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Biomimetic Oxygen-Evolving Photobacteria Based on Amino Acid and Porphyrin Hierarchical Self-Organization Kai Liu,†,§ Han Zhang,† Ruirui Xing,† Qianli Zou,† and Xuehai Yan*,†,‡,§ †

State Key Laboratory of Biochemical Engineering and ‡Center for Mesoscience, Institute of Process Engineering, Chinese Academy of Sciences, 100190 Beijing, China § University of Chinese Academy of Sciences, 100190 Beijing, China S Supporting Information *

ABSTRACT: Biomimetic organization provides a promising strategy to develop functional materials and understand biological processes. However, how to mimic complex biological systems using simple biomolecular units remains a great challenge. Herein, we design and fabricate a biomimetic cyanobacteria model based on self-integration of small bioinspired molecules, including amphiphilic amino acid, 3,4-dihydroxyphenylalanine (DOPA), and metalloporphyrin and cobalt oxide nanoparticles (Co3O4 NPs), with the assistance of chemical conjugation and molecular self-assembly. The assembled amino acid fiber can be modified by DOPA to form covalently bound DOPA melanin containing hydroxyl and quinone species via Schiff base reaction. The adhering template can further tune the self-assembly of metalloporphyrin and Co3O4 NPs into Jaggregation and dispersive distribution, respectively, mainly via coordination binding. Metalloporphyrin molecules in the resulting hybrid fibers capture light; quinone species accept the excited electrons, and Co3O4 NPs catalyze water oxidation. Thus, the essential components of the photosystem-II protein complex in cyanobacteria are simplified and engineered into a simple framework, still retaining a similar photosynthetic mechanism. In addition, this architecture leads to efficient coupling of antenna, quinone-type reaction center, and photocatalyst, which increases the flux of light energy from antenna to reaction center for charge separation, resulting in enhanced oxygen evolution rate with excellent sustainability. KEYWORDS: amino acids, porphyrins, self-organization, oxygen evolution, biomimetic photosynthesis

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four redox equivalents are accumulated and water is split to oxygen.9 Over billions of years of evolution, the oxygenic photosystem has remained similar in cyanobacteria, algae, and plants,10 indicative of its perfect performance. Therefore, design and fabrication of biomimetic PSII with optimization of primary structure is an excellent paradigm for solar energy utilization and deep insight into the complex photosynthetic oxygen evolution process. Due to the large size and structural complexity of PSII, it is only feasible to engineer a “minimal” structural unit that encompasses the essential cofactors.11 Focus has mostly been on integration of pigments (e.g., semiconductors and organic

xygenic photosynthesis leads to the great oxidation event and provides conditions for aerobic metabolism in the evolution of life.1,2 Oxygen evolution has also been recognized as a bottleneck in artificial photosynthetic schemes, as it is a kinetically slow process.3 Cyanobacteria first made a breakthrough with photosystem-II (PSII) relying on sophisticated organization of various pigments and redox-active cofactors within the protein environment to realize highly efficient light harvesting and charge separation (Scheme 1a,b).4−6 The protein template plays a major role in modulating energy transfer and redox properties of the cofactors.7 The trapped energy from pigment−protein complexes can excite the primary electron donor P680, which is formed by chlorophyll molecules, to eject an electron to the quinone-type electron acceptor (Scheme 1c,d).8 The generated P680•+ species extract electrons from an inorganic catalyst CaMn4O5 cluster, where © 2017 American Chemical Society

Received: November 19, 2017 Accepted: December 1, 2017 Published: December 1, 2017 12840

DOI: 10.1021/acsnano.7b08215 ACS Nano 2017, 11, 12840−12848

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Cite This: ACS Nano 2017, 11, 12840−12848

