Remote Optically Controlled Modulation of Catalytic Properties of

Sep 24, 2016 - Catalytic Properties of Nanoparticles through. Reconfiguration of the Inorganic/Organic. Interface. Randy L. Lawrence,. †. Billy Scol...
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Remote Optically Controlled Modulation of Catalytic Properties of Nanoparticles through Reconfiguration of the Inorganic/Organic Interface Randy L. Lawrence,† Billy Scola,† Yue Li,‡ Chang-Keun Lim,§ Yang Liu,‡ Paras N. Prasad,*,§ Mark T. Swihart,‡ and Marc R. Knecht*,† †

Department of Chemistry, University of Miami, 1301 Memorial Drive, Coral Gables, Florida 33146, United States Department of Chemical and Biological Engineering and §Department of Chemistry and Institute for Lasers, Photonics, and Biophotonics, University at Buffalo, The State University of New York, Buffalo, New York 14260, United States

‡

ABSTRACT: We introduce here a concept of remote photoinitiated reconfiguration of ligands adsorbed onto a nanocatalyst surface to enable reversible modulation of the catalytic activity. This is demonstrated by using peptide-ligand-capped Au nanoparticles with a photoswitchable azobenzene unit integrated into the biomolecular ligand. Optical switching of the azobenzene isomerization state drives rearrangement of the ligand layer, substantially changing the accessibility and subsequent catalytic activity of the underlying metal surface. The catalytic activity was probed using 4-nitrophenol reduction as a model reaction, where both the position of the photoswitch in the peptide sequence and its isomerization state affected the catalytic activity of the nanoparticles. Reversible switching of the isomerization state produces reversible changes in catalytic activity via reconfiguration of the biomolecular overlayer. These results provide a pathway to catalytic materials whose activity can be remotely modulated, which could be important for multistep chemical transformations that can be accessed via nanoparticle-based catalytic systems. KEYWORDS: Au nanoparticles, peptides, biointerface reconfiguration, catalysis, photoactivated switch

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affinity between the ligand and NP must be sufficiently strong that the ligands do not dissociate from the surface; and (3) the reconfiguration process should be remotely triggered. Peptides have emerged as ideal passivants to meet the first two conditions and unlock the ability to reconfigure NP interfacial structures.20,21 Peptides have been isolated with affinity for numerous inorganic compositions.22−24 These typically bind the NP surface through multiple weak, noncovalent interactions.21,24,25 Collectively, these interactions rival the overall binding affinity of covalently attached ligands, but they are individually weak enough to allow for passivant reconfiguration.24 To meet the third key condition, a photoisomerizable azobenzene26−31 can be incorporated into the peptide to reversibly change the conformation of the biomolecular overlayer structure.20,21 This capability has been demonstrated by incorporating azobenzene into the Au-binding AuBP1

anoparticle (NP) catalysts provide high specific surface areas and corresponding high specific catalytic activity.1 Unsupported, dispersed NP catalysts must be passivated with ligands to prevent their aggregation,2−8 and these ligands inevitably block a portion of the metallic surface, diminishing catalytic activity. The conformation of the organic/ inorganic interface can be optimized for a single reaction;9 however, different interfacial structures are optimal for different reactions.10−15 Creation of ligands that allow reconfiguration of an inorganic−organic interface would enable selective alteration of catalytic reactivity, with different configurations of the interface optimized for different reactions. While reconfigurable interfaces are desirable for catalysis, most organic ligands employed with metal NPs cannot change conformation. Typically, they are rigidly bound to the NP surface through a single covalent interaction (i.e., alkanethiols on Au16), locking them into a static orientation.17−19 To generate reconfigurable interfaces, three key conditions must be met: (1) Individual interactions between the NP and ligand must be sufficiently weak to permit structural changes; (2) the © 2016 American Chemical Society

Received: July 8, 2016 Accepted: September 24, 2016 Published: September 24, 2016 9470

DOI: 10.1021/acsnano.6b04555 ACS Nano 2016, 10, 9470−9477

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peptide (WAGAKRLVLRRE),32 where these hybrid biomolecules were used to fabricate Au NPs.20,21,24 Photoswitching of the azobenzene can then result in dramatic and reversible reconfiguration of the NP inorganic/organic interface.31 Here, we demonstrate the switching capabilities of biohybrid molecules to directly and reversibly manipulate the catalytic activity of colloidally dispersed NPs. In our interface design, we linked the AuBP1 peptide with an azobenzene photoswitch at either its N- or C-terminus. Four distinct configurations, differing in the position of the azobenzene and its isomerization state (trans vs cis), were considered. Once the NPs were prepared and characterized, their catalytic activity for the reduction of 4-nitrophenol to 4-aminophenol was quantified. This reaction is highly sensitive to the NP surface structure33,34 and is thus valuable as a probe of the effects of interface reconfiguration. The catalytic activity proved to be highly sensitive to the interface configuration, where the position of the photoswitch was important for both NP stability and catalytic activity. Most importantly, the reactivity was reversibly changed though optically driven interface reconfiguration over multiple switching cycles. These results demonstrate an approach to directly and reversibly manipulate the catalytic activity of dispersed NPs via a remotely triggered process. Refining these capabilities could provide a means to guide multiple reactions in complex solutions by turning on and off reactivity for individual steps to minimize byproduct generation and maximize production of desired products.

