DF + laser in the same region, but Figure S1 supports our DF conclusions above by showing that the stability of the signal has the same time scale as the DF + laser illumination in Figure 6b.

Figure 6.

Figure 6

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Dark-field scattering images for the R. mucilaginosa sample using white light illumination (a) without additional red laser excitation and (b) with additional red laser turned on. The images were acquired in the spots indicated in image (c). (c) Dark-field image of the Rm-AgNPs made by raster scanning the sample with white light illumination. (d) Spectra on the orange lines indicated in image (b).

4. Conclusions

In this contribution, silver nanoparticles encapsulated by a protein-capping layer were studied by SEM, AFM, and optical spectroscopy techniques. These nanoparticles were produced by two fungi: R. glutinis and R. mucilaginosa. The AFM phase image allowed the estimation of the protein-capping layer width to be 21 nm (R. glutinis) and 24 nm (R. mucilaginosa). The enhanced Raman spectra obtained are very unstable, indicating that the structural conformations of the protein involving the silver core are affected by the laser and/or by the enhanced fields from the silver core. The results presented here allowed the identification of α-helix, β-sheet, and protein mixed structures. The protein–silver interaction seems to happen through the amine group. Raman spectroscopic signatures of this group could be identified for most particles. Dark-field measurements showed that not only the protein structure is affected by the laser but also the silver metallic core, contributing to the instabilities found in the Raman spectra, temporal fluctuations. Our results are important for defining the proper applications of biogenic nanoparticles and their limitations.

Acknowledgments

We gratefully acknowledge the financial support from Brazilian Agencies for Scientific and Technological Development: CNPq (408790/2016-4), CAPES (23038.000936/2018-46), and Funcap (PNE-0112-00048.01.00/16). A.R.P. thanks CNPq Universal call 01/2016 process number 426584/2016-3 for the financial support. The authors also thank the Central Analítica-UFC/CT-INFRA/MCTI-SISNANO/Pró-Equipamentos for the grant provided to support the research on nanoparticles.

Supporting Information Available

The Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/acsomega.9b02867.

  • Raman time series measurement on the same sample used for acquiring Figure 6 but on different particles: (a) time series Raman images of Rm-AgNP and (b) Rg-AgNP, (c) Raman spectra at the selected times shown in image (a) for Rm-AgNP, and (d) Raman spectra at the selected times shown in image (a) for Rg-AgNP (Figure S1); experimental details for Figure S1 (PDF)

The authors declare no competing financial interest.

Supplementary Material

ao9b02867_si_001.pdf (223.3KB, pdf)

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