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C: Surfaces, Interfaces, Porous Materials, and Catalysis

Optical Control of Biomimetic Nanoparticle Catalysts Based Upon the Metal Component Randy L. Lawrence, Vincent J. Cendan, Billy Scola, Yang Liu, ChangKeun Lim, Paras N. Prasad, Mark T. Swihart, and Marc R. Knecht J. Phys. Chem. C, Just Accepted Manuscript • DOI: 10.1021/acs.jpcc.8b07676 • Publication Date (Web): 07 Nov 2018 Downloaded from http://pubs.acs.org on November 8, 2018

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The Journal of Physical Chemistry

Optical Control of Biomimetic Nanoparticle Catalysts Based Upon the Metal Component Randy L. Lawrence,1 Vincent J. Cendan,1 Billy Scola,1 Yang Liu,3 Chang-Keun Lim,3 Paras N. Prasad,3 Mark T. Swihart,2 Marc R. Knecht1,* 1. Department of Chemistry, University of Miami, 1301 Memorial Drive, Coral Gables, Florida 33146, United States 2. Department of Chemical and Biological Engineering and 3. 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: Nanoparticle catalysts provide an intriguing route to achieving sustainable reactivity. Recent evidence has suggested that both the underlying metallic core and the passivating ligand layer can be exploited to control reactivity. The intimate interactions between the core metal and structure of the ligand layer can change based upon the metal used to generate the catalytic particle. Through judicious selection of both components, nanoparticle catalytic systems can be designed to be stimuli responsive for controlled reactivity. Herein we demonstrate the effects of the underlying metal on the optically modulated catalytic activity of peptide-capped noble metal nanoparticles. For this, a photoswitch was incorporated into the peptide that enables reversible reconfiguration of the bioligand overlayer structure between two conformations based upon the isomerization state of the photoswitch. These changes in activity are dependent upon the inorganic metal of the particle core, and we exploit this dependence to demonstrate changes in the activity. The materials were fully characterized via spectroscopic methods and microscopy to correlate the observed reactivity to the material composition. The results provide new pathways to achieve remotely responsive catalysts that could be important for controlled multistep reactions or be exploited for other applications including biosensing and plasmonic devices.

Introduction Catalytic applications of colloidal nanoparticles (NPs) have advanced rapidly in recent years, and major research efforts remain devoted to understanding how the metal/ligand interface affects the overall reactivity in these systems.1-9 This interfacial structure is directly related to the underlying metallic composition of the particle, where changes in the metal identity can alter the ligand overlayer morphology.10-12 In most cases, the ligands are statically bound through a rigid covalent interaction, locking them into a single conformation.13 The ability to change this conformation on demand could prove to be critically important for catalysis, allowing one to remotely initiate or selectively alter the reactivity of the material.5, 10, 1417 To access such capabilities, molecules that bind to the particle surface with sufficient strength to stabilize the materials are required; however, these interactions must also be weak enough to allow for dynamic reconfiguration of the ligands.5 As an alternative to conventional ligands, one can employ materials directing peptides that recognize, bind, and stabilize colloidal dispersions of NPs.11-12, 18 These peptides have a strong affinity for inorganic surfaces through the multiple, weak noncovalent interactions of the individual residues, which can be manipulated to change the peptide surface conformation.12, 18 One approach to triggering peptide conformational changes is via optical stimulation.5, 19-22 Through conju-

gation of a non-natural azobenzene photoswitch into the peptides,23 reversible changes in the biomolecular overlayer structure on a NP surface can be accessed via azobenzene photoisomerization (e.g. cis vs. trans). These changes in the isomerization state alter the affinity of the biomolecule for the metallic surface and can be used to optically tune the final size of the nanoparticle.21-22 Photoisomerization can also be accomplished using non-linear optical (NLO) approaches under specific conditions.21 The catalytic properties of NPs capped with photoswitchable peptides are sensitive to isomerization-based structural changes and can be varied between two different reaction regimes based upon the reversible peptide conformation.5, 10 Further studies have demonstrated that additional factors such as the peptide sequence and photoswitch position are critical in determining catalytic activity changes as a function of the peptide overlayer morphology for Au NPs.24 While the inorganic NP composition clearly affects the catalytic activity, it is also known to have dramatic implications on photoswitchable peptide reconfiguration.12, 25-26 Here we study the behavior of these optically triggered peptides across different metallic interfaces. Photoswitchable peptides incorporating the azobenzene group at different locations were used to synthesize Ag and Pd NPs, and the effects of changing the metal/peptide interface on the catalytic activity was examined. The NPs were synthesized under identical conditions, and fully characterized by optical and electron microscopy