RESULTS AND DISCUSSION Hybrid Biomolecules. Photoswitchable peptides were produced using an azobenzene flanked by two maleimide groups, termed MAM.21 The maleimide moieties are used to couple the photoswitch into the peptide at a free thiol group. For this purpose, a cysteine residue was appended at either the N- or C-terminus of the parent AuBP1 sequence. Hereafter, MAM−CAuBP1 represents the molecule with the azobenzene at the N-terminal cysteine, while AuBP1C−MAM denotes the hybrid biomolecule with the azobenzene incorporated at the Cterminal cysteine (Scheme 1). Coupling of the two species and purification of the product are straightforward, as previously described.21 The final structure of each purified hybrid biomolecule was confirmed by MALDI-TOF mass spectrometry prior to use. Scheme 1b presents the binding pattern of the four different structures of the biomolecule to the Au surface. As previously demonstrated via computational modeling,20,21 the configuration of the azobenzene in the MAM unit can have significant effects on the binding pattern of the individual residues of the peptide, thus substantially altering the peptide structure on the Au NP surface. The color palette used in the scheme represents the percentage of persistent contact of the individual residues with the metallic surface, which is notably affected by the position of the MAM unit within the peptide sequence and its cis or trans state. Note that noncovalent interactions dominate the binding events between the hybrid biomolecules and the Au NPs. Nanoparticle Synthesis, Characterization, and Biointerface Reconfiguration via Photoswitching. Au NPs capped with the hybrid biomolecules were fabricated using standard methods. This was carried out by mixing either AuBP1C−MAM or MAM−CAuBP1 in the trans conformation with Au3+ ions at a 2:1 metal to peptide ratio, followed by reduction with excess NaBH4. During this reaction, a color

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(a) Switchable catalytic capabilities. In one biomolecule configuration, the surface of the catalyst is minimally exposed; however, upon photoswitching of the biomolecular structure, enhanced metal exposure occurs to increase catalytic rates. (b) Contact score analysis for the hybrid biomolecules.21 The binding of the overall biomolecule to the Au surface, and thus its conformation on the NP, varies based upon the position and isomerization state of the MAM unit.

change from pale yellow to brownish-red was observed, consistent with Au NP production. The resulting NP dispersions were quite stable with no precipitation noted, even after 1 week. The Au NPs were initially characterized via UV−vis spectroscopy, as shown in Figure 1a and b. For both the AuBP1C−MAM and MAM−CAuBP1 systems, spectra of the hybrid biomolecule alone, complexed with Au3+, and after reduction with NaBH4 were measured. For the AuBP1C− MAM system specifically (Figure 1a), the peptide exhibited a strong absorbance at 320 nm and a weak absorbance at 450 nm, corresponding to the n−π* and π−π* transitions of the azobenzene moiety, respectively.31 When the peptide was complexed with the Au3+ ions, no significant changes in the spectrum were noted; however, the weaker π−π* transition was no longer distinguishable from the background. After reduction, a significant increase in absorbance toward shorter wavelengths was noted, consistent with Au NP formation. While the π−π* transition was masked by the NP absorbance, the 320 nm n−π* transition of azobenzene remained observable, providing an optical handle to monitor isomerization of the photoswitch. Nearly identical results were obtained for the MAM−CAuBP1 species (Figure 1b). 9471

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Figure 2. Photoswitching of the azobenzene structure monitored via UV−vis absorbance. Parts (a) and (b) show the decrease in intensity of the 320 nm peak of azobenzene upon UV light exposure, confirming trans to cis switching of (a) AuBP1C−MAM and (b) MAM−CAuBP1 molecules on the AuNP surface. Photoswitching with visible light produced an increase in the 320 nm absorbance, shown in parts (c) for AuBP1C−MAM and (d) for MAM−CAuBP1, reflecting cis to trans switching.

Figure 1. UV−vis and TEM characterization of the peptide-capped Au NPs. (a, b) UV−vis absorbance spectra and (c, d) TEM images of (a, c) AuBP1C−MAM- and (b, d) MAM−CAuBP1-capped Au NPs. All NP synthesis and analysis shown here were conducted with the MAM in the trans configuration.

TEM imaging of the biomolecule-capped Au NPs was completed to quantify particle size distribution. For the particles capped with either AuBP1C−MAM (Figure 1c) or MAM−CAuBP1 (Figure 1d), the MAM moiety was in the trans configuration during synthesis. The resulting NPs were spherical with diameters of 2.7 ± 0.7 and 2.4 ± 0.6 nm for AuBP1C−MAM- and MAM−CAuBP1-capped Au NPs, respectively. Such sizes are consistent with the lack of observable LSPR absorbance in the UV−vis spectra, as the particles are too small to support a well-defined LSPR. Once the material structure was confirmed, photoswitching of the MAM moiety on the inorganic surface was tested. Under UV illumination, the azobenzene group isomerizes from the trans to cis state. It returns to the trans state upon irradiation with 440 nm light or by simple heating.31 Figure 2a presents the photoswitching analysis for the AuBP1C−MAM peptide on the Au NP surface. Photoswitching was monitored by changes in the 320 nm absorbance of the azobenzene. For these NPs capped with the peptide in the trans form, upon exposure to 365 nm light for 30 min, the azobenzene peak intensity diminishes, consistent with trans to cis switching. 20,21 Irradiation for longer times produced no further change, as the photostationary state was reached in under 30 min. To reverse the process and switch the peptide back to the trans conformation, the NPs were irradiated with 440 nm light, resulting in an increase in the 320 nm absorbance, confirming the switching event. As shown previously, the process is fully reversible and can be repeated over several switching cycles without inducing aggregation or precipitation of the NPs.20,21 Again, nearly identical switching results were noted for the MAM−CAuBP1 system, suggesting that the azobenzene is readily able to photoisomerize on the NP surface when attached at either end of the peptide. Prior computational modeling studies have shown that the azobenzene switching process is propagated through the peptide structure on the NP surface, resulting in a significant restructuring of the biomolecule overlayer.21 Scheme 1 presents the contact anchor score for each residue of both the

AuBP1C−MAM and MAM−CAuBP1 peptides in either the trans or cis configuration of the azobenzene unit.21 From this, clear changes in the anchoring of the peptides to the Au NP surface are evident, giving rise to the significant structural shifts of the biomolecular overlayer. Note that the azobenzene unit remains strongly adsorbed to the Au NP surface in both the cis and trans conformations. CD spectroscopy confirmed the changes in the peptide structure as a result of azobenzene switching.21 In this regard, the peptides on the Au NP demonstrated variations in the ellipticity of the peak at 198 nm. This peak is associated with the random coil peptide structure, which is anticipated for short sequences such as AuBP1. Control studies of the azobenzene free peptides demonstrated no changes in CD spectra upon exposure to UV or visible light, as expected, confirming the effect of the azobenzene in switching the biomolecular overlayer. As the trans conformation of the azobenzene molecule is more thermodynamically stable than the cis, thermally driven cis to trans isomerization can occur without visible light exposure.31 To assess the lifetime of the cis conformation, the half-life of the peptides with the azobenzene in the cis conformation was determined at room temperature. This was studied for both the free hybrid biomolecules in solution and on the Au NP surface. For this, each system was irradiated with 365 nm light for at least 30 min to reach the photostationary state. Their UV−vis absorbance was then monitored over a 24 h period to measure the rate of cis to trans isomerization. Figure 3 presents the thermal switching analysis for all four systems (two peptides either free in solution or bound to the NP surface). The analysis for the free AuBP1C−MAM in solution is shown in Figure 3a. In this case, the half-life of the cis conformer was 3.4 ± 1.5 h, which is comparable to that of other azobenzene-containing molecules; half-lives ranging from 0.7 s to 43 h have been measured depending on the structure of molecules attached to the azobenzene moiety.35 9472

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Figure 3. Analysis of the thermally driven azobenzene switching of the biohybrid molecules. Each panel shows the growth in intensity of the 320 nm absorbance over time. Panels (a) and (b) show results for free and surface-bound AuBP1C−MAM, respectively, while (c) and (d) show the same results for MAM−CAuBP1.

Figure 4. Analysis of the 4-nitrophenol reduction reaction catalyzed by Au NPs capped with AuBP1C−MAM in the trans configuration. Part (a) shows a sequence of UV−vis absorbance spectra. The decrease in absorbance at 400 nm as a function of time is plotted in part (b). Part (c) displays a plot of ln(A/A0) vs time from which a pseudo-first-order rate constant was determined. Finally, part (d) presents an Arrhenius plot used to determine the activation energy.

For the AuBP1C−MAM peptide bound to the NP surface (Figure 3b), a substantially longer half-life of 321 ± 22 h was determined. This change is likely a result of the strong interaction of the MAM unit with the inorganic surface, as identified in prior studies.20,21 This interaction inhibits thermally induced switching by constraining the MAM at the NP surface, consistent with previous studies of azobenzene molecules in various constrained systems.21 The thermal isomerization of the MAM−CAuBP1 molecule was similar to that of the AuBP1C−MAM (Figure 3c and d). Half-lives of 2.9 ± 0.1 and 315 ± 53 h were measured for the free and NPbound MAM−CAuBP1 biomolecule, respectively. Thus, over the time frame of all experiments conducted here, thermal isomerization of the surface-bound molecules is negligible. Biointerface Reconfiguration Effects on Catalytic Activity of Au NPs. Changes in configuration of the peptide layer on the Au NP surface can reasonably be expected to produce corresponding changes in catalytic activity; alterations in molecular conformation at the NP surface can change the number and identity of exposed active sites on the metal surface. Here, we employed Au NP-catalyzed reduction of 4nitrophenol to 4-aminophenol by NaBH4 to probe these effects (Scheme 2). This well-studied reaction follows the Langmuir−

absorbance at 400 nm (Figure 4a). Figure 4b presents the change in absorbance as a function of time, showing that the reaction was complete within 200 s. Analysis of the central portion of the absorbance (A) vs time data allows extraction of the pseudo-first-order rate constant. Figure 4c plots ln(A/A0) vs time, where A0 is the initial absorbance, and A/A0 is proportional to the fraction of the initial 4-nitrophenol remaining. The slope of this plot gives the rate constant.2 For the Au NPs capped with the AuBP1C−MAM in the trans configuration at 20 °C, this analysis delivers a rate constant of (9.0 ± 1.0) × 10−3 s−1. Repeating the kinetic analysis in triplicate at several temperatures allows for the determination of the activation energy (Ea) for the reaction. For the AuBP1C− MAM system in the trans configuration, the rate constants at the selected reaction temperatures are listed in Table 1 and compared in Figure 5a. The rate constant linearly increased from (10.9 ± 0. 3) × 10−3 s−1 at 25 °C to (16.6 ± 2.0) × 10−3 s−1 at 40 °C, yielding an activation energy (Figure 4d) of 23.0 ± 3.5 kJ/mol. To study the kinetics of 4-nitrophenol reduction with MAM in the cis state, the NPs were illuminated with 365 nm light for 30 min to reach the cis-dominant photostationary state. Reduction of 4-nitrophenol at 20 °C in the presence of the resulting Au NPs yielded a pseudo-first-order rate constant of (4.2 ± 1.0) × 10−3 s−1. This value is more than a factor of 2 smaller than that obtained with the Au NPs capped with the same biomolecule in the trans conformation ((9.0 ± 1.0) × 10−3 s−1). The reaction was subsequently carried out at temperatures up to 40 °C (Table 1, Figure 5b), from which an Ea value of 35.3 ± 4.0 kJ/mol was determined for 4-nitrophenol reduction in the presence of the AuBP1C−MAM Au NPs in the cis state. This activation energy is significantly greater than that obtained with the trans-AuBP1C−MAM Au NPs. This further demonstrates the sensitivity of the catalytic activity to the configuration of the biomolecule overlayer. When the reduction of 4-nitrophenol was studied using the MAM−CAuBP1-capped Au NPs, with the azobenzene at the N-terminus of the peptide, different results were obtained.

Scheme 2. 4-Nitrophenol Reduction Reaction

Hinshelwood mechanism, occurring directly on the NP metal surface in the presence of NaBH4.34 When the NaBH4 is in substantial excess, the reaction follows pseudo-first-order kinetics with respect to 4-nitrophenol,2,34,36 allowing for a simple and direct analysis of the effect of changes in the biomolecular overlayer on reaction rates. Figure 4 displays the analysis for AuNPs capped with AuBP1C−MAM in the trans configuration. The reduction of 4nitrophenol concentration was monitored by the decrease in 9473

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Table 1. Comparison of Rate Constants and Activation Energies for the 4-Nitrophenol Reduction Reaction Driven by the Peptide-Capped Au NPs in the trans and cis State rate constants (103 s−1) peptide AuBPIC−MAM trans AuBP1C−MAM cis MAM−CAuBP1 trans MAM−CAuBP1 cis

20 °C 9.0 4.2 9.4 20.2

± ± ± ±

1.3 0.7 3.0 3.0

25 °C 10.9 8.9 12.1 9.7

± ± ± ±

30 °C

0.4 0.8 0.1 0.1

12.5 9.9 11.9 11.1

± ± ± ±

0.4 0.8 2.0 0.3

40 °C

activation energy (kJ/mol)

± ± ± ±

23.0 ± 3.5 35.3 ± 4.0

16.6 12.1 10.3 8.3

0.7 1.1 0.3 0.2

in contact with the metallic surface >60% of the time). Furthermore, for the MAM−CAuBP1 hybrid biomolecules, these anchor groups tend to be clustered at the biomolecule termini; however, for the C-terminally modified AuBP1C− MAM biomolecules, these anchors are more evenly distributed throughout the sequence. As such, a higher degree of colloidal stability is likely to be observed for the AuBP1C−MAM-based Au NPs, where the hybrid biomolecules have more extensive noncovalent interactions with the Au throughout the entire biomolecular structure, which is indicated in the catalytic analysis. In a final point, it is important to mention that the reaction process catalyzed by the peptide-capped NPs with the azobenzene in the cis state is truly driven from these materials in the cis conformation. Thermal switching does eventually drive isomerization back to the more stable trans state; however, this process is significantly slower than the 4nitrophenol reduction (hours vs seconds). Thus, the thermal conversion of the cis MAM moieties to the trans state during the course of the catalytic reaction is negligible. Recyclability and Reversibility. Once the catalytic activity of the NPs was established for all four variants of the Au NPs, the recyclability of the Au NP catalysts and reversibility of the isomerization-induced reactivity changes were analyzed. To probe the recyclability of the materials, the AuBP1C−MAMcapped Au NPs were tested in both trans and cis conformations at 30 °C (Figure 6a and b). In each case, once the reaction reached completion, sufficient 4-nitrophenol was added to reestablish the original substrate:catalyst ratio. Using the trans AuBP1C−MAM-capped Au NPs, the k values ranged from (14.0 ± 3.0) × 10−3 s−1 to (18.0 ± 1.0) × 10−3 s−1. Similarly, for the same NPs in the cis configuration, the rate constants were lower, at approximately 9.0 × 10−3 s−1, for each reaction cycle. In these studies, the interface state remained the same for repeated reactions. Even though the NPs remained catalytically active over multiple reaction cycles, it might be expected that switching the interfacial state could irreversibly change the surface structure, affecting the catalytic properties. To probe this effect (Figure 6c), the reactivity of the AuBP1C−MAM-capped Au NPs was again studied in the trans configuration at 30 °C, yielding a k value of (14.0 ± 3.0) × 10−3 s−1. The biointerface was then switched to the cis conformation and the catalytic activity was measured, demonstrating a rate constant of (11.0 ± 1.0) × 10−3 s−1. Upon reaction completion with the NPs in the cis conformation, the biointerface structure was reversed back to the starting trans configuration. In this state, the reaction rate was again measured, and an increased rate constant of (13.3 ± 0.3) × 10−3 s−1 was determined. This demonstrates that the initial reactivity was restored upon reversal of the photoswitching process, suggesting that after one complete switching cycle only minor changes in the NP surface structure occurred. The NPs were again photoswitched back to the cis state and

Figure 5. Comparison of the pseudo-first-order rate constants for the reduction of 4-nitrophenol driven via Au NPs capped with the (a) AuBP1C−MAM and (b) MAM−CAuBP1 peptides in the trans and cis configuration.

Using the trans MAM−CAuBP1-capped Au NPs at 20 °C, a k value of (9.4 ± 3.0) × 10−3 s−1 was obtained; however, when these same NPs were used with the MAM moiety in the cis conformation, a dramatic increase in the rate constant to (20.2 ± 3.0) × 10−3 s−1 was observed. This more than 2-fold increase in the reaction rate after isomerization to the cis state contrasts sharply with the more than 2-fold decrease in reaction rate observed upon switching the AuBP1C−MAM Au NPs to the cis state. This demonstrates that the change in the surface structure of the Au NPs is highly dependent upon the position of the MAM unit, which is known to dramatically impact the surface configuration of the peptide.21 Whether in the cis or trans state, the MAM−CAuBP1-capped Au NPs did not show the usual Arrhenius temperature dependence of the rate constant (Figure 5b), which was clearly observed for the AuBP1C−MAM-capped materials. The failure to exhibit a monotonic increase in rate constant with temperature is due to loss of colloidal stability (aggregation) at higher temperatures. This likely arises as the MAM− CAuBP1 peptides, in either the cis or trans configuration, have fewer significantly strong anchor groups to the Au surface as compared to the AuBP1C−MAM species (i.e., residues that are 9474

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CONCLUSION In summary, we have presented the first demonstration that the catalytic properties of metallic NPs can be directly manipulated via remotely triggered changes in the ligand overlayer structure. This was achieved via photoactuation of a photoswitch incorporated into materials binding peptides bound at the NP surface. Switching of the azobenzene resulted in reversible changes in the adsorbed peptide overlayer, which led to changes in the catalytic activity of the NPs. These results open a pathway toward achieving remotely controlled reactivity, where enhancements in such capabilities can be achieved through bioligand design. An ultimate goal of this research would be to achieve reactivity that is initiated and fully terminated through ligand overlayer structural changes. While our results have not fully accessed such capabilities, they demonstrate a conceptual approach to achieving such behavior. Changes in the peptide ligand structure are presently being explored to achieve such capabilities. MATERIALS AND METHODS Materials. HAuCl4 was purchased from Acros Organics, and NaBH4 was acquired from Sigma-Aldrich. Trifluoroacetic acid (TFA), tri-isopropyl silane (TIS), and 4-nitrophenol were obtained from Alfa Aesar, while acetonitrile, methanol, and N,N-dimethylformamide (DMF) were purchased from BDH Chemicals. Finally, all FMOCprotected amino acids, Wang resins, and coupling reagents were acquired from Advanced Chemtech. Ultrapure water (18.2 MΩ·cm) was used for all experiments, and all reagents were used as received. Peptide Synthesis and Azobenzene Coupling. Standard solidphase FMOC peptide synthesis protocols were used on a TETRAS peptide synthesizer (Creosalus).37 Peptides were cleaved from the Wang resins using a TIS/H2O/TFA cleavage cocktail and purified via reverse-phase HPLC. The purified peptides were confirmed using MALDI-TOF mass spectrometry. Coupling of the azobenzene moiety into the biomolecule followed previously published protocols.21 Briefly, the maleimide−azobenzene−maleimide molecule was synthesized and purified as previously described.21 It was then coupled into the peptide at the thiol groups of the cysteine residues following standard thiol−maleimide coupling protocols. Excess MAM was used to ensure that only a single peptide was coupled to each MAM unit. Peptide-Capped Au NP Production. Standard peptide-capped NP synthesis protocols were used for the generation of all materials, regardless of the hybrid biomolecule employed.36 Briefly, 10 μL of 0.1 M HAuCl4 was diluted with 2.99 mL of water, followed by the addition of 2 mL of 0.25 mM MAM-containing peptide in water. This solution was mixed at room temperature for 15 min, after which 30 μL of cold 0.10 mM NaBH4 was slowly added. The mixture was swirled and then left to react on the benchtop for 1 h. Characterization. Once fabricated, the NPs were optically characterized using an Agilent 8453 UV−vis spectrophotometer with a 1 cm path length quartz cuvette. The size and shape of the Au NPs were characterized using a JEOL JEM-2010 TEM operating at a working voltage of 200 kV. Samples were prepared for imaging by drop-casting 5 to 15 μL of the NP dispersion onto a carbon-coated Cu TEM grid. Nanoparticle size distributions were constructed by measuring >100 individual nanoparticles from TEM images of each sample, using Nano Measurer 1.2 image analysis software. Within this software, the boundaries of each nanoparticle were located manually. Catalytic Reaction Analysis. Catalytic reduction of 4-nitrophenol to 4-aminophenol was carried out using previously described methods.2,34,36 In a glass vial, 1 mL of 0.2 mM peptide-capped Au NPs was mixed with 500 μL of 63.0 mM NaBH4 and 500 μL of water for 15 min. The mixture was then transferred to a 1 cm path length quartz cuvette, to which 2 mL of 900 μM 4-nitrophenol was added. The reaction was monitored using UV−vis spectroscopy, with a spectrum recorded every 15 s. The reaction was conducted separately using Au NPs with the azobenzene in the cis and trans form.

Figure 6. Recyclability and reversibility analysis. Parts (a) and (b) show the recyclability analysis for the AuBP1C−MAM-capped Au NPs in the trans and cis states, respectively, demonstrating no significant reactivity changes after three catalytic cycles. Part (c) presents the reversibility analysis for the same Au NPs. Finally, parts (d) and (e) present TEM images of the materials (d) before and (e) after the complete reversibility analysis of part (c).

analyzed for 4-nitrophenol reduction, again demonstrating diminished activity (k = (11.4 ± 0.3) × 10−3 s−1). When the materials were subsequently recycled through the surface switching/reaction for a third cycle, similar trends in reactivity were observed, suggesting that peptide switching at the Au NP surface has minimal effects on the catalytically active sites of the materials. Indeed, imaging of the Au NPs before and after the reversibility analysis (Figure 6d and e) demonstrated no changes in the particle size, indicating minimal effects of the switching/reaction on the NP surface structure/morphology. 9475

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(18) Hostetler, M. J.; Wingate, J. E.; Zhong, C.-J.; Harris, J. E.; Vachet, R. W.; Clark, M. R.; Londono, J. D.; Green, S. J.; Stokes, J. J.; Wignall, G. D.; Glish, G. L.; Porter, M. D.; Evans, N. D.; Murray, R. W. Alkanethiolate Gold Cluster Molecules with Core Diameters from 1.5 to 5.2 Nm: Core and Monolayer Properties as a Function of Core Size. Langmuir 1998, 14, 17−30. (19) Carducci, T. M.; Blackwell, R. E.; Murray, R. W. ChargeTransfer Effects in Ligand Exchange Reactions of Au25 MonolayerProtected Clusters. J. Phys. Chem. Lett. 2015, 6, 1299−1302. (20) Palafox-Hernandez, J. P.; Lim, C.-K.; Tang, Z.; Drew, K. L. M.; Hughes, Z. E.; Li, Y.; Swihart, M. T.; Prasad, P. N.; Knecht, M. R.; Walsh, T. R. Optical Actuation of Inorganic/Organic Interfaces: Comparing Peptide-Azobenzene Ligand Reconfiguration on Gold and Silver Nanoparticles. ACS Appl. Mater. Interfaces 2016, 8, 1050−1060. (21) Tang, Z.; Lim, C.-K.; Palafox-Hernandez, J. P.; Drew, K. L. M.; Li, Y.; Swihart, M. T.; Prasad, P. N.; Walsh, T. R.; Knecht, M. R. Triggering Nanoparticle Surface Ligand Rearrangement Via External Stimuli: Light-Based Actuation of Biointerfaces. Nanoscale 2015, 7, 13638−13645. (22) Dickerson, M. B.; Sandhage, K. H.; Naik, R. R. Protein- and Peptide-Directed Syntheses of Inorganic Materials. Chem. Rev. 2008, 108, 4935−4978. (23) Briggs, B. D.; Knecht, M. R. Nanotechnology Meets Biology: Peptide-Based Methods for the Fabrication of Functional Materials. J. Phys. Chem. Lett. 2012, 3, 405−418. (24) Tang, Z.; Palafox-Hernandez, J. P.; Law, W.-C.; Hughes, Z. E.; Swihart, M. T.; Prasad, P. N.; Knecht, M. R.; Walsh, T. R. Biomolecular Recognition Principles for Bionanocombinatorics: An Integrated Approach to Elucidate Enthalpic and Entropic Factors. ACS Nano 2013, 7, 9632−9646. (25) Palafox-Hernandez, J. P.; Tang, Z.; Hughes, Z. E.; Li, Y.; Swihart, M. T.; Prasad, P. N.; Walsh, T. R.; Knecht, M. R. Comparative Study of Materials-Binding Peptide Interactions with Gold and Silver Surfaces and Nanostructures: A Thermodynamic Basis for Biological Selectivity of Inorganic Materials. Chem. Mater. 2014, 26, 4960−4969. (26) Raimondo, C.; Kenens, B.; Reinders, F.; Mayor, M.; Uji-i, H.; Samori, P. Au Nanoparticle Scaffolds Modulating Intermolecular Interactions among the Conjugated Azobenzenes Chemisorbed on Curved Surfaces: Tuning the Kinetics of Cis-Trans Isomerisation. Nanoscale 2015, 7, 13836−13839. (27) Simoncelli, S.; Aramendia, P. F. Mechanistic Insight into the Z-E Isomerization Catalysis of Azobenzenes Mediated by Bare and CoreShell Gold Nanoparticles. Catal. Sci. Technol. 2015, 5, 2110−2116. (28) Ahonen, P.; Schiffrin, D. J.; Paprotny, J.; Kontturi, K. Optical Switching of Coupled Plasmons of Ag-Nanoparticles by Photoisomerisation of an Azobenzene Ligand. Phys. Chem. Chem. Phys. 2007, 9, 651−658. (29) Biswas, T. K.; Sarkar, S. M.; Yusoff, M. M.; Rahman, M. L. Synthesis and Characterization of Azobenzene-Based Gold Nanoparticles for Photo-Switching Properties. J. Mol. Liq. 2016, 214, 231− 237. (30) Titov, E.; Lysyakova, L.; Lomadze, N.; Kabashin, A. V.; Saalfrank, P.; Santer, S. Thermal Cis-to-Trans Isomerization of Azobenzene-Containing Molecules Enhanced by Gold Nanoparticles: An Experimental and Theoretical Study. J. Phys. Chem. C 2015, 119, 17369−17377. (31) Bandara, H. M. D.; Burdette, S. C. Photoisomerization in Different Classes of Azobenzene. Chem. Soc. Rev. 2012, 41, 1809− 1825. (32) Hnilova, M.; Oren, E. E.; Seker, U. O. S.; Wilson, B. R.; Collino, S.; Evans, J. S.; Tamerler, C.; Sarikaya, M. Effect of Molecular Conformations on the Adsorption Behavior of Gold-Binding Peptides. Langmuir 2008, 24, 12440−12445. (33) Bedford, N. M.; Hughes, Z. E.; Tang, Z.; Li, Y.; Briggs, B. D.; Ren, Y.; Swihart, M. T.; Petkov, V. G.; Naik, R. R.; Knecht, M. R.; Walsh, T. R. Sequence-Dependent Structure/Function Relationships of Catalytic Peptide-Enabled Gold Nanoparticles Generated under Ambient Synthetic Conditions. J. Am. Chem. Soc. 2016, 138, 540−548.

AUTHOR INFORMATION Corresponding Authors

*E-mail (P. N. Prasad): pnprasad@buffalo.edu. *E-mail (M. R. Knecht): [email protected]. Notes

The authors declare no competing financial interest.

ACKNOWLEDGMENTS This material is based upon work supported by the Air Office of Scientific Research, grant number FA9550-12-1-0226. We also thank the University of Miami for support. REFERENCES (1) Bhandari, R.; Coppage, R.; Knecht, M. R. Mimicking Nature’s Strategies for the Design of Nanocatalysts. Catal. Sci. Technol. 2012, 2, 256−266. (2) Bhandari, R.; Knecht, M. R. Effects of the Material Structure on the Catalytic Activity of Peptide-Templated Pd Nanomaterials. ACS Catal. 2011, 1, 89−98. (3) Briggs, B. D.; Li, Y.; Swihart, M. T.; Knecht, M. R. Reductant and Sequence Effects on the Morphology and Catalytic Activity of PeptideCapped Au Nanoparticles. ACS Appl. Mater. Interfaces 2015, 7, 8843− 8851. (4) Astruc, D. Palladium Nanoparticles as Efficient Green Homogeneous and Heterogeneous Carbon−Carbon Coupling Precatalysts: A Unifying View. Inorg. Chem. 2007, 46, 1884−1894. (5) Zhang, S.; Leem, G.; Srisombat, L.-o.; Lee, T. R. Rationally Designed Ligands That Inhibit the Aggregation of Large Gold Nanoparticles in Solution. J. Am. Chem. Soc. 2008, 130, 113−120. (6) Kah, J. C. Y.; Zubieta, A.; Saavedra, R. A.; Hamad-Schifferli, K. Stability of Gold Nanorods Passivated with Amphiphilic Ligands. Langmuir 2012, 28, 8834−8844. (7) Bhandari, R.; Knecht, M. R. Synthesis, Characterization, and Catalytic Application of Networked Au Nanostructures Fabricated Using Peptide Templates. Catal. Sci. Technol. 2012, 2, 1360−1366. (8) Wright, L. B.; Merrill, N. A.; Knecht, M. R.; Walsh, T. R. Structure of Arginine Overlayers at the Aqueous Gold Interface: Implications for Nanoparticle Assembly. ACS Appl. Mater. Interfaces 2014, 6, 10524−10533. (9) Bedford, N. M.; Ramezani-Dakhel, H.; Slocik, J. M.; Briggs, B. D.; Ren, Y.; Frenkel, A. I.; Petkov, V.; Heinz, H.; Naik, R. R.; Knecht, M. R. Elucidation of Peptide-Directed Palladium Surface Structure for Biologically Tunable Nanocatalysts. ACS Nano 2015, 9, 5082−5092. (10) Lévy, R. Peptide-Capped Gold Nanoparticles: Towards Artificial Proteins. ChemBioChem 2006, 7, 1141−1145. (11) Strimbu, L.; Liu, J.; Kaifer, A. E. Cyclodextrin-Capped Palladium Nanoparticles as Catalysts for the Suzuki Reaction. Langmuir 2003, 19, 483−485. (12) Park, J. Y.; Aliaga, C.; Renzas, J. R.; Lee, H.; Somorjai, G. A. The Role of Organic Capping Layers of Platinum Nanoparticles in Catalytic Activity of Co Oxidation. Catal. Lett. 2009, 129, 1−6. (13) Coppage, R.; Slocik, J. M.; Ramezani-Dakhel, H.; Bedford, N. M.; Heinz, H.; Naik, R. R.; Knecht, M. R. Exploiting Localized Surface Binding Effects to Enhance the Catalytic Reactivity of Peptide-Capped Nanoparticles. J. Am. Chem. Soc. 2013, 135, 11048−11054. (14) Wu, B.; Huang, H.; Yang, J.; Zheng, N.; Fu, G. Selective Hydrogenation of A,B-Unsaturated Aldehydes Catalyzed by AmineCapped Platinum-Cobalt Nanocrystals. Angew. Chem., Int. Ed. 2012, 51, 3440−3443. (15) Bastús, N. G.; Merkoçi, F.; Piella, J.; Puntes, V. Synthesis of Highly Monodisperse Citrate-Stabilized Silver Nanoparticles of up to 200 Nm: Kinetic Control and Catalytic Properties. Chem. Mater. 2014, 26, 2836−2846. (16) Poirier, G. E.; Pylant, E. D. The Self-Assembly Mechanism of Alkanethiols on Au(111). Science 1996, 272, 1145−1148. (17) Templeton, A. C.; Wuelfing, W. P.; Murray, R. W. MonolayerProtected Cluster Molecules. Acc. Chem. Res. 2000, 33, 27−36. 9476

DOI: 10.1021/acsnano.6b04555 ACS Nano 2016, 10, 9470−9477

Article

ACS Nano (34) Wunder, S.; Polzer, F.; Lu, Y.; Mei, Y.; Ballauff, M. Kinetic Analysis of Catalytic Reduction of 4-Nitrophenol by Metallic Nanoparticles Immobilized in Spherical Polyelectrolyte Brushes. J. Phys. Chem. C 2010, 114, 8814−8820. (35) Dong, M.; Babalhavaeji, A.; Samanta, S.; Beharry, A. A.; Woolley, G. A. Red-Shifting Azobenzene Photoswitches for in Vivo Use. Acc. Chem. Res. 2015, 48, 2662−2670. (36) Li, Y.; Tang, Z.; Prasad, P. N.; Knecht, M. R.; Swihart, M. T. Peptide-Mediated Synthesis of Gold Nanoparticles: Effects of Peptide Sequence and Nature of Binding on Physicochemical Properties. Nanoscale 2014, 6, 3165−3172. (37) Chan, W. C.; White, P. D. Fmoc Solid Phase Peptide Synthesis: A Practical Approach; Oxford University Press: New York, NY, 2000.

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DOI: 10.1021/acsnano.6b04555 ACS Nano 2016, 10, 9470−9477