Diiron Dithiolate Complex Induced Helical Structure of Histone and

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Cite This: ACS Appl. Mater. Interfaces XXXX, XXX, XXX−XXX

Diiron Dithiolate Complex Induced Helical Structure of Histone and Application in Photochemical Hydrogen Generation Xiantao Hu, Weijian Chen, Shuyi Li, Jian Sun, Ke Du, Qiuyu Xia, and Fude Feng* Key Laboratory of High Performance Polymer Material and Technology of Ministry of Education, Department of Polymer Science & Engineering, School of Chemistry & Chemical Engineering, Nanjing University, Nanjing 210023, China

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ABSTRACT: Very-lysine-rich calf thymus histone proteins form disordered structure and hydrophobic interaction-driven aggregates in weakly acidic solution. We reported that the conjugation of diiron dithiolate complex to the lysine residues induced formation of helical conformation and condensed nanoassemblies with a high loading capacity up to 18.7 wt %. The incorporated diiron dithiolate complex showed photocatalytic activity for hydrogen evolution in aqueous solutions, with a turnover number (based on [FeFe] catalyst moiety) up to 359 that was more than 6 times that of the free catalyst. The increase of helical conformation in proteins was well correlated to the increasing enhancement of photocatalytic activity. We demonstrated that the [FeFe]−hydrogenase-mimic biohybrid system based on the photocatalyst-induced protein conformational conversion and reassembly is efficient for hydrogen generation regardless of the relatively large size. KEYWORDS: histone, diiron dithiolate complex, helical conformation, biohybrid catalyst, photochemical hydrogen generation

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INTRODUCTION

spleen apoferritin could accumulate a large quantity of [FeFe] catalyst moieties, enhance the hydrogen generation activity, and lead to a high turnover number (TON) up to 8.3 × 103 (based on single protein), by taking advantage of the longdistance electron transfer across the protein shell that was composed of α-helical peptides.17 As compared to the proteins and supramolecular protein assemblies embedding active sites to facilitate the interaction between catalyst and photosensitizer, large sized biohybrids of small peptides and multiple photoactive components are rarely studied and the performance of photochemical hydrogen generation remains to be understood. Histone H1 consists of three distinct domains: a short Nterminal domain (NTD) (20−35 amino acids), a stably folded central globular domain (∼80 amino acids), and a long Cterminal domain (CTD) (∼100 amino acids).18,19 The globular domain is extremely conserved, while the terminal domains, in particular, the CTD, are very rich in lysine (∼40%), fully mobile and intrinsically unstructured in aqueous

Efficient conversion of water molecules into energy-rich H2 using sunlight has been pursued in chemistry and material fields for decades.1−3 Natural hydrogenases catalyze the reduction of protons based on transition metals such as Fe and Ni under mild conditions,4 which inspires considerable efforts in developing artificial photosynthesis systems, among which biomacromolecules including polysaccharides,5,6 polypeptides,7 proteins,8 and membranes9 have shown great potential in improving the performance of catalysts in activity or stability.10 For example, Hayashi et al. coordinated a single iron−carbonyl complex to the apocytochrome c matrix to raise the catalytic activity by a factor of ∼8.11 The β-barrel structure of nitrobindin was found to increase the stability of a diiron dithiolate ([FeFe]) complex modified at the entrance of the cavity.12 Similarly, Utschig and co-workers explored flavodoxin to embed catalyst in the binding pocket or attach photosensitizers to the cysteine residues.13,14 However, for most artificial systems, the catalysts or photosensitizers were mounted to the cysteine residues of proteins via thiol−iron coordination or thiol−maleimide chemistry, and the active sites were limited by the location and amount of accessible cysteine residues.15,16 Most recently, we reported that horse © XXXX American Chemical Society

Received: January 28, 2019 Accepted: May 20, 2019

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DOI: 10.1021/acsami.9b01866 ACS Appl. Mater. Interfaces XXXX, XXX, XXX−XXX

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ACS Applied Materials & Interfaces Scheme 1a

(a) Preparation of H−Fe nanoparticles by amidation reaction between Fe2S2−NHS and lysine residues of histone H1. Protonation of lysine was omitted. The diiron core interacted with histones by covalent linkage at lysine residues and possible coordination between iron and adjacent amino acids. (b) Schematic of the photochemical H2 generation by H−Fe nanoparticles in water. a

solution.20−22 As the CTD has a high helix potential, the neutralization of lysine positive charges by chemical modifications can induce the folding of the CTD with proportions of secondary structure motifs.21,23,24 Herein, we selected commercially available calf thymus histone H1 as the carrier of [FeFe] catalyst because of its exceptional stability of peptide backbones, plenty of lysine residues for immobilization, and most importantly the self-assembly property that allows for extensive study on the protein conformational changes and aggregates.25−28 As shown in Scheme 1, the active ester [Fe2(lip-NHS)(CO)6] (Fe2S2−NHS)29 was conjugated to the lysine residues of disordered histone proteins to form histone-g-Fe2S2 (H−Fe) nanoparticles after a reassembly process. Different from apoferritin encapsulating [FeFe] catalyst via coordination interaction,17 the linkage of histone with [FeFe] catalyst is dominated by covalent amide bonding to ensure no leakage of catalyst in broad pH ranges and induce a conversion of histone proteins from disordered structure to helical structure. With Ru(bpy)32+ as photosensitizer and ascorbic acid as electron sacrificial agent as well as proton donor, the artificial [FeFe]-hydrogenase activity of H−Fe biohybrid nanoparticles was investigated.

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infrared (FT-IR) spectra were measured at ambient temperature on a Bruker ALPHA FT-IR spectrometer. The steady state fluorescence were detected on a Hitachi F-7000 fluorimeter. Average hydrodynamic diameters of nanoparticles and zeta potentials were determined on Zetasizer nanoseries (Nano zs90, Malvern Instruments Ltd., U.K.). Transmission electron microscopy (TEM) images were analyzed on a JEM-2100 TEM instrument (JEOL, Ltd., Japan). Cyclic voltammetry measurements were carried out on a CHI-1230C electrochemical workstation (CH Instruments, Inc. China). Photocurrent response and electrochemical impedance experiments were conducted on a CHI-730E electrochemical analyzer (CH Instruments, Inc. China). Circular dichroism (CD) spectra were obtained via Chirascan CD (Applied Photophysis, U.K.). The Fe content of H−Fe nanoparticles were determined according to the KMnO4 oxidation-based method.31 Protein concentrations were determined by BCA assay. The photocatalytic hydrogen generation experiments were conducted in a 100 mL airtight reactor which was connected to an inline closed gas circulation system (CEL-SPH2N, Beijing China Education Au-light Co., Ltd.). The amounts of evolved hydrogen were determined by gas chromatography (GC-7920, Beijing China Education Au-light Co., Ltd.) equipped with a thermal conductivity detector (TCD) and a 5 Å molecular sieve column. Preparation of H−Fe Nanoparticles. Fe2S2−NHS reacted with histone in 0−20% DMSO solution at a given pH, using conditions shown in Table 1. After reaction overnight at 4 °C, the mixture was

EXPERIMENTAL SECTION Table 1. Preparation Conditions for H−Fe Nanoparticles

Chemicals. All commercially available reagents were purchased and used as received without further purification unless otherwise noted. Fe2S2−NHS was synthesized according to the published literature with minor modification.29,30 Calf thymus histone H1 was obtained from Worthington Biochemical Co. Nafion was purchased from Aldrich as a dispersion of 5% Nafion in aliphatic alcohols. Instruments and Methods. The 1H and 13C NMR spectra were recorded on a Bruker AMX 400 spectrophotometer, and chemical shifts were reported with tetramethylsilane as the internal reference. The ultraviolet−visible (UV−vis) spectra were collected on a Shimadzu UV-2600 spectrophotometer. The Fourier transform B

H−Fe

Rw

DMSO, vol %

Reaction pH

LC, wt %

H−Fe-1 H−Fe-2 H−Fe-3 H−Fe-4 H−Fe-5 H−Fe-6 H−Fe-7

4 4 4 8 8 8 16.7

20 20 20 20 10 0 20

6.0 5.0 4.0 4.0 4.0 4.0 4.0

18.7 14.5 10.7 7.9 9.4 11.0 4.8


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ACS Applied Materials & Interfaces

Figure 1. Characterization of Fe2S2−NHS, histone H1 and H−Fe-1. (a) UV−vis absorption spectra of Fe2S2−NHS in acetonitrile, histone and H− Fe-1 in water. (b) FT-IR spectra of histone, Fe2S2−NHS and H−Fe-1. (c) The size distribution of histone and H−Fe-1 in water at pH 5.0. (d) TEM image of H−Fe-1. Scale bar indicates 200 nm. electrode and dried, followed by coating of Ru(bpy)3Cl2 (40 μL) and Nafion (40 μL) to produce the working electrode modified with Fe2S2−NHS and Ru(bpy)3Cl2; (3) The H−Fe-1 (20 μL, 1.88 mM incorporated [FeFe] catalyst) was coated onto another ITO electrode and dried, followed by coating of Ru(bpy)3Cl2 (40 μL) and Nafion (40 μL) to produce the working electrode modified with H−Fe-1 and Ru(bpy)3Cl2. An Xe-lamp (λ > 380 nm) was used as light source and 0.1 M Na2SO4 aqueous solution was used as the electrolyte. Electrochemical impedance spectra (EIS) measurements were also carried out in the above-mentioned three-electrode system and recorded over a frequency range of 0.1−103 Hz at −1.2 V. Photochemical Hydrogen Evolution Experiments. The experiments were conducted in a quartz cell containing 25 mL of photochemical reaction mixture containing certain amounts of H−Fe, Ru(bpy)3Cl2, and ascorbic acid. The pH was adjusted to a given value using aq. NaOH or HCl. The whole device was vacuumed until the pressure gage was kept stable at −0.1 MPa to deprive of oxygen, and the reaction mixture was irradiated by a 300 W Xe-lamp (200 mW cm−2, Beijing China Education Au-light Co., Ltd.) with a light cutoff filter (λ ≥ 400 nm). The headspace gas was automatically extracted at a 15 min interval and measured by GC using nitrogen as the carrier gas. After photochemical reaction was completed, 1 mL of hydrogen was immediately injected into GC as the internal standard for quantitation of evolved hydrogen. Analysis of Iron Leaching after Photochemical Hydrogen Evolution. After photochemical reaction for H−Fe-1, the reaction mixture was dialyzed with molecular weight cutoff of 10000 Da and concentrated by polyethylene glycol. The iron concentration was determined by the KMnO4 oxidation based method, and the overall iron content was compared with the initial iron content.31 Quantum Yield Measurement..34,35 For measurement of H2 generation quantum yield (QY), the number of reacted electrons is equal to the double amount of H2 in moles, and the number of incident photons is calculated from the power of the incident light (400 nm Xe-lamp, 200 mW cm−2), in which the irradiated area is confined in 20 cm2. In a 1 h irradiation, the amount of hydrogen generated is about 17 μmol, so the QY can be calculated as ∼0.073% according to the following formula:

dialyzed with molecular weight cutoff of 10 000 Da. To investigate the self-assembly process, 2 mL of solution was taken out of the reaction mixture after varying reaction time (1−19 h) and dialyzed before TEM imaging. Circular Dichroism Measurements. CD spectra were recorded in the far-ultraviolet wavelength range of 190−260 nm in a quartz cell (0.1 cm) using the following parameters: bandwidth, 1 nm; step resolution, 0.1 nm; scan speed, 10 nm min−1; and response time, 1 s. The data of each spectrum was acquired as the average of three scans. All samples were tested at the same protein concentration (25 μg mL−1 in water at pH 5.0). Thioflavin T Fluorescence Assay. Each of histone samples (300 μg mL−1) was incubated with 20 μM ThT at pH 5.0 at 37 °C with shaking at 600 rpm. The fluorescence intensities were measured at 1 h interval with excitation at 450 nm and emission at 485 nm. Photoelectrochemical Measurements. Cyclic voltammetry experiments were carried out on an electrochemical analyzer (CHI1230C, CH Instrument Inc., Shanghai), using a one-compartment three electrode cell at room temperature with a 3 mm glassy carbon working electrode, a platinum wire auxiliary electrode and an Ag/ AgCl (saturated KCl) reference electrode. The glassy carbon working electrode was polished with a 0.05 mm alumina paste and sonicated for 10 min. The 0.1 M n-Bu4NPF6 and 0.1 M Na2SO4 were used as the supporting electrolyte solutions for measurement in acetonitrile and aqueous media, respectively. Before each measurement, the solution was purged with N2 for 30 min and then measured at a scan rate of 50 mV s−1. All potentials were obtained against NHE via E(NHE) = E(Ag/AgCl) + 0.197 V.32,33 Photocurrent response experiments were conducted at a bias potential of 0.5 V on an electrochemical analyzer (CHI730E) with a standard three-electrode system, using prepared samples as the working electrodes with an active area of ca. 1 cm2, a platinum wire as the counter electrode and Ag/AgCl (saturated KCl) as a reference electrode. The working electrodes were prepared as follows: (1) Ru(bpy)3Cl2 aqueous solution (40 μL, 23 mM) was mixed with Nafion (40 μL) to form a slurry. The slurry was then coated onto a 1 cm2 indium tin oxide (ITO) electrode, and dried in an oven at 80 °C for 2 h to produce working electrode modified with Ru(bpy)3Cl2; (2) The Fe2S2−NHS (24 μL, 1.54 mM) was coated onto an ITO C


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ACS Applied Materials & Interfaces QY =

lowered Rw of 4. However, Rw smaller than 4 risked emergence of precipitates. Changing pH had a more obvious influence on the composition of H−Fe. At a fixed Rw of 4 in the presence of DMSO, higher pH (pH < 7.0 to avoid precipitation of protein) was more favorable for amidation reaction44,45 and led to greater LC up to 18.7 wt % (pH 6.0). DLS analysis (Figure S3) showed that the DH values of these H−Fe nanoparticles were ranging from 105.7 to 141.8 nm. Amidation-Induced Conformational Change. Interestingly, the far-UV CD spectra revealed conformational changes of histone H1 before and after loading of catalyst. As shown in Figure 2a, natural histone proteins at pH 5.0 presented large

2n(H2)NAhc t(s) P(w cm−2)S(cm 2)λ

where n(H2) is the mole number of hydrogen generated, NA is the Avogadro constant (6.02 × 1023 mol−1), h is the Planck constant (6.63 × 10−34 J·s), c is the light speed (3.00 × 108 m s−1), t is the irradiation time, P is the light power density, S is the irradiation area, and λ is the incident wavelength.

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RESULTS AND DISCUSSION

Structure and Photophysical Properties of H−Fe Nanoparticles. The H−Fe nanoparticles were obtained by amidation reaction in water containing varied proportions of DMSO and stored in deionized water or as a red solid after lyophilization. The UV−vis spectra of H−Fe in water showed intense absorption at 274 and 330 nm (Figure 1a), well consistent with the absorption characteristics of histone and [FeFe] catalyst. In the FT-IR spectra (Figure 1b), the stretching CO bonds of [FeFe] catalyst36 were unchanged at 2071 (s), 2026 (s), and 1980 (sh) cm−1 before and after conjugation to histone H1 that indicated strong amide vibration bonds at 1622 and 1528 cm−1.37 The vibrational signal of NHS at 1815, 1786, and 1738 cm−1 disappeared as a result of amidation reaction.38 Histone H1 in water at pH 5.0 showed an average hydrodynamic diameter (DH) of 122.4 nm (Figure 1c) as determined by dynamic light scattering (DLS) analysis, owing to the strong propensity of histone H1 to exist in an association state like fibrils or amorphous aggregates as revealed by the imaging of transmission electron microscope (TEM, Figure S1).39,40 One of possible reasons for the slight increase of DH for H−Fe-1 (141.8 nm, Figure 1c) relative to histone H1 was attributed to the reduced hydrophilicity of proteins after modification of primary amines and thereby loss of positive charges. The appearance of H−Fe-1 in a compact lump structure imaged by TEM (Figure 1d) suggested occurrence of a reassembly process of proteins upon linkage of [FeFe] catalyst. The TEM images (Figure S2) also showed that the biohybrid particles gradually grew into larger and more compact structures as Fe2S2−NHS and histone H1 was mixed in 20% DMSO (pH 6.0) over increasing times (1−19 h), which is consistent with the reassembly process. As a result, the zeta-potential of H−Fe-1 was much more positive than histone H1 (+20.2 mV vs +10.1 mV), although the content of free lysine residues was reduced. By changing the feed weight ratio (Rw) of histone to Fe2S2− NHS, the proportion of DMSO and pH in reaction solution, we obtained H−Fe-1 to H−Fe-7 (Table 1) and the content of diiron catalyst in the H−Fe products was estimated by iron quantification according to the KMnO4 oxidation based method.31 The amounts of proteins in H−Fe products were estimated by BCA assay. A proportion of DMSO was used to enhance the solubility of hydrophobic Fe2S2−NHS, extend the structure of histone, and weaken the possible noncovalent adsorption of [FeFe] catalyst.41−43 The loading capacity (LC) was defined as the weight ratio of loaded [FeFe] catalyst to H−Fe (for calculation of LC, the structural formula of incorporated catalyst was expressed as [Fe2{(m-SC2H4)(mSCH)(CH2)4CO−}(CO)6]). At pH 4.0, the LC at Rw 8 was 11.0 wt % in water, and decreased as the DMSO content in reaction was increased because of diminished nonspecific adsorption. With DMSO/H2O (1:4, v/v) as solvent, the LC was only 4.8 wt % at Rw 16.7 and rose to 10.7 wt % at a

Figure 2. (a) CD spectra of histone proteins (25 μg mL−1) and H−Fe nanoparticles (25 μg mL−1 incorporated histone) in water (pH 5.0). Histonea and Histoneb denote the untreated histone H1 and histone treated by 20% DMSO, respectively. (b) ThT fluorescence after interaction of ThT (20 μM ThT) with histone proteins and H−Fe nanoparticles (300 μg mL−1 histone) in water (pH 5.0).

negative ellipticity in the 190−200 nm region and weak negative ellipticity at 222 nm, which indicated the untreated proteins were generally in the disordered form.46 The disordered conformation of proteins was not affected after treatment with reaction solvent (20% DMSO in water), as evidenced by the unchanged CD signal. However, significant changes of CD spectra in the intensities at 190−200 and 222 nm took place for H−Fe which was prepared in 20% DMSO solution. As the LC increased, the ellipticity near 190 nm region was changed from negative to positive, and the new negative minimum at ca. 206 nm is supposed to originate from n → π* transition for the peptide bond of α-helices,47 accompanied with a stronger negative band at 222 nm. These phenomena were in analogy to the acetylation or metal ions (e.g., Cu2+ and Ni2+)-induced conformational changes of histone,48−51 and suggested a transition from the original disordered state to more ordered state, particularly generation of α-helical secondary structure. The formation of ordered secondary conformation in the biohybrid system was ascribed to the enhanced hydrophobicity23,52 after reducing the quantity of protonated lysine residues by conjugation with [FeFe] complex, and could ensure that [FeFe] complex moieties resided in a more rigid environment. These structural properties were favorable for electron transfer from electron donors to the active catalytic sites.53,54 Meanwhile, the profound conformational changes were reasonably responsible for the observation with the more dense morphology imaged by TEM (Figure 1d) and more positively charged surface detected by zeta potential measurement. We checked the form of histone H1 and H−Fe nanoparticles in water at pH 5.0 using Thioflavin T (ThT), which D


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ACS Applied Materials & Interfaces was widely accepted to probe hydrophobic protein fibrils.39 As shown in Figure 2b, ThT fluorescence at 480 nm was gradually enhanced over a period of 0−3 h in the presence of histone H1 to indicate the protein fibrillation which originated from hydrophobic interactions, and came to a plateau after 3 h. This finding was consistent with the aggregation behavior of natural histone H1 detected by DLS and TEM. The quenching events were present with H−Fe bound ThT (Figure 2b), and the steady increase of ThT fluorescence with incubation time correlated to the slowed accumulation of ThT into protein fibrils. As [FeFe] complex has poor spectral overlap with ThT, a mechanism of electron transfer from excited dyes to metal complex, rather than energy transfer, likely contributed to the low level of fluorescence. The efficient quenching events suggest the long-distance electron transfer likely occurs, favored by the helical structures of proteins. The reduced exposure of hydrophobic protein segments for the condensed H−Fe nanoparticles may aggravate the weakening of ThT fluorescence. Electron Transfer Between Photosensitizer and H−Fe Nanoparticles. To investigate the electron transfer between photosensitizer and the incorporated [FeFe] complex, we monitored the gradual quenching of Ru(bpy)32+ luminescence (λex456 nm, λem630 nm) by titrating H−Fe-1 into the aqueous solution (pH 5.0) that contained sodium ascorbate (10 mM) and Ru(bpy)3Cl2 (5 μM). The fluorescence intensities in the absence and presence of H−Fe-1 at a catalyst concentration (Ccat) were denoted as I0 and Ip, respectively. The KSV was estimated to be 5.0 × 103 M−1 according to the Stern−Volmer plot by plotting (I0/Ip − 1) values against Ccat (Figure S4), reflecting efficient electron transfer between Ru(bpy)32+ and incorporated catalyst. We also examined the electrochemical properties of Fe2S2− NHS and H−Fe by cyclic voltammetry (CV). Glass carbon electrode was used as the working electrode and the free diiron catalyst Fe2S2−NHS showed a reduction peak at −0.75 V vs NHE in CH3CN (Figure S5a). By comparison, the reductive potential of H−Fe-1 determined as −0.57 V vs NHE in aqueous solution was more positive than that of free Fe2S2− NHS (Figure S5b). This decline was due to the effect of solvent and protein environment. In previous reported works, there was an evident shift in the reduction potential of Co(dmgH)2 pyCl and [Ni(P2PhN2Ph)2](BF4)2 when bound with PSI and apoflavodoxin.13,55 Besides, the reduction potential of photocatalyst necessary for H2 generation has a significant solvent dependence,55,56 in good agreement with that H−Fe-1 in water accepted electrons more easily than Fe2S2−NHS in CH3CN. Furthermore, the reductive potential of H−Fe-1 and [FeFe] catalyst was strikingly more positive than that of Ru(bpy)3+ (−1.30 V vs NHE).56,57 The greater driving force renders a faster electron transfer to catalyst and allows for the [FeIFeI] state to be reduced to the [FeIFe0] state.58 Hence, the effective electron transport can ensure photocatalytic H2 generation. To further examine the role of histone H1 in photoinduced electron transfer from Ru(bpy)3Cl2 to [FeFe] catalyst, we measured the photocurrent response of 1) pure Ru(bpy)3Cl2, 2) Ru(bpy)3Cl2/Fe2S2−NHS and 3) Ru(bpy)3Cl2/H−Fe-1 deposited on indium tin oxide (ITO) electrode by several on− off cycles of illumination in 0.1 M Na2SO4 aqueous solution. As shown in Figure 3a, apparent photocurrent response was observed for all three samples, indicating an efficient separation of photoinduced electron−hole and successful transfer of

Figure 3. (a) Photocurrent response of Ru(bpy)3Cl2, Ru(bpy)3Cl2/ Fe2S2−NHS and Ru(bpy)3Cl2/H−Fe-1 deposited on ITO electrode. (b) EIS Nyquist plots of Fe2S2−NHS and H−Fe-1. Measurements were conducted in 0.1 M Na2SO4 aqueous solution.

excited state electrons to the ITO glass. The photocurrent intensity of the Ru(bpy)3Cl2/Fe2S2−NHS deposited electrode was about 2 times larger than that of Ru(bpy)3Cl2, which suggested [FeFe] catalyst may accelerate the electron transfer and suppress the photoinduced electron−hole recombination. In comparison, the photocurrent response of Ru(bpy)3Cl2/H− Fe-1 is higher than that of Ru(bpy)3Cl2/Fe2S2−NHS or Ru(bpy)3Cl2 alone. The increase of α-helical structure in H− Fe could be a pivotal factor in promoting electron transfer process. It is common that a protein matrix possesses good electroconductivity to facilitate electron transfer and lower charge recombination.17,53 However, a continuous attenuation of photocurrent intensity occurred with the increased of switch-on/off cycles, likely due to the charge recombination.59 We also measured the electrochemical impedance spectra (EIS) of Fe2S2−NHS and H−Fe-1 in a three-electrode system over a middle frequency region ranging from 0.1 Hz to 1 kHz, which provided the charge transfer resistance across electrode/ electrolyte interface. In the Nyquist diagram, a smaller semicircle reflects a lower interfacial charge transfer resistance and more efficient charge transfer process.60,61 According to the Nyquist plots (Figure 3b), H−Fe-1 sample showed the smaller semicircle as compared to that of Fe2S2−NHS, which further confirmed the faster interfacial electron transfer of the biohybrid system relative to pure [FeFe] catalyst.62,63 Photochemical Hydrogen Generation Using H−Fe Nanoparticles as Biohybrid Catalysts. The photochemical H2 evolution behavior of H−Fe nanoparticles was studied in conventional acidic conditions. The reaction mixture (25 mL, pH 5.0) was irradiated under vacuum by visible light (200 mW cm−2) via an Xe-lamp (300 W, λ > 400 nm). The volume of evolved H2 was measured at 15 min intervals by gas chromatography (GC). As shown in Figure 4a, as compared to the photocatalytic system containing H−Fe-7 (8 μM incorporated catalyst, referred to solution molarity in terms of [FeFe] catalyst moiety in the H2 generating solutions), Ru(bpy)32+ (140 μM) and ascorbic acid (40 mM), negligible H2 was detected in the control experiments with at least one component absent, which revealed that each component was indispensable for the photochemical H2 generation. It is noteworthy that the photochemical H2 generation ceased after 4 h. This phenomenon was also found in the previous reports,15,64 attributed to the decomposition of catalyst that involved photosensitized dissociation of Fe-CO bonds.17,65,66 According to the iron content assay, the amount of [FeFe] catalyst in H−Fe nanoparticles was reduced by 26.5% after photochemical H2 generation, which implied that the leaching E


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Figure 4. (a) Photochemical H2 evolution in the solutions containing two or three components of Ru(bpy)32+ (140 μM), ascorbic acid (40 mM), and H−Fe-7 (8 μM incorporated [FeFe] catalyst) in water at pH 5.0. (b) Photochemical H2 generation by irradiation of solutions containing H− Fe with different LC (4 μM incorporated [FeFe] catalyst), Ru(bpy)32+ (300 μM), ascorbic acid (160 mM) in water at pH 5.0.

Figure 5. TON values for H−Fe system by 4 h irradiation of solutions containing (a) H−Fe-1 (4 μM incorporated catalyst), Ru(bpy)32+ (400 μM), and ascorbic acid (160 mM) at varied pH values, (b) H−Fe-1 (4 μM incorporated catalyst), ascorbic acid (160 mM), and varied concentrations of Ru(bpy)32+ at pH 5.0, or (c) H−Fe-1 (4 μM incorporated catalyst), Ru(bpy)32+ (400 μM), and varied concentrations of ascorbic acid at pH 5.0. (d) Comparison of H2 evolution by 4 h irradiation of solutions containing Ru(bpy)32+ (400 μM), ascorbic acid (160 mM), and H− Fe-1 (4 μM or 6 μM incorporated catalyst) or free Fe2S2−NHS (4 μM) at pH 5.0.

donation of electrons to the excited photosensitizer.68 That was why the downward angled curvature appeared in the plot of evolved H2 TON against pH value (Figure 5a). At pH 5.0 that was optimal in the presence of 4 μM incorporated catalyst, 400 μM Ru(bpy)32+ and 160 mM ascorbic acid, the TON in 4 h reached 340, which was 6 and 12 times that determined at pH 4.0 and pH 6.0, respectively. In comparison to the pH effect, Ru(bpy)32+ and ascorbic acid concentrations affected the photochemical reaction in a much lesser extent. As shown in Figure 5b, the reaction was tested with Ru(bpy)32+ in the range of 100 to 700 μM, and the highest TON was achieved in the presence of 400 μM Ru(bpy)32+. Decreasing the amount of Ru(bpy)32+ to only 100 μM caused a slump of the TON by 30% in 4 h, reflecting that the electron transfer from the excited photosensitizer was inefficient. However, high concentration of photosensitizer also caused a loss of TON because of the increasing triplet−triplet annihilation among photosensi-

of iron upon photochemical reaction could be another reason for the leveling off H2 generation. As LC increased, the photochemical H2 generation was more efficient, well correlated with the increasing conversion of random protein coils into helical secondary conformation (Scheme 1 and Figure 2a). Under the same condition, irradiation of the 25 mL solutions containing H−Fe nanoparticles (4 μM incorporated catalyst), Ru(bpy)32+ (300 μM) and ascorbic acid (160 mM) at pH 5.0 generated greater amount of H2 as LC increased (Figure 4b). We selected H−Fe-1 for optimization of photocatalytic conditions including pH, Ru(bpy)32+ and ascorbic acid concentrations, since H−Fe-1 exhibited the greatest TON (on a basis of diiron catalyst moiety) (Figure 4b). In general, acidic condition gave rise to high concentration of protons for accepting electrons from reduced [FeFe] catalyst.67 However, too low pH could reduce the availability of ascorbate in F



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tizers.11,69 The concentration of ascorbic acid greater than 160 mM indicated insignificant impact on TON (Figure 5c). Under the optimal condition, the activity of the incorporated catalyst (4 μM) over 6 h of light irradiation was enhanced relative to that of free catalyst (4 μM) (TON 359 versus 54, based on the [FeFe] catalyst moiety, Figure 5d). The photonto-H2 quantum yield for H−Fe-1 system was calculated to be 0.073%, which was comparable to the previously reported systems using Ru-based photosensitizers.70−73 As aforementioned, the ordered structure of histone proteins induced by the functionalization of [FeFe] complex plays an important role in catalyst stabilization and long-distance electron transfer, which benefits the amplified activity of incorporated catalyst. Moreover, as Ccat increased from 4 to 6 μM, the volume of evolved H2 over 6 h reached 1.2 mL with a marginal TON fluctuation. The TON up to 359 (based on 6 h of light irradiation) and the initial turnover frequency (TOF) up to 1.8 min−1 (based on the initial 2 h of light irradiation) in this system are comparable to or advantageous over most of the reported polypeptide and protein matrix-based artificial photosynthesis systems (Table S1). After 1 week storage at a high Ccat of 120 μM and 4 °C, H−Fe-1 showed an unchanged absorption spectrum and DH (Figure S6), and most importantly maintained the catalytic activity comparable to the initial state (Figure S7), which highlighted the excellent stability of the biohybrid system.

ACKNOWLEDGMENTS We’re grateful to Prof. Wei Wang (Nanjing University) for help with DLS measurements, Prof. Danke Xu (Nanjing University) and Prof. Weiyin Sun (Nanjing University) for support of photoelectrochemical measurements. We thank National Key R&D Program of China (2017YFA0701301), National Basic Research Program of China (2015CB856300), and Program for Changjiang Scholars and Innovative Research Team in University (IRT1252) for financial support.

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CONCLUSIONS In summary, we incorporated a diiron dithiolate complex into random-coiled histone H1 by covalent linkage, and elucidated a reassembly process that involved a conversion of disordered protein structure to helical structure. The remarkable conformational changes were induced by the conversion of hydrophilic protonated amines of lysine residues into hydrophobic [FeFe] complex moieties. The formation of ordered protein structure as well as possible coordination interaction of [FeFe] complex with adjacent amino acids led to much more condensed nanoassemblies as compared to the natural state of histone H1 in aqueous solution. The biohybrid system showed excellent stability and enhanced activity in photochemical H2 generation with a TON up to 359 (based on [FeFe] catalyst) or ∼3 × 103 (based on single protein), and will spur the development of biomimetic photocatalysts for efficient photochemical H2 generation. ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acsami.9b01866.

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REFERENCES

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Research Article

TEM images, DLS analysis, Stern−Volmer plots, cyclic voltammograms, UV−vis spectra, and comparison of the reported photochemical systems (PDF)

AUTHOR INFORMATION

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*E-mail: [email protected]. ORCID

Fude Feng: 0000-0002-5348-5959 Notes

The authors declare no competing financial interest. G


Research Article

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Diiron Dithiolate Complex Induced Helical Structure of Histone and

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