Which Amino Acids are Capable of Nucleating Fluorescent Silver

Article pubs.acs.org/JPCC

Cite This: J. Phys. Chem. C XXXX, XXX, XXX−XXX

Which Amino Acids are Capable of Nucleating Fluorescent Silver Clusters in Proteins? Tomash S. Sych,† Andrey A. Buglak,† Zakhar V. Reveguk,† Vladimir A. Pomogaev,‡,§ Ruslan R. Ramazanov,† and Alexei I. Kononov*,† †

Department of Molecular Biophysics and Polymer Physics, Saint Petersburg State University, Saint-Petersburg 199034, Russia Department of Physics, Tomsk State University, Tomsk 634050, Russia § Department of Chemistry and Green-Nano Materials Research Center, College of Natural Sciences, Kyungpook National University, 1370 Sankyuk-dong, Buk-gu, Daegu 702-701, Republic of Korea

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‡

S Supporting Information *

ABSTRACT: In this experimental and theoretical joint study, we used single amino acids as model systems for studying protein−cluster interactions. We probed 12 natural amino acids with different functional groups as potential templates of fluorescent silver (Ag) nanoclusters obtained by sodium borohydride reduction of Ag ions. We also calculated the Gibbs free energies of the complexes formed between Ag+ ions, Ag atoms, and two-atom Ag clusters with the amino acids’ various functional groups. Only cysteine and tyrosine could form fluorescent complexes with Ag clusters. This agrees with the calculated Gibbs free energies for the Ag cluster−amino acid complexes. We also show that the tyrosine-based fluorescent Ag cluster could be obtained using a green synthetic method in which tyrosine, at alkali pH, acts as a reducing agent. The optimized structure of a complex of Ag3+ cluster with three semiquinone tyrosine rings is proposed. These results can be used in designing and synthesizing new peptidetemplated biolabels.

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INTRODUCTION Metal nanoclusters (NCs) are a special class of materials with molecule-like optical properties1−3 that appear distinctly different from the optical features of metal nanoparticles.4 With the decreased size, the evolution of the continuous electronic band structure into distinct energy levels leads to well-defined electronic transitions.5 The molecular-like electronic structure of NCs results in a large energy gap between the NCs’ highest unoccupied molecular orbital (HOMO) and lowest unoccupied molecular orbital (LUMO), which may lead to photoluminescence, a unique property of NCs. Luminescent NCs are of special interest in chemistry and biology, as they can be applied in optoelectronics, bioimaging, and chemical sensing.6−19 The chemically stable gold NCs have been the most extensively investigated.15,16 However, fluorescent silver (Ag) clusters have a certain advantage as nanoemitters. Due to their high fluorescence quantum yield and absorption cross section, they exhibit excellent brightness and high photostability. Typically, Ag NCs are prepared by reducing Ag ions with the presence of various polymer templates in the solution.7−13,20−25 Biomolecule-protected NCs are of special interest for bioimaging applications. DNA-protected fluorescent Ag NCs have been synthesized in a wide spectral range, from visible to near infrared, varying DNA sequences, and synthesis conditions.8,10,11,19,26−28 The protein templates used © XXXX American Chemical Society

for synthesizing luminescent NCs also exhibit many advantages for sensing and bioimaging.29−31 Protein-protected gold NCs have been synthesized on many protein matrices, such as bovine serum albumin (BSA),32,33 lysozyme,33−35 trypsin,33 lactotransferrin,36 insulin,37 pepsin,33,38 and horseradish peroxidase.39 In contrast, there have been only a few studies on protein-protected fluorescent Ag NCs. Chymotrypsin,40 BSA,41−46 human serum albumin, egg albumin,47 and lysozyme48 have been used as templates for Ag NC synthesis. A few peptides have also been explored in the synthesis of fluorescent Ag clusters.49−52 Knowledge of the NC binding sites in protein matrices is vital for further design of fluorescent cluster−protein complexes and for tuning their spectral properties. At the same time, the NC nucleation sites in huge protein globules are not clear. It is possible for single amino acids (AAs) to be explored as model systems for studying protein−cluster interactions. Fluorescent Ag clusters have been synthesized using the modified phenylalanine (Phe)-based hydrogel template.53 To the best of our knowledge, there have been no reports on the synthesis of fluorescent Ag clusters in Received: September 13, 2018 Revised: October 18, 2018 Published: October 23, 2018 A