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(a) Optical image of fibrous marine cyanobacteria.64 (b) Schematic illustration of the architecture of PSII in cyanobacteria, that is, proteintemplated organization of antenna and reaction center. (c) Schematic illustration of antenna in PSII, which is composed of several arranged chlorophylls. (d) Schematic illustration of reaction center in PSII. The pink lines indicate electron transfer from CaMn4O5 to primary electron donor P680 and to quinone. The yellow line represents energy transfer from antenna to reaction center. The models of antenna and reaction center are extracted and simplified from the PSII in Protein Data Bank (id: 1IZL). (e) Schematic representation of the biomimetic cyanobacteria fabricated by assembled fiber-templated self-integration of antenna, quinone-type reaction center, and photocatalyst for oxygen evolution. a

adhesive and cohesive behavior.37 The interfacial adhesion is associated with the catechol group, which interacts with metal ions and metal oxides through a coordination bond or hydrogen bond.38,39 The quinone form of DOPA is primarily responsible for cross-linking reactions to solidify the protein adhesive.40 In addition, quinone species can undergo Michaeltype addition and/or condensation reactions with nucleophiles, such as primary amines.41−43 Inspired by the mussel protein, synthetic chemistry approaches have been adopted to form DOPA-conjugated polymers or polypeptides to work as adhesive,44,45 self-healing polymer,46 and surface coating for metal oxides.47 DOPA-containing self-assembling peptides have been designed to form ordered supramolecular nanostructures substantially decorated with catechol functional groups.48 Although great successes have been achieved in these studies, the synthetic translation is a tough work due to DOPA’s inherent susceptibility to oxidation.49 An alternative way is to directly use the DOPA monomer based on the chemical basis. DOPA melanin can be generated through autoxidation and selfpolymerization of DOPA and shows various properties, such as conductivity, antioxidation, and radical scavenging.50 In situ formation of DOPA melanin has been used to modify many inorganic and organic substrates,51−54 which exclusively focus on structural integration in view of the adhesive behavior of DOPA melanin. Taking full advantage of the multifunctionality, DOPA melanin can be envisaged not only as adhesive for architectural construction but also as an active component to participate in physicochemical processes, such as electron mediation, leading to alternative perspectives of exploitation of DOPA. Herein, we develop a biomimetic cyanobacteria model through peptide-templated self-integration of light-harvesting antenna, quinone-type reaction center, and photocatalyst, which mimics architectural principles and functional mechanisms of PSII (Scheme 1e). Aromatic peptide amphiphiles are popular building blocks with the propensity to form β-sheet structures by combination of aromatic stacking interactions and hydrogen bonding.24 Amino acids modified with the 9fluorenylmethyloxycarbonyl (Fmoc) group have lower synthesis costs but still maintain similar structural features, and the

dyes) with photocatalysts/quinones on the molecular level by chemical deposition/conjugation or direct mixture. 12−16 Although high efficiency for photocatalytic performance can sometimes be obtained, these devices generally lack hierarchically organized architectures and finely tuned reaction coordinates, for example, for energy transfer and charge separation. Molecular self-organization is a bottom-up approach to fabricate functional materials with appreciation of the roles of architecture.17−20 Inspired by nature, artificial model proteins have been designed to systematically bind single pigment and a quinone molecule to mimic the quinone-type reaction center.21,22 A virus scaffold protein has been used to mediate the co-organization of pigments and photocatalysts to significantly improve the light-driven water oxidation performance.23 However, genetic modification and protein screening are inevitable to obtain special cofactor (i.e., porphyrin, metallic oxide) binding sites, which requires complicated and timeconsuming operation. Peptides are among the most common building blocks because of their simple structure, easy modification, and controllably assembled structure. 24−26 Biomimetic light-harvesting systems have already been fabricated using short peptide- and even amino acid-tuned self-organization of porphyrins based on templated selfassembly,27−29 binary co-assembly,30,31 and self-assembly of a peptide−porphyrin complex.32 However, reports about the further integration of the antenna module with charge separation center are relatively fewer, expect for the case of in situ mineralization of titanium dioxide,33,34 because it requires sophisticated design for multicomponent integration and strict conditions for energy-level matching. To the best of our knowledge, a biomimetic electronic mediator (e.g., quinone species) has never been directly investigated to funnel the energy from antenna assembly for charge separation, but these are most relevant for the biological function. Therefore, it still remains a big challenge to develop PSII mimics using a facile and efficient method to reciprocally integrate an antenna and photosynthetic center where charge separation and photocatalysis occur.35,36 3,4-Dihydroxyphenylalanine (DOPA, Figure S1a) is the core functionality in mussel foot proteins that endow them with 12841