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methods to monitor changes in the peptide conformation as a function of photoswitch state. The catalytic capabilities of the materials were measured by monitoring the reduction of 4-nitrophenol to 4-aminophenol with the bound peptides in both the cis and trans configurations. The results demonstrated a level of catalytic sensitivity to changes in the biomolecular ligand overlayer structure, in connection with differences in metal composition. Such results provide a pathway to understanding how reconfigurable interfaces can be manipulated by NP properties. This capability could be beneficial in obtaining fine synthetic control over inorganic nanomaterials for use in multistep reaction pathways. Materials and Methods Materials. AgNO 3 , K 2 PdCl 4 , NaBH 4 , 1,2-ethanedithiol, thioanisole, and anisole were purchased 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) was purchased from BDH chemicals. Lastly, FMOC-protected amino acids, Wang resins, and coupling reagents were obtained from Advanced Chemtech. All reagents were used without further purification, and ultrapure water (18.2 MΩ•cm) was used for all aqueous experiments. Peptide Synthesis and Azobenzene Coupling. Standard solidphase FMOC peptide synthesis protocols were employed using a TETRAS peptide synthesizer (CreoSalus).34 Cleavage of the peptide from the resin occurred over 4 h in a TFA/EDT/thioanisole/anisole cocktail (90:3:5:2). The resulting mixture was purified via reverse phase HPLC (Waters Co. Delta 600 with 2498 UV-vis detector). All peptides were confirmed with ESI mass spectrometry. Once purified, the biomolecules were lyophilized and stored at -80 °C. Coupling of the photoswitch. Coupling of the MAM to the peptide was carried out through standard thiol-maleimide coupling protocols.19 To discourage double coupling of the MAM and peptide, the reactions were conducted under a slight excess of the photoswitch. Once the coupling was complete, the reaction was purified using centrifuge filtration (Amicon Ultra-0.5 Centrifugal Filter Devices 3000 NMWL - Millipore). The retentate was diluted with ~2 mL of water before the sample was lyophilized. Peptide-capped NP Synthesis. Fabrication of peptide-capped Ag NPs was achieved through standard approaches.35 In a glass vial, 2.96 mL of water was mixed with 10 μL of AgNO 3 (0.1 M) and 2.00 mL of the peptide-MAM conjugate dissolved in water (0.25 mM). The mixture was left to slowly stir at room temperature for 15 min, allowing for the metal ions to complex with the peptide. Afterwards, 30 μL of freshly prepared NaBH 4 (0.1 mM) was added dropwise to the mixture and swirled by hand three times, resulting in a color change from pale yellow to bright orange. The mixture was left on the benchtop for 1 h undisturbed, allowing for metal ion reduction and NP formation to occur. Identical protocols were employed for the production of peptide-capped Pd NPs; however, the resulting material suspension produced a pale brown color. Characterization. Once the particles were prepared, they were fully characterized. UV-vis analysis of the materials was conducted using an Agilent 8453 UV-vis spectrophotometer with 1 cm quartz cuvettes. TEM images of the peptide-capped materials were obtained using a JEOL JEM-2010 TEM operating at a 200-kV working voltage. Samples were prepared by drop-casting 10 μL of the particle dispersion onto a carbon coated TEM grid. Each NP was sized using ImageJ, with at least 100 particles sized over various different regions on the grid. Catalytic Analysis. To test the catalytic properties of the particles, the model reduction of 4-nitrophenol was employed using previously published methods.5, 35-36 Briefly, all reactions were carried out in 1 cm path length quartz cuvettes, where 975 μL of water was mixed with 450 μL of the nanoparticle solution. This sample was allowed to equilibrate to the selected reaction temperature for 15 min prior to starting the analysis. Next, 25 μL of freshly prepared NaBH 4 was added, and the solution was left to incubate for 10 min. After this

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time, 50 μL of 4-nitrophenol was added into the reaction mixture and monitoring of the absorbance at 400 nm was conducted. Note, the NaBH 4 was added in excess to ensure that the reaction was pseudofirst order with respect to the substrate. After all reagents were added, the final working volume was 1.5 mL. The reactivity was measured for all prepared materials at temperatures between 10 and 40 °C with the peptides on the NP surface in both the trans and cis conformations.