DOI: 10.1021/acs.jpcc.8b08979 J. Phys. Chem. C XXXX, XXX, XXX−XXX

Article

The Journal of Physical Chemistry C

half-maximum of about 2 ns. Emission bandpass was set at 14 nm. The quantum yield of the Ag−BSA complex was measured by the direct method using a Quanta-φ integrating sphere (Horiba Jobin Yvon). The quantum yield of the Ag−Cys cluster was estimated using the Ag−BSA complex as a reference. The fluorescence quantum yield of the Ag−Tyr cluster was measured using Tryptophan in water (QY = 0.20) as a reference.61 Absorption spectra were obtained with a Specord 210 Plus double-beam spectrophotometer (Analytik Jena).

solution using natural AAs. In this paper, we studied 12 natural AAs with different functional groups that can bind with Ag nanoclusters obtained by reducing Ag ions with sodium borohydride (NaBH4). We also calculated the Gibbs free energies of the complexes formed between Ag+ ions (Ag+), Ag atoms (Ag0), and two-atom Ag (Ag2) clusters with the AAs’ various functional groups. We show that cysteine (Cys) and tyrosine (Tyr) are the only natural AAs that can form complexes with fluorescent Ag clusters in a solution. This agrees with the calculated Gibbs free energies of the Ag cluster−AA complexes.

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RESULTS AND DISCUSSION Thiols can stabilize Ag clusters53 and fluorescent clusters.62,63 Accordingly, Cys can be expected to also stabilize fluorescent clusters. The Ag−Cys NCs were prepared by a common NaBH4 reduction of Cys−Ag+ complexes. The as-prepared Ag−Cys NCs exhibited a broad emission band with the maximum at about 800 nm (Figure 1). Table 1 presents the

EXPERIMENTAL AND THEORETICAL METHODS Chemicals. We investigated 12 natural AAs representing the different functional groups that can bind with Ag nanoclusters: leucine (Leu) and sulfur-containing methionine (Met) with nonpolar aliphatic R-groups; lysine (Lys), arginine (Arg), and histidine (His) with positive-charge R-groups; Cys and glutamine (Gln) with polar uncharged R-groups; aspartate (Asp) and glutamate (Glu) with negative-charge R-groups; and Phe, Tyr, and tryptophan (Trp) with nonpolar aromatic Rgroups. The AAs and BSA were purchased from Sigma-Aldrich. Synthesis of Clusters. Typically, 0.1 M AgNO3 solution was added to 1 mg/mL Cys and BSA solutions (other AAs, 0.1 mg/mL). Sodium hydroxide was added to the solutions before the addition of Ag nitrate to achieve the desired pH value of 12. The mixture was incubated for 1 h under vigorous stirring at room temperature. Next, freshly prepared 10 mM NaBH4 solution was added dropwise, and the mixture was kept at 4 °C in the dark until further analysis (usually after 24 h). The optimal molar ratios were as follows: 1.1:1 Ag/Cys and 1:1 NaBH4/Ag for Cys; 1:1 Ag/AA and 1:1 NaBH4/Ag for other AAs. The as-synthesized mixture was centrifuged for 5 min at 10 000 rpm and sediment was filtered off. For BSA, the final molar ratios were 30:1 Ag/BSA and 1:10 NaBH4/Ag. The Ag− Cys solution was diluted three times before taking the spectra. Gibbs Free Energy Calculation for Ag−AA Complexes. The geometries of all complexes were optimized using the Hartree−Fock second-order Møller−Plesset perturbation theory with a resolution of identity approximation (RI-MP2) realized in the ORCA 3.0 program package.54 The 6-31G + (d) basis set was used in all geometry optimizations and Hessian calculations. Ag atoms were treated with effective core potential def2TZVP.55,56 Calculation of the Electronic Absorption Spectrum. The geometry of the complex of Ag3+ cluster with three semiquinone tyrosine rings was optimized using RI-MP2 method with 6-31G(d) basis set, silver atoms were treated with effective core potential LANLTZ.57,58 The electronic absorption spectrum of the complex was calculated at the G09 M062X59/def2TZVP/P56 level of theory. Spectral Methods. Fluorescence emission and excitation spectra and fluorescence decay curves were obtained at room temperature using a Fluorolog-3 spectrofluorometer (Horiba Jobin Yvon). The measurements were carried out using a 0.4 cm quartz cuvette. Long-wave pass filters were used to remove scattered light. The fluorescence emission spectra were corrected for instrument sensitivity. The fluorescence excitation spectra were corrected for the inner filter effect due to the high absorbance of the samples in the UV range as described elsewhere.60 The bandpass for excitation and emission was set at 5 nm. Fluorescence lifetime measurements were performed with light-emitting diodes with full width at

Figure 1. Fluorescence excitation and emission spectra of the Ag−Cys complex (λex 520 nm, λem 780 nm) and Ag−BSA complex (λex 500 nm, λem 700 nm). All spectra are normalized to their peaks.

dependence of the fluorescence intensity on the reagents’ ratio. The maximal yield of the emitting clusters was achieved at 1.1 Ag+/Cys and 1.0 Ag+/NaBH4 ratios. The fluorescence excitation spectrum (Figure 1) was measured using a dilute Ag−Cys solution to cover a wide spectral range from 300 nm, where the sample absorbance increased significantly. The fluorescence excitation spectrum had three main peaks at about 520, 420, and ∼300 nm (Figure 1). It resembled the excitation spectrum of the Ag clusters in BSA (shown in the same figure), although the excitation and emission spectra of the Ag−Cys NCs were shifted to the red side as compared to BSA. The fluorescence decay curves of the Cys- and BSA-protected clusters (Figures S1 and S2) exhibited practically the same lifetimes of the major components, i.e., 1.4 and 1.2 ns, respectively. Thus, it can be supposed that Cys residues stabilize the fluorescent clusters in BSA. The red shift (ca. 0.15 eV) of the fluorescence excitation and emission bands in the case of the free AA can be explained by the difference in environment. The fluorescence quantum yields for Ag clusters in BSA and Cys were 20 and 1%, respectively. However, for Cys, this value may have been significantly underestimated due to the absorption and scattering of the excitation light by nonfluorescent Ag nanoparticles. We varied the pH conditions of the cluster formation in a wide range. Figure S3 shows the pH dependence of the fluorescence intensity. Cys had three pKa values associated with carboxyl, amino, and thiol groups: 1.71, 10.78, and 8.33, respectively.64 The fluorescent Ag−Cys complexes were formed at pH > 10, reaching the maximum effect at pH 12 B


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Table 1. Dependence of the Fluorescence Intensity at 790 nm (Excitation [λex] at 520 nm) of Ag−Cys Clusters on the Molar Ratios of Reagents NaBH4/Ag+ molar ratio normalized fluorescence intensity at 790 nm (λex 520 nm) Ag+/Cys molar ratio

0.25 0.5 1 1.1 1.3 2

0.1

0.25

0.5

1

2

3

4

0.00 0.00 0.07

0.00 0.02 0.14

0.08 0.11 0.50 0.86 0.59 0.00

0.23 0.70 0.46 0.13

0.00

0.00 0.09 0.42 1.00 0.61 0.00

0.28 0.83 0.68 0.30

0.00

0.00 0.05 0.28 0.44 0.56 0.00

successfully applied for synthesizing fluorescent Ag clusters. Figure 2 shows the fluorescent emission spectrum of the clusters acquired 1 h after mixing the AA with Ag nitrate. It is worth noting that the Ag−Tyr cluster remained stable at room temperature at least for 1 month. The maximal yield of the clusters was achieved at 1:1 Ag/Tyr molar ratio (Figure S5) and pH 12 (Figure S6). The as-prepared Ag−Tyr fluorescent complex could be purified using high-performance liquid chromatography (HPLC) (Figures S7 and S8). Excitation spectrum appears to be of similar shape as the absorption spectrum of the HPLC-purified cluster (Figure 2), which implies that mostly one specie is present. A band at 450 nm is attributed to nonfluorescent species. We calculated a quantum yield value of 0.4 using Tryptophan solution as a reference. Table 2 summarizes the fluorescence characteristics of the Ag clusters synthesized on BSA, Cys, and Tyr matrixes. Inspired by our previous observations that the complexes of Ag3+ cluster with carbonyl groups of thymine had the absorption peak at about 320 nm,66 we obtained the QMoptimized structure of a complex of Ag3+ cluster with three semiquinone tyrosine rings (Figure 2). The stick spectrum of this complex calculated at G09 M06-2X/def2TZVP/P level (Figure 2) is very close to the experimental excitation spectrum of the tyrosine-based Ag cluster. The other AAs probed in our study did not form fluorescent complexes with the Ag clusters. The fluorescence signal coincided with the background fluorescence at all pH ranges from 2 to 12, at which the synthesis was carried out; it is illustrated in Figure S9 for His. However, most AAs were able to stabilize Ag nanoparticles at alkali pH. Figure S10 shows the UV spectra for Ag+−AA solutions after reduction with NaBH4. All the solutions, except that with Cys, Leu, Phe, and Arg, exhibited a typical plasmonic band at about 400 nm, which indicates the formation of Ag nanoparticles. To explain why only Cys and Tyr were capable of forming fluorescent Ag clusters, we calculated the Gibbs free energies for the complexes formed between Ag+ ions, Ag atoms, and two-atom Ag clusters with the AAs’ various functional groups. The functional R-groups of Cys, Tyr, and aspartic and glutamic acids had the highest Gibbs free energies (Table 3). These results suggest that the Cys and Tyr complexes with small Ag clusters can truly be more stable in comparison with that

(Figure S3). In these conditions, all the groups were deprotonated. In the case of BSA, however, the carboxyl and amino groups formed peptide bonds. Therefore, it can be concluded that the deprotonated thiol groups stabilized the Ag NC clusters. Tyr was also able to form a fluorescent complex with Ag clusters. Figure 2 presents the fluorescence excitation and

Figure 2. Fluorescence excitation and emission spectra of the Ag−Tyr complex (λex 320 nm, λem 420 nm); absorption spectrum of the fraction eluted in high-performance liquid chromatography (HPLC) at 4.66 min (all spectra are normalized to their peaks). Stick spectrum of the complex of Ag3+ cluster with three semiquinone tyrosine rings (shown at right) calculated at G09 M06-2X/def2TZVP/P level.

emission spectra of the Ag cluster−Tyr complexes. The excitation spectrum exhibited the lowest-energy transition at ca. 320 nm. The emission band was located at about 400 nm. Similar excitation/emission maxima were observed for the complex of Ag clusters with a Tyr-containing peptide.50 The fluorescence decay of the Tyr-based Ag cluster exhibited two components with the lifetimes of 1.3 ns (57%) and 5.3 ns (43%) (Figure S4), which implies a relatively high fluorescence quantum yield. It appears that the same fluorescent clusters can be synthesized more effectively without the addition of NaBH4. At alkali pH, Tyr can act as a reducing agent in the synthesis of Ag nanoparticles.65 In doing so, the phenolic form of Tyr converts to the semiquinone form.65 Here, we show for the first time that the same green synthetic method can be

Table 2. Fluorescence Characteristics of the Ag Clusters Stabilized by BSA, Cys, and Tyr matrix

BSA

Cys

Tyr

emission maximum, eV excitation maxima, eV average fluorescence lifetime, ns fluorescence quantum yield

1.73 2.5; 3.0; 4.0 1.7 20%

1.57 2.4; 2.9; >3.5 1.5 1%

3.1 4.0 1.8 40%

C


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optimized structure of a complex of Ag3+ cluster with three semiquinone tyrosine rings is proposed. These results can be used in the design of novel effective protein- and peptide-based biolabels.

Table 3. Gibbs Free Energies for Ag+, Ag0, and Ag2 Binding with AA Functional Groups compound Ag+_CH3NH2 Ag0_CH3NH2 Ag2_CH3NH2 +

Ag _imidazole Ag0_imidazole Ag2_imidazole Ag+_CH3COO−1 Ag+_CH3COO−1 Ag0_CH3COO−1 Ag0_CH3COO−1 Ag2_CH3COO−1 Ag2_CH3COO−1 Ag+_CH3CONH2 Ag0_CH3CONH2 Ag2_CH3CONH2 Ag+_phenolate Ag0_phenolate Ag2_phenolate Ag+_CH3OH Ag0_CH3OH Ag2_CH3OH Ag+_CH3SCH3 Ag0_CH3SCH3 Ag2_CH3SCH3 Ag+_CH3S− Ag0_CH3S− Ag2_CH3S−

bond 1 Ag−N Ag−N Ag−N 2 Ag−N Ag−N Ag−N 3 Ag−O1 Ag−O2 Ag−O1 Ag−O2 Ag−O1 Ag−O2 4 Ag−O Ag−O Ag−O 5 Ag−O Ag−O Ag−O 6 Ag−O Ag−O Ag−O 7 Ag−S Ag−S Ag−S 8 Ag−S Ag−S Ag−S

ΔG, kcal/mol

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ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.jpcc.8b08979. Fluorescence decays of the Ag clusters, pH dependence of the fluorescence intensity of the Ag−Cys and Ag−Tyr clusters, chromatograms of the Ag−Tyr solution, fluorescence emission spectra of the Ag−His complexes at different pH values, absorption spectra of the Ag−AAs complexes (PDF)

−71.03 −25.42 −7.47 −177.58 −40.25

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−28.87

AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected].

−61.79 −22.01 −3.12

ORCID

Tomash S. Sych: 0000-0002-7799-4950 Andrey A. Buglak: 0000-0002-6405-6594 Zakhar V. Reveguk: 0000-0001-5475-3030 Vladimir A. Pomogaev: 0000-0003-4774-3998 Ruslan R. Ramazanov: 0000-0002-3019-8762 Alexei I. Kononov: 0000-0001-5787-3599

−164.92 −38.39 −26.24 −50.14 −22.08 −1.18

Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This work was supported by the Russian Science Foundation (project 16-13-10090). Spectral measurements were performed using equipment of Centre for Optical and Laser Materials Research and Chemical Analysis and Materials Research Centre of Saint Petersburg State University.

−58.76 −22.61 −3.44 −192.01 −50.99 −42.83

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formed with other AAs. This is line in with the above experimental findings, where only Cys and Tyr formed fluorescent complexes with Ag clusters in a solution. Although the carboxyl groups of the aspartic and glutamic acids also exhibited high affinity to the Ag2 cluster, no fluorescent Ag clusters were formed in the solutions of these AAs. Of course, the Ag2 cluster is a very simple model. Although theoretical calculations show that the fluorescent ligand-stabilized Ag clusters may be of small size indeed,28,67 the detailed structure of the fluorescent clusters is not known. Besides the energetic aspect, other factors can play a role in the formation of the fluorescent clusters. Probably, some stereochemical aspects are also important for the formation of the Ag−ligand fluorescent complexes, which requires further investigations.

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CONCLUSIONS Cys and Tyr are the only natural AAs that can form complexes with fluorescent Ag clusters. This finding is supported by the Gibbs free energies derived for the complexes formed between Ag+ ions, Ag atoms, and two-atom Ag clusters with the AAs’ various functional groups. We also show that the Tyr-based fluorescent Ag cluster can be obtained using a green synthetic method, where Tyr acts as a reducing agent at alkali pH. The D


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