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Figure 1. (a) TEM image of Fmoc-L-Lys fibers. (b) SEM image of Fmoc-L-Lys fibers without metal spraying. (c) CD spectra of Fmoc-L-Lys solution and assembled Fmoc-L-Lys fibers. (d) FTIR spectrum of Fmoc-L-Lys fibers. (e) Fluorescence spectra of Fmoc-L-Lys solution and Fmoc-L-Lys fibers (λex = 280 nm). Inset is the enlarged fluorescence spectra. (f) Schematic illustration of the molecular packing pattern in Fmoc-L-Lys fibers. The yellow and blue parts represent fluorenyl groups and lysine, respectively. The pink dashed lines are the intermolecular hydrogen bond between carbonyl and amino groups.

resultant supramolecular structures are easier to modify.25 Therefore, 9-fluorenylmethoxycarbonyl-L-lysine (Fmoc-L-Lys, Figure S1b) is chosen as a model of amphiphilic amino acid, with additional advantage of having the chemically active primary amine. A nanofiber template is prepared by selfassembly of amphiphilic Fmoc-L-Lys. Then an adhering layer is incorporated by a Schiff base reaction between the ε-amino group on the surface of Fmoc-L-Lys fibers and DOPA melanin. Sn(IV)tetrakis(4-pyridyl)porphyrin (SnTPyP, Figure S1c) and Co3O4 NPs, mimicking chlorophyll and the inorganic core of PSII, respectively, are co-assembled onto the adhering fibers in close proximity mainly via coordinate bond and electrostatic interaction. The quinone species acts as an electron mediator to accept the electrons from photoexcited Sn(IV)TPyP* to form a radical cation Sn(V)TPyP+. The holes are accumulated on Co3O4 NPs to drive water oxidation. The resulting architecture can be regarded as a prototype of cyanobacteria for oxygenic photosynthesis. The SnTPyP molecules are strongly coupled in a circle on the fibers with a close distance to quinone species and Co3O4 NPs, which facilities energy transfer and charge separation, resulting in significantly enhanced oxygen evolution compared to the free system. This study provides an experimental case for constructing biomimetic architectures by adaptive and hierarchical self-organization of simple biologyinspired molecules.

spraying (Figure 1b), indicative of the inherent conductivity. Circular dichroism (CD) shows a negative peak at 218 nm for Fmoc-L-Lys fibers (Figure 1c), suggesting a β-sheet structure, as further proven by the peaks at 1685 and 1635 cm−1 in the Fourier transform infrared (FTIR) spectroscopy analysis (Figure 1d), which are ascribed to the hydrogen bond in the β-sheet.25 In the CD spectrum, the absorbance between 250 and 350 nm is attributed to transitions from fluorenyl− fluorenyl interactions (Figure 1c). After assembly, the main emission peak of Fmoc-L-Lys is red-shifted from 319 to 326 nm, and a wide peak around 400−600 nm is generated (Figure 1e). These results suggest that the fluorenyl groups are arranged in strongly ordered chiral structures via π−π stacking.55 This aggregation facilitates charge transfer and makes Fmoc-L-Lys fibers conductive, contributing to electron transfer in catalytic reactions. Electrostatic screening by changing pH induces Fmoc-L-Lys molecules to self-assemble into fibrous scaffolds based on π-stacking and hydrogen bonding (Figure 1f). The amphiphilic nature makes the hydrophobic fluorenyl remain buried in the fiber core and hydrophilic amino groups stand on the periphery. In alkaline condition (e.g., pH 8.0), the DOPA solution becomes brown (Figure S3), indicative of DOPA melanin, which arises from the oxidation of DOPA into DOPA quinone and then polymerization.40,56 Under the same conditions, the incubation of Fmoc-L-Lys fibers with DOPA led to deep brown precipitates (Figure S4a), indicating that the DOPA melanin is integrated on the fibers. The precipitates (abbreviated as FmocL-Lys/DOPA, where DOPA here means the initial ingredient and actual component is DOPA melanin) have a fibrous structure (Figure 2a,b) and remain as a β-sheet from Fmoc-LLys fibers (Figure S4b), suggesting that the DOPA melanin does not disturb the self-assembly of Fmoc-L-Lys. After corrosion of Fmoc-L-Lys/DOPA by hydrochloric acid, fibrous