Results and Discussion Photoswitchable peptides were generated, as shown previously, with an azobenzene incorporated at either the N- or Cterminal domain of the Au-binding AuBP1 peptide (WAGAKRLVLRRE - Scheme 1).19 The photoswitch structure is comprised of an azobenzene flanked by maleimides (termed MAM – Scheme 1a), which allows facile coupling at cysteine residues incorporated into the peptide sequence. The peptide/photoswitch hybrid products are denoted as MAMCAuBP1 and AuBP1C-MAM, corresponding to the N- and Cterminal attachments, respectively (Scheme 1b). Scheme 1: Structures of (a) the MAM photoswitch in trans (tMAM) and cis (cMAM) conformations and (b) the peptidephotoswitch hybrids MAM-CAuBP1 (top) and AuBP1CMAM (bottom)

Ag Nanoparticle Synthesis, Characterization, and Biointerface Reconfiguration via Photoswitching. Previous studies19-20 using Quartz Crystal Microbalance (QCM) analysis quantified the affinity of the two peptides for the Ag surface in the trans and cis states, yielding ∆G values of -35.8 ± 0.7 and -35.7 ± 1.0 kJ/mol for the MAM-CAuBP1 peptide in the trans and cis conformations, respectively. For the AuBP1C-MAM, ∆G values of -35.6 ± 0.6 kJ/mol for the trans conformation and -34.6 ± 0.6 kJ/mol for the cis conformation were extracted from the time-dependent QCM measurements. Characterization of the peptide-capped Ag NPs began with UV-vis spectroscopy (Figure 1). Figure 1a specifically presents the spectra of the Ag NPs prepared with the AuBP1CMAM. The red spectrum corresponds to the peptide alone in solution at the reaction concentrations, which demonstrated a strong absorbance at 320 nm and a weaker absorbance centered around 450 nm. These two peaks are consistent with the


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π-π* and n-π* absorbance from the azobenzene photoswitch, respectively.27-28 When Ag+ was allowed to complex with the peptide, as shown in the blue spectrum, no significant changes from the metal free system were observed. After reduction (green spectrum), the materials presented two notable absorbance peaks at 320 and 450 nm. The first peak at 320 nm corresponds to the azobenzene moiety in the peptide, while the absorbance centered around 450 nm is consistent with the plasmon band typically observed with Ag NPs. The sharper plasmon band at 450 nm is quite strong and masks the substantially weaker n-π* absorbance of the azobenzene at the same wavelength. For the Ag NPs capped with MAMCAuBP1, nearly identical spectra were collected (Figure 1b) as compared to the materials prepared using the AuBP1CMAM. Such results are consistent with previous studies and suggest that similar structures of the inorganic materials were prepared, regardless of the position of the MAM unit within the peptide.20

compared to the AuBP1C-MAM-stabilized materials; however, this difference was relatively minor, considering the small size of the materials. The optical switching capabilities of the photoswitchable peptides bound to the NP surface were next probed using UVvis spectroscopy (Figure 3). Initially, the Ag NPs were capped with the peptides in the trans configuration, which was photoisomerized to the cis conformation via UV irradiation. Figure 3a presents the spectra collected for Ag NPs capped with AuBP1C-MAM to examine the photoisomerization process.

Figure 2: TEM images and histograms for the Ag NPs capped with (a and c) AuBP1C-MAM and (b, and d) MAM-CAuBP1.

Figure 1: UV-vis characterization of the Ag NPs capped with the (a) AuBP1C-MAM and (b) MAM-CAuBP1 peptides.

Upon confirmation of the absorbance properties of the Ag NPs, TEM imaging of both samples was employed to characterize the particle size and morphology. Both the Ag NPs capped with AuBP1C-MAM (Figure 2a) and MAM-CAuBP1 (Figure 2b) were imaged with the photoswitch in the trans conformation. For both samples, quasispherical materials were observed with average particle diameters of 3.9 ± 0.8 (Figure 2c) and 4.7 ± 1.6 nm (Figure 2d) for Ag NPs capped with AuBP1C-MAM and MAM-CAuBP1, respectively. For each sample, sizing of at least 100 NPs over multiple TEM images was employed. In general, the MAM-CAuBP1capped NPs displayed a somewhat broader size distribution as

In this analysis, the red spectrum presents the absorbance of the NPs prior to UV irradiation in the trans configuration, with the π-π* transition at 320 nm. The sample was then irradiated under UV light for 30 min at room temperature to drive the photoswitch from the trans conformation to the less energetically stable cis.27 As seen in the blue spectrum, a diminished 320 nm peak was noted, consistent with trans to cis switching. The particles were then illuminated for 30 min under visible light to switch the cis configuration of the azobenzene back to the trans. This was consistent with an increase in absorption at 320 nm observed in the green spectrum. Similar spectra were collected from Ag NPs capped with MAMCAuBP1, as outlined in Figure 3b. Prior studies employing Circular Dichroism (CD) spectroscopy have confirmed that isomerization of the photoswitch in these biomolecules on Ag NP surfaces does result in a measurable change in peptide conformation.20 Such results are in line with previous results demonstrating that the MAM remains functional even when bound to a NP surface.20 While optical irradiation is typically employed to drive photoswitch isomerization, thermal-based switching from cis-totrans can also occur due to the greater thermodynamic stability of the trans conformation.28 By monitoring the increase in the 320 nm absorbance over time without optical irradiation, the half-life of the cis conformation can be determined (Supporting Information, Figure S1). To examine this effect, the peptide-capped Ag NPs were irradiated under 365 nm light for at least 30 min to ensure that the photoswitch was in the cis photostationary state. In the dark, the samples were moni-



tored at 25 °C overnight to determine the half-life. The materials demonstrated half-lives of 94.9 ± 7.0 and 132.4 ± 9.9 h when capped with the AuBP1C-MAM and MAM-CAuBP1 peptides, respectively. These values are substantially longer than for the free peptides in solution: 3.4 ± 1.5 h for AuBP1CMAM and 2.9 ± 0.1 h for MAM-CAuBP1.5 Such results demonstrate that thermally-driven switching from cis-to-trans is an exceedingly slow process. The basis for these long halflives and changes between the free and nanoparticle-bound peptides likely arises from steric effects of the azobenzene molecule in direct contact with the NP metallic surface.19-20 We note, however, that the difference between the two halflives is significant, thus the position of the photoswitch in the peptide sequence appears to affect the isomerization rate. This suggests that the chemical environment at the molecular level surrounding the photoswitch bound to the NP surface is indeed different; however, these differences do not substantially inhibit the photo-driven switching process.

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min and reduced with NaBH 4 . The resulting mixture yielded a light brown solution after 1 h of reduction on the bench top. The Pd NPs remained dispersed for over a week with no visible precipitate. The Pd NPs were fully characterized using UV-vis spectroscopy and TEM. Using the AuBP1C-MAM in the trans conformation, each step of Pd NP synthesis was examined, as shown in Figure 4a. As expected, there was a strong absorbance at 320 nm and a less pronounced band at ~450 nm for the free peptide, arising from the azobenzene moiety (red spectrum). When the peptide was complexed with Pd2+, the resulting spectrum (in blue) showed no major changes from the peptide only system. After reduction and NP formation, the absorbance (shown in green) at 320 nm remained; however, a broad increasing absorbance between 400 and 500 nm was observed. This absorbance arises from the Pd NPs, consistent with previous studies.29 Under identical conditions, Pd NPs capped with MAM-CAuBP1 were analyzed, where the results are presented in Figure 4b. The spectra were similar to those of AuBP1C-MAM-capped Pd NPs. To confirm Pd NP formation, TEM analysis was performed on the peptide-capped materials. The system was imaged with the photoswitch in the trans conformation. For the materials capped with AuBP1C-MAM (Figure 5a) or MAM-CAuBP1

Figure 3: Photoswitching analysis of the MAM unit in the (a) AuBP1C-MAM- and (b) MAM-CAuBP1-capped Ag NPs.

Pd Nanoparticle Synthesis, Characterization, and Biointerface Reconfiguration via Photoswitching. Initial analysis of peptide binding to Pd was undertaken using QCM. However, release of metal ions from the sensor surface was observed upon exposure to the peptides, preventing extraction of binding affinities on Pd by QCM analysis. While ∆G values could not be determined, release of Pd in the presence of the peptide suggests a strong affinity of the biomolecules to the metallic surface. Pd NPs were then prepared using the peptide/photoswitch hybrids in the same manner as the Ag NPs discussed above. Briefly, the Pd NPs were produced by mixing Pd2+ with either AuBP1C-MAM or MAM-CAuBP1 for 15

Figure 4: UV-vis characterization of the Pd NPs capped with the (a) AuBP1C-MAM and (b) MAM-CAuBP1 peptides.


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Figure 5: TEM images and histograms for the Pd NPs capped with (a and c) AuBP1C-MAM and (b, and d) MAM-CAuBP1.

(Figure 5b), quasispherical Pd NPs were generated with average diameters of 2.5 ± 0.4 and 3.4 ± 0.9 nm, respectively. Interestingly, as with the Ag NPs, the MAM-CAuBP1-capped Pd NPs were slightly larger than those capped with AuBP1CMAM species. This suggests that the position of the MAM group may affect NP size; however, based upon the standard deviations in the measurements, such a conclusion is somewhat speculative. With the identification of the Pd NP morphology, the photoswitching capability of the azobenzene moiety was examined. Optical irradiation of the sample with UV and visible light was again exploited to monitor peptide conformational changes. Focusing on the Pd NPs capped with AuBP1CMAM (Figure 6a), the anticipated degrees of biomolecule switching were observed. In this regard, when the original trans-based materials (red spectrum) were irradiated with UV light, a diminished absorbance at 320 nm was observed (blue spectrum), confirming trans to cis switching.28 When this same sample was then irradiated with visible light (green spectrum), the absorbance at 320 nm increased, restoring the original intensity. CD analysis of this system demonstrated changes in the peptide ellipticity in response to the isomerization state of the biomolecule on the NP surface (Supporting Information, Figure S2). This data provides evidence that the photoswitch is capable of changing conformation while on the Pd surface. Under the same conditions, MAM-CAuBP1capped Pd NPs were examined, with the results presented in Figure 6b. These data are directly comparable to the Pd NPs capped with the AuBP1C-MAM peptide, with no remarkable differences. This suggests that the hybrid peptide photoswitch can be exploited on different metallic NP surfaces without an observable loss in functionality. It is interesting to note that for both the Pd and Ag NPs, not all of the MAM molecules in the peptide ligands undergo trans-to-cis switching under UV light. This likely arises from the more stable trans conformation on the metal surface preventing complete photoswitching. For the catalytic properties of the NPs to change, however, only a fraction of the ligands must change their conformation.

Figure 6: Photoswitching analysis of the MAM unit in the (a) AuBP1C-MAM- and (b) MAM-CAuBP1-capped Pd NPs.

To monitor the half-life of the photoswitchable peptides on the Pd surface, thermal-based switching of the biomolecules was again conducted in the dark (Supporting Information, Figure S1). From this analysis, the Pd NPs prepared with AuBP1C-MAM presented a half-life of 67.4 ± 8.0 h; however, the MAM-CAuBP1-capped particles produced a significantly shorter half-life of 14.5 ± 2.4 h. While the MAM-CAuBP1 system demonstrated the shortest half-life of all of the materials studied, it is still substantially longer than the actual catalytic reaction, demonstrating that thermally-driven switching is unlikely to interfere with the reactivity. We also note the difference in the half-life values between the two peptide-photoswitch hybrids on the selected inorganic NPs. The half-lives are substantially longer on Ag compared to Pd. These differences are related to how the biomolecules interact with the metallic surface, which are known to alter photoswitch isomerization processes.20 Nanoparticle Catalytic Activity as a Function of Biointerfacial Conformation. With confirmation of NP formation and adsorbed peptide photoswitching, the Ag and Pd NPs were examined for their relative catalytic activity as a function of peptide surface structure. Changes in the photoswitch isomerization state, and thus peptide overlayer structure, are known to directly influence reaction rates.5, 24 This has been largely attributed to substrate accessibility to reaction sites along the metallic NP surface. Because the metal of the particle plays a direct role in controlling peptide conformation when bound, changes in the reactivity based upon the NP



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metal through its effect on the ligand conformation are possible, along with effects of the catalytic metal.12, 20 To probe such effects, we studied the reduction of 4-nitrophenol to 4aminophenol (Scheme 2). This model reaction follows a Langmuir-Hinshelwood mechanism, in which the substrate is reduced directly at the particle metallic surface.30-31 Scheme 2: Reduction of 4-nitrophenol to 4-aminophenol

Each of the four NP systems with different metals and peptide surface conformations was tested for its catalytic activity in triplicate (Supporting Information, Figure S3 and Table S1). Figure 7 specifically details the reaction analysis for the Ag NPs capped with AuBP1C-MAM in the trans conformation at 25 °C. For this reaction, the NPs were mixed with an excess of NaBH 4 in water, which allows the metal surface to become saturated with hydrogen. After a 10 min incubation period, the 4-nitrophenol substrate was added to the reaction, resulting in rapid product (4-aminophenol) formation. A decrease in the absorbance at 400 nm is observed during the reaction (Figure 7a). Plotting this absorbance as a function of time (Figure 7b) showed that the reaction reached completion at ~300 s. Using this analysis, the pseudo-first-order rate constant (k obs ) can be calculated from a plot of ln(A t /A o ) vs time, where A 0 corresponds to the initial absorbance and A t is the absorbance at time t (Figure 7c). The k obs value can be obtained from slope of this plot.5, 31 Using this analysis for the Ag NPs capped with AuBP1C-MAM in the trans configuration gave a rate constant of (24.2 ± 3.0) × 10-3 s-1 at 25 °C. The NP-driven reduction reaction was conducted at five different temperatures ranging from 10 to 40 °C, so that an activation energy (E a ) could be determined (Figure 7d). In a plot of ln(k obs ) vs 1/T, the slope of the best fit line corresponds to –E a /R. For the AuBP1C-MAM-capped Ag NPs with the peptide in the trans structure, the k obs values ranged from (4.6 ± 0.2) × 10-3 to (49.6 ± 3.3 s-1) × 10-3 s-1, increasing over the reaction temperature range (Figure 8a) with an activation energy of 59.4 ± 1.2 kJ/mol. For Ag NPs with the peptide in the cis conformation, the apparent rate constant increased from (3.3 ± 0.1) × 10-3 s-1 at 10 °C to (20.2 ± 1.2) × 10-3 s-1 at 40 °C, corresponding to an activation energy of 44.7 ± 1.9 kJ/mol. Directly comparing the rate constants and activation energies for the Ag NPs with the biomolecular ligands in the trans and cis states reveals clear differences in activity that we attribute to a structural change in the NP interface upon photoswitching. We also note that the absolute values of k obs were higher for the configuration with the higher activation energy, which suggests that other factors such as total accessible metal surface area are important, in addition to the energetic barrier to reaction. Similar results were observed when the Ag NPs capped with MAM-CAuBP1 were employed to drive the catalytic reaction. Using the NPs with the peptide in the trans state, the k obs values increased with temperature from (5.5 ± 0.2) × 10-3 to (34.6 ± 1.5) × 10-3 s-1 (Figure 8b), from which an activation

Figure 7: Reaction analysis for the reduction of 4-nitrophenol on Ag NPs capped with AuBP1C-MAM in the trans state. Panel (a) presents the absorbance spectra of the reaction mixture over time, while panel (b) displays the decrease in absorbance at 400 nm as the substrate is consumed. Panel (c) provides a plot of ln(A t /A 0 ) vs time from which the k obs value can be determined. Finally, panel (d) presents an Arrhenius plot for the reduction reaction.

energy of 44.2 ± 1.4 kJ/mol was determined. When the peptide was switched to the cis conformation, diminished rate constants were observed in general, especially at the higher temperatures. For example, at a temperature of 10 °C, a k obs value of (5.8 ± 1.0) × 10-3 s-1 was calculated. As the temperature increased, the rate constants also increased, reaching a maximum of (18.5 ± 1.2) × 10-3 s-1 at 40 °C. By fitting the Arrhenius plot using these data, an activation energy of 27.8 ± 2.1 kJ/mol was determined for the MAM-CAuBP1-capped Ag NPs. As noted for the Ag NPs capped with the AuBP1CMAM peptides that positioned the photoswitch at the opposite terminus, clear reactivity differences were observed for the materials based upon the azobenzene isomerization state, and larger k obs values were again noted for the reaction with the higher E a value. Similar catalytic studies were also conducted using the Pd NPs capped with two peptide/photoswitch hybrids. With the photoswitch in the trans state, the AuBP1C-MAM-capped particles produced a series of increasing k obs values that ranged from (3.7 ± 0.7) × 10-3 s-1 at 10 °C to (13.0 ± 0.6) × 103 -1 s at the highest temperature studied (40 °C – Figure 8c). The data, which increased linearly as a function of reaction temperature, were analyzed to calculate an E a of 30.9 ± 5.1 kJ/mol. When the same Pd NPs were employed with the peptide photoswitch in the cis conformation, a similar increase in k obs values with temperature was observed. For this system, the rate constants were greater in magnitude as compared to the trans NPs, ranging from (10.5 ± 1.5) × 10-3 to (20.8 ± 0.3) × 10-3 s-1 over the selected temperature range. From these rate constants, an activation energy of 16.6 ± 2.9 kJ/mol was determined. The Pd NPs capped with the MAM-CAuBP1 biomolecules were finally studied for their catalytic reactivity as a function of the biointerface configuration. For the particles with the peptides in the trans state, a k obs value of (4.8 ± 0.6) × 10-3 s-1 was observed at 10 °C, increasing to (18.9 ± 1.9) × 10-3 s-1 at 40 ºC. From this data, an E a value of 35.0 ± 1.3 kJ/mol was


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Figure 8: Comparison of rate constants (k obs ) for 4-nitrophenol reduction reactions catalyzed by Ag NPs capped with (a) AuBP1C-MAM and (b) MAM-CAuBP1, and Pd NPs capped with (c) AuBP1C-MAM and (d) MAM-CAuBP1.

calculated. Very similar data were obtained when the photoswitch was isomerized to the cis conformation on the Pd NP surface. For these materials, the k obs values increased linearly from (5.7 ± 0.1) × 10-3 to (20.8 ± 0.5) × 10-3 s-1. This resulted in an activation energy of 32.5 ± 1.9 kJ/mol for this system from the Arrhenius plot. While clear reactivity differences are observed between the cis and trans states of the biomolecules for both Ag and Pd, the half-lives of the peptides on the metal NP surface can change as a function of temperature. These changes could affect the observed reactivity, thus the half-lives of the peptides on the NPs were measured at the highest reaction temperature, 40 °C. As shown in Table S2 of the Supporting Information, these values ranged from the 2.2 ± 0.15 to 11.2 ± 0.6 h for the AuBP1C-MAM and MAM-CAuBP1 peptides bound to the Pd NP surface. Because the reaction is completed on the metal particles in < 3 min, thermally driven biomolecule switching is not anticipated to substantially affect the observed k values. Taking into account the reactivity trends for the two different inorganic materials (Ag and Pd) passivated with two different peptides (AuBP1C-MAM and MAM-CAuBP1) in two different conformations (cis vs. trans), interesting trends in the NP reactivity can be observed that give rise to substantial property differences. First, when considering the two Ag NP systems, we observe that the trans state of the biomolecule generally resulted in higher k obs values when compared to the same particles with the photoswitch in the cis state. This is especially evident at the higher temperatures, such as at 40 °C where the Ag NPs capped with the AuBP1C-MAM species in the trans configuration demonstrated a rate constant that was 2.5 times greater than for the NPs with the peptide in the cis conformation. Remarkably, however, for both Ag NP systems, the materials with the peptide in the cis arrangement demonstrated notably lower activation energy values as compared to the particles with the biomolecules in the trans conformation. Such effects were quite surprising that lower reaction rate constants would be observed for systems with lower E a values, suggesting that another factor is likely responsible for the reactivity differences.

Additional information concerning the reactivity trends can be extracted from the Arrhenius plot, including the frequency factor value (A). A represents the frequency of collisions between the substrate and the catalyst per unit of time, where higher A values could lead to increased reactivity, especially at higher temperatures.32-33 When considering the data for the AuBP1C-MAM-capped Ag NPs in the trans and cis states, A values of 5.0 × 108 and 6.4 × 105 s-1, respectively, were determined (Supplemental information, Table S1). This represents a three order of magnitude difference between the two isomeric systems, which is reflective of the higher k obs values noted for the materials in the trans state over the cis, regardless of the effects of activation energy. As such, the reaction for this system appears to be more dependent on the A value over the E a , suggesting that structural differences between the two materials lead to the variations in reactivity. In this regard, to generate the higher k obs values, the interfaces for the transbased materials must be structured to optimize the interactions between substrate and catalytic surface, as compared to the same NPs with the peptides in the cis conformation. Similar results were also observed for the Ag NPs capped with the MAM-CAuBP1 peptides with A values of 1.9 × 106 s-1 for the trans conformation and 9.3 × 102 s-1 for the cis conformation. This system also demonstrates a strong dependence on the frequency factor over the activation energy, indicating that significant structural differences are giving rise to the observed changes in reactivity. Note that a larger A value, in general, reflects higher entropy in the transition state for the reaction (smaller decrease in entropy relative to the separated reactants). While this analysis should be applied with caution to complex reactions at an interface in solution, a larger A value implies a larger number of pathways or transition state conformations that can lead to reaction. In contrast, a relatively small A value implies relatively fewer pathways leading to reaction, or a relatively small number of conformations through which the reaction can occur. These observations thus suggest not only differences in the number of accessible surface sites for the different peptide configurations, but differences in the flexibility of the biomolecular ligand layer to allow reactants to approach the surface by many paths and in many different orientations. When using the exact same biomolecules, but changing the metal to Pd, notably different trends were observed in the catalytic reactivity. Considering the Pd NPs capped with AuBP1C-MAM, higher k obs values were noted for the materials with the peptides in the cis structure over the trans, especially at lower reaction temperatures. In this regard, at 10 °C, the trans AuBP1C-MAM-capped Pd NPs demonstrated a k obs value that was 2.8 times lower than the same materials with the peptides in the cis conformation. Interestingly, the activation energies for this system fell directly in line with the observed rate constants where a lower E a value was observed for the cis AuBP1C-MAM-capped Pd materials that demonstrated greater k obs values as compared to the same NPs with the biomolecular overlayer in the trans conformation. Frequency factors of 2.2 × 103 and 1.3× 101 s-1 were calculated for the AuBP1C-MAM-passivated structures in the trans and cis conformation, respectively. While a greater A value was noted for the trans system as compared to the cis, the reaction rates were notably higher for the cis system, due to the E a value differences. This suggests that while structural differences are likely present, the effect of the ligand conformation on the activation energies plays a bigger role in determining



reactivity differences. This would also explain why greater reactivity differences were observed at lower temperatures, as the system is dominated by energetics and not by the frequency of interactions between the substrate and catalyst surface. In the final system, the Pd NPs capped with the MAMCAuBP1 peptides, no substantial differences in reactivity were noted in the rate constants, activation energies, or frequency factors (1.5 × 104 s-1 for trans and 9.1 × 103 s-1 for cis). While structural changes are anticipated for this system based upon the switching of the azobenzene moiety, these effects do not appear to play a notable role in the reactivity. This could arise from at least two scenarios. One possibility is that only minor structural changes could be occurring during the peptide photoswitching process that do not notably alter the exposure of the catalyst materials; however, in the second situation, substantial biomolecular overlayer structural changes could be occurring, but the degree of Pd surface accessibility could be similar between the two conformations. In either case, similar degrees of reactivity would be anticipated. Overall, the underlying metallic interface of the NP directly influences both the catalytic process itself and the ability to change catalytic activity through ligand reconfiguration. Comparing these results for Ag and Pd NPs to previously published work with Au NPs prepared with the same peptide/photoswitch hybrids showed comparable results.5 In general, the k obs values for the present system were quite similar to those obtained for the Au NPs;5 however, the Au peptide-capped materials were controlled by activation energies and not the A values. Overall, we find the behavior of these photoswitchable nanoparticle catalysts is highly dependent upon the underlying inorganic material, and we can envision multiple pathways to exploit this sensitivity to design new photoswitchable peptide-capped NPs with enhanced catalytic control via optical stimulation. Conclusions In conclusion, the results presented here demonstrate that the nature of the underlying inorganic NP plays a critical role in optical manipulation of catalytic properties of NPs capped with photoswitchable peptides. The catalytic reactivity of the NPs was sensitive to structural changes in the photoswitchable peptide ligand layer. Differences in catalytic activity between states were dominated by the either activation energy (Pd NPs capped with AuBP1C-MAM) or the frequency factors (Ag NPs). These differences can potentially be exploited to enhance reactivity in multistep reactions. To this end, the ability to turn catalytic reactivity on and off remotely could be accessed with further refinement of this approach, thus allowing for reactions to be turned on at specific time points. It would also allow for a catalyst to be fully deactivated to prevent byproduct formation without the need for separation from the reaction, thus enhancing the overall reaction efficiency. While such on/off reactivity was not achieved herein, pathways towards realizing such capabilities were demonstrated.

ASSOCIATED CONTENT Supporting Information. Half-life and additional catalytlic reactivity analysis.

AUTHOR INFORMATION

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Corresponding Author MRK – [email protected]

Author Contributions The manuscript was written through contributions of all authors. All authors have given approval to the final version of the manuscript.

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