RESULTS AND DISCUSSION After tuning the acid Fmoc-L-Lys solution to pH value of 4.0− 9.0, white turbid liquid appears (Figure S2a), indicating the formation of assembled structures. Transmission electron microscopy (TEM) and scanning electron microscopy (SEM) images reveal a network of solid fibers with diameters of ∼200 nm (Figure 1a) and lengths of ∼50 μm (Figure S2b). Fmoc-LLys fibers can be directly observed by SEM without metal 12842

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Figure 2. (a) TEM and (b) SEM images of Fmoc-L-Lys/DOPA fibers. (c) TEM image of Fmoc-L-Lys/DOPA fibers after treatment with 1 M HCl. (d) ESI-MS spectra of the Fmoc-L-Lys/DOPA fibers dissolved in hexafluoroisopropanol (HFIP). The inset is the high-resolution MS spectra centered around the m/z peak of 735. (e) Molecular structure deduced from (a) with a molecular weight of 736. (f) SEM image of Fmoc-L-Lys/DOPA fibers after incubation with silver nitrate (AgNO3). Inset is energy-dispersive X-ray (EDX) spectrum of (f), confirming that the decorated nanoparticles are Ag NPs. (g) Atomic force microscope (AFM) image of Fmoc-L-Lys/DOPA fibers after incubation with ferroferric oxide (Fe3O4) NPs, showing granular protuberances. (h) UV−vis spectra of the solution of Fmoc-L-Lys/DOPA fibers after incubation with ferric chloride (FeCl3) at pH 8.0. Inset is the photograph of the mixed solution.

DOPA fibers are adhesive and can bind metal oxide and metal ions, possibly due to the coordination bonds between the DOPA hydroxyl and the metal atoms.57,58 In addition, the amount of incorporated DOPA melanin in the Fmoc-L-Lys/ DOPA fibers can be flexibly tuned as required (Figure S6). Our results prove a moderate strategy to utilize the interfacial covalent character of DOPA/amine bonds for adhesive bonding, which is intrinsically different from the DOPA melanin-based surface modification via metal coordination, hydrogen bonding, and π-stacking.54 SnTPyP is used as a model of the photosensitizer due to its large extinction coefficient and high redox potential for water oxidation (+1.1 V vs NHE at pH 7.0).28 SnTPyP can bond to the adhering Fmoc-L-Lys/DOPA fibers. The resulting Fmoc-LLys/DOPA/SnTPyP reserves the fibrous morphology, and some fibers stick together (Figure 3a,b), probably resulting from the enhanced surface hydrophobicity after binding of SnTPyP. This integration changes the color of SnTPyP solution from pink to yellow-brown (inset of Figure 4a). The corresponding Soret and Q-bands of SnTPyP are significantly

residue is observed (Figure 2c), which probably results from the DOPA melanin bound on the surface of Fmoc-L-Lys fibers. Based on electrospray ionization mass spectrometry (ESI-MS) analysis (Figure 2d), DOPA can react with Fmoc-L-Lys in alkaline solution to generate a Fmoc-L-Lys/DOPA melanin conjugation through Schiff base reaction between the quinone site in the DOPA melanin and amine group of Fmoc-L-Lys (Figure 2e; for detailed reaction mechanism, see Figure S5). Catechol functionality is mainly responsible for DOPA’s adhesive versatility. Along with the alkali-induced oxidation, the chemical equilibria of catechol/quinone shift to quinone. We first use a silver reduction test to determine whether hydroxyl groups remain in Fmoc-L-Lys/DOPA fibers. Fmoc-LLys/DOPA fibers can reduce silver ion to silver NPs due to the hydroxyl species (Figure 2f). Interestingly, metal oxide (e.g., Fe3O4 NPs) can be decorated on the surface of the fibers (Figure 2g). In addition, brown-blue color with an absorption peak around 550 nm occurs after addition of iron ion into the fiber solution (Figure 2h), which is ascribed to an iron− hydroxyl complex. These results indicate that Fmoc-L-Lys/ 12843

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Figure 3. (a) SEM and (b) TEM images of Fmoc-L-Lys/DOPA/SnTPyP fibers. The inset is the enlarged TEM image of single Fmoc-L-Lys/ DOPA/SnTPyP fiber. (c) TEM image of a Fmoc-L-Lys/DOPA/SnTPyP/Co3O4 hybrid fiber. (d) Enlarged TEM image of (c) showing discrete Co3O4 NPs on the surface of the hybrid fiber. (e) High-resolution TEM image of Co3O4 nanocrystal. (f) Sn 3d and (g) Co 2p XPS spectra of the hybrid fibers. (h) X-ray powder diffraction (XRD) spectra and (i) CD spectra of Fmoc-L-Lys fibers and the hybrid fibers.

Figure 4. (a) UV−vis absorption spectra of SnTPyP (predissolved in 1 M HCl) and Fmoc-L-Lys/DOPA/SnTPyP fibers in ultrapure water adjusted to pH 8.0 by 1 M NaOH; the concentration of SnTPyP is 10 μM. The inset is the photograph of SnTPyP (left) and Fmoc-L-Lys/ DOPA/SnTPyP solution (right). (b) CD spectra of SnTPyP and Fmoc-L-Lys/DOPA/SnTPyP fibers. (c) Stern−Volmer relation for SnTPyP mixed with DOPA melanin in solution and assembled on Fmoc-L-Lys/DOPA fibers at different concentrations of initial DOPA. (d) Electron paramagnetic resonance spectra of Fmoc-L-Lys/DOPA/SnTPyP fibers before and after illumination.

broadened and red-shifted compared to the those in the monomeric state (Figure 4a and Figure S7). The CD spectrum exhibits a strong signal in the visible range for the Fmco-L-Lys/ DOPA/SnTPyP: a negative Cotton effect (λmin) at 429 nm and a positive Cotton effect (λmax) at 448 nm (Figure 4b). These signals arise from exciton coupling of J-aggregates between well-ordered neighboring pigments.31 The Sn center prefers six-

coordinated geometry; it can bind with hydroxyl groups in the adhering fiber via coordination interaction. Furthermore, the intermolecular coordination between the Sn center and peripheral pyridyl groups may facilitate the fixation of SnTPyP at a certain dihedral angle. The adhering template (Figure S8) and metal center (Figure S9) are indispensable to form a wellordered porphyrin structure. The self-assembly of SnTPyP 12844

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Figure 5. (a) Time-course oxygen evolution for mixture of SnTPyP and Co3O4 NPs in solution (free system I); mixture of SnTPyP, DOPA melanin, and Co3O4 NPs in solution (free system II); and Fmoc-L-Lys/DOPA/SnTPyP/Co3O4 hybrid fibers (assembled system). The concentrations of initial DOPA, SnTPyP, and Co3O4 are fixed at 0.25 mM, 10 μM, and 0.13 mM, respectively. The dashed line is a linear fitting curve of the reaction profile for determination of initial reaction rate. (b) Reusability of Fmoc-L-Lys/DOPA/SnTPyP/Co3O4 hybrid fibers for oxygen evolution.

tuned by Fmco-L-Lys/DOPA fibers mimics the light-harvesting (LH) antenna complex in purple bacteria, where proteins organize bacteriochlorophyll into a highly symmetric wheel-like architecture.59 Furthermore, the fluorescence of SnTPyP on the Fmoc-LLys/DOPA fibers is dramatically suppressed (Figure 4c and Figure S10). Fmoc-L-Lys/DOPA has a Stern−Volmer quenching constant (KSV) of 38.6 mM−1, whereas native DOPA melanin has a KSV of 3.18 mM−1. This enhanced quenching is possibly because the strongly coupled porphyrin and the close proximity of neighboring species (i.e., porphyrins, quinone) facilitate exciton migration23 and electron transfer,15 respectively. In the electron paramagnetic resonance (EPR) spectrum, radical signals are observed (Figure 4d), predominantly arising from carbon-centered radical and semiquinone free radical in the DOPA melanin.60,61 After illumination, the signal intensity increases (Figure 4d), presumably due to generation of more semiquinone radicals (Figure S11). These results confirm that light-induced electron transfer occurs from SnTPyP to quinone species in the Fmoc-L-Lys/DOPA/SnTPyP fibers, working like a quinone-type reaction center. Co3O4 is used as a model photocatalyst for its easy availability and excellent catalytic performance on water oxidation.62,63 The Fmoc-L-Lys/DOPA fibers can be used as a template to bind Co3O4 NPs (Figure S12). Besides the adhesive property, where the hydroxyl groups of Fmoc-L-Lys/ DOPA have a strong binding affinity to the cobalt atom, the carboxyl group in DOPA can also bind the positively charged Co3O4 NPs (+20 mV) via electrostatic interaction. After simultaneous incubation of SnTPyP and Co3O4 NPs with the Fmoc-L-Lys/DOPA fibers, the resulting fibers are dispersedly decorated with ∼3 nm Co3O4 nanocrystals (Figure 3c,d). The high-resolution TEM electron lattice spacing shows dominance of the (311) plane of Co3O4 (Figure 3e), confirming that the crystal structure is spinel-type. Elements of tin (Figure 3f) and cobalt (Figure 3g) are both detected by X-ray photoelectron spectroscopy (XPS) analysis, suggesting that SnTPyP molecules and Co3O4 NPs are co-assembled on the fiber template, which facilitates their contact in close distance. In addition, the bound SnTPyP and Co3O4 NPs do not change the crystal form (Figure 3h) and secondary structure (Figure 3i) of Fmoc-L-Lys fibers because they are integrated on the surface of the template. The incorporated Co3O4 NPs also have negligible effect on the organization structure and light capture of SnTPyP molecules (Figure S13), probably due to their low

concentration, which is 0.13 mM, as determined by inductively coupled plasma mass spectrometry (ICP-MS) analysis. Oxygen evolution occurs on the Fmoc-L-Lys/DOPA/ SnTPyP/Co3O4 hybrid fibers under the illumination of visible light (λ ≥ 400 nm) using sodium persulfate (Na2S2O8) as an electron acceptor in borate buffer (10 mM, pH 8.0). After 6 h illumination, the oxygen accumulates up to 27.3 μmol, which is in contrast to only 2.7 and 4.1 μmol of oxygen generated with the free SnTPyP in the absence and presence of DOPA melanin, respectively (Figure 5a). The oxygen evolution rate for the SnTPyP on the hybrid fiber is 3.6 times higher than that of the free one, with a turnover frequency (TOF) of 5 × 10−3 and 1.4 × 10−3 s−1, respectively. The enhancement rate is mainly due to the charge separation between SnTPyP and the quinone species on the hybrid fiber (Figure 4c,d), as proven by the increase of TOF (2.1 × 10−3 s−1 vs 1.4 × 10−3 s−1) after a mixture of DOPA melanin with SnTPyP. The SnTPyP molecules are strongly coupled and in close distance with quinone species in the hybrid fiber, which facilitates delocalization of excitons and energy transfer to the reaction center, further enhancing charge separation. The generated charges can be more quickly transferred from the oxidized Sn(V)TPyP+ to the adjacent Co3O4 NPs. In addition, the hybrid fibers can ceaselessly produce oxygen for at least 6 h, while oxygen evolution is saturated with the free SnTPyP monomers after about 30 min (Figure 5a). The deactivation of organic pigments usually arises from oxidation of the free radical by a sacrificial electron acceptor.28 Excitation energy transfer can lead to exciton relaxation among the assembled SnTPyP molecules, which suppresses direct degradation and thus improves their stability. The Co3O4 NPs are anchored on the surface of the fibers, which avoids colloid aggregation and further precipitation. The availability of the surface cobalt atoms is a primary factor ruling water oxidation.63 Thus, the homogeneous distribution of the reactive centers also contributes to the operation stability. The hybrid fibers can be reused and show 66% efficiency for oxygen evolution compared to the first cycle (Figure 5b), with a cumulative turnover number of SnTPyP up to ∼115. This sustainable photocatalytic performance is based on the robust structure of the hybrid fibers (Figure S14) and enhanced photostability of assembled SnTPyP (Figure S15). 12845

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Preparation of Fmoc-L-Lys/DOPA/SnTPyP/Co3O4 Hybrid Fibers. Co3O4 NPs with a size of ∼3 nm were synthesized by hydrothermal treatment of cobalt(II) acetate tetrahydrate46 and preserved in methanol with a concentration of 4.8 mg mL−1. SnTPyP (0.8 mg) was dissolved in 1 mL of 1 M HCl. Ten microliters of SnTPyP and 10 μL of Co3O4 were added to 980 μL of the preprepared Fmoc-L-Lys/DOPA fibers. The mixture was adjusted to pH 8.0 with 1 M NaOH and incubated at room temperature for 48 h. The resulting hybrid fibers were collected by centrifugation at 4000 rpm for 10 min. For preparation of Fmoc-L-Lys/DOPA/SnTPyP fibers, the steps are the same except the addition of Co3O4 NPs. The amount of SnTPyP and Co3O4 incorporation was measured by the changed UV absorbance of SnTPyP and Co content in the supernatant, respectively, before and after incubation with Fmoc-L-Lys/DOPA fibers. Characterizations. SEM analysis was performed using a microscope (S-4800, Hitachi, Japan), equipped with EDX. TEM analysis was conducted on an electron microscope (JEM-2100F, JEOL, Japan), under a 200 kV accelerating voltage. AFM observation was carried out on FASTSCANBIO (Bruker) in tapping mode. FTIR was performed on a FTIR spectrometer (TENSOR 27, Bruker) with a resolution of 4 cm−1. UV−visible absorbance spectra were obtained with a spectrophotometer (UV-2600, Shimadzu). CD spectra were measured by a spectrograph (J-815, JASCO) at room temperature, with a cell length of 1.0 cm and a bandwidth of 1 nm. Fluorescence at room temperature was measured by a fluorescence spectrometer (Hitachi F4500). The excitation wavelength was 400 nm in each case, and excitation and emission slit widths were fixed at 10 nm. EPR signal was tested on a spectrometer (ESP-300, Bruker) equipped with a xenon lamp at room temperature. XPS measurements were performed using an ultrahigh vacuum electron spectrometer (ESCALab220i-XL, VG). The spectra were excited using a monochromated Al KR X-ray source (1486.7 eV) operated at 15 kV. XRD patterns were obtained with a diffractometer (Empyrean, PANalytical) under the following conditions: Cu Kα radiation, λ = 1.5406 Å. ESI-MS was recorded with a mass spectrometer (LCMS-2010, Shimadzu) under spray voltage of 1.8 kV. High-resolution ESI-MS was recorded by the mass spectrometer (Solarix 9.4T, Bruker) under a spray voltage of 3 kV. Negative ion mode electrospray ionization was used. The sample was diluted with methanol before being introduced into the spectrometer. The content of Co was determined by ICP-MS (NexION 300X, PerkinElmer). Samples were dissolved in concentrated nitric acid and diluted to suitable concentration. Standard curve was constructed using standard Co solution at a concentration of 1−50 μg L−1. Photocatalytic Oxygen Evolution. Photocatalytic oxygen evolution was carried out in a Pyrex top-irradiation reaction vessel connected to a glass-closed gas circulation system. In a typical photocatalytic experiment, Fmoc-L-Lys/DOPA/SnTPyP/Co3O4 hybrid fibers containing 10 μM of SnTPyP, 0.13 mM of Co3O4 NPs, and 5 mM of sodium persulfate were added to 100 mL of borate buffer solution (10 mM) with pH held at 8.0. The reactant solution was evacuated several times to remove air completely prior to irradiation under a 300 W Xe lamp with a cut-on filter (λcut‑on ≥ 400 nm). The intensity of the incident light was 108.2 mW cm−2 (ILT 950 spectroradiometer). The temperature of the reactant solution was maintained at room temperature by a flow of cooling water during the reaction. The evolved gases were analyzed by gas chromatography with a gas chromatograph (TRACE 1300, Thermo Fisher Scientific) equipped with a thermal conductive detector and a 5 Å molecular sieves column using argon as a carrier gas. For the reuse of the hybrid fibers, they were first recycled by centrifugation at 4000 rpm for 10 min and then mixed with freshly prepared borate buffer solution containing sodium persulfate (5 mM). Oxygen evolution of the resulting solution was measured according to the above procedure.

CONCLUSIONS In conclusion, we have developed a simple but robust strategy to fabricate a biomimetic cyanobacteria model possessing lightharvesting antenna and reaction center based on self-assembly/ organization of amphipathic amino acid, DOPA, metalloporphyrin, and metal oxide. The biomimetic model (hybrid fibers) with self-integration of multiple functionalities results in the superior catalytic activity and sustainability, reminiscent of natural cyanobacteria. The hybrid fibers have similar morphology,64 architectural principles (i.e., templated organization of porphyrins and cofactors), and functional mechanism (i.e., energy transfer from antenna to quinone-type reaction center) to that of cyanobacteria. The coupling of antenna, quinone acceptor, and catalyst facilitates exciton delocalization and charge separation. Therefore, they can be regarded as a biomimetic cyanobacteria model with simplified PSII. Interestingly, that architecture is similar to the LH1 of purple bacteria, where porphyrins form a large ring that encloses the quinone reaction centers. During the evolution from anaerobic to oxygenic photosynthesis, an inorganic core to drive a fourelectron oxidation of water to oxygen is indispensable.65 Therefore, the biomimetic cyanobacteria may give a plausible procyanobacteria model that bridges the evolutionary scenario between purple bacteria and cyanobacteria. In addition, this study provides a feasible solution to design a platform for biomimetic utilization of solar energy in water oxidation and a good case for the fabrication of bioinspired materials via simplification of biological prototypes to indispensable building blocks and reintegration according to their inherent architectural principles by using of covalent and noncovalent organization. METHODS Materials. Fmoc-L-Lys-OH hydrochloride was purchased from Energy Chemical. L-DOPA was purchased from Acros Organics. HFIP, AgNO3, FeCl3, and Fe3O4 NPs, and cobalt(II) acetate tetrahydrate were purchased from Sigma-Aldrich. SnTPyP and meso-tetra(4-Nmethylpyridyl)porphyrin (TMPyP) were purchased from Frontier Scientific. All products were used as obtained. Preparation of Fmoc-L-Lys/DOPA Fibers. Fmoc-L-Lys (5 mg) was dissolved in 50 μL of 1 M HCl and diluted with 950 μL of ultrapure water. The above solution was tuned to pH 4.0 using 1 M NaOH. The resulting white precipitate was separated by centrifugation at 4000 rpm for 10 min. A DOPA solution of 2.0 mg mL−1 was prepared by dissolving DOPA in pH 8.0 Tris-HCl (10 mM). Serial volume of DOPA solution (1, 2, 10, 25, 50, 250, and 500 μL) was added to the precipitate. After being supplemented with proper ultrapure water, the finial volume reached 1 mL, with DOPA concentrations of 2 × 10−3, 4 × 10−3, 2 × 10−2, 5 × 10−2, 1 × 10−1, 5 × 10−1, and 1 mg mL−1. The mixtures were adjusted to pH 8.0 with 1 M NaOH and allowed to stand at room temperature for 48 h. The final precipitate was centrifuged at 4000 rpm for 10 min and resuspended in ultrapure water. The amount of DOPA incorporation was measured by the decreased UV absorbance of DOPA melanin (λ = 280 nm) in the supernatant compared to that of the control DOPA melanin solution prepared with the same operations as DOPA except for the incubation with Fmoc-L-Lys fibers. Reduction and Adhesion Test of Fmoc-L-Lys/DOPA Fibers. AgNO3 (3.4 mg), FeCl3 (1.6 mg), and Fe3O4 NPs (2.3 mg) were dissolved or dispersed in 1 mL of ultrapure water, and 100 μL of the solution was added to 900 μL of the preprepared Fmoc-L-Lys/DOPA fibers with initial DOPA of 0.1 mg mL−1. The mixture was incubated at room temperature for 24 h (for AgNO3) or 48 h (for FeCl3 and Fe3O4) and then analyzed by EDX-SEM, AFM, and UV−vis spectroscopy.

ASSOCIATED CONTENT S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acsnano.7b08215. 12846

DOI: 10.1021/acsnano.7b08215 ACS Nano 2017, 11, 12840−12848

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ACS Nano

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Molecular structures of building blocks; structural characterization (SEM and CD) of Fmoc-L-Lys fibers and Fmoc-L-Lys/DOPA fibers; reaction mechanism for DOPA; determination of the amount of DOPA melanin and SnTPyP in Fmoc-L-Lys/DOPA fibers and Fmoc-LLys/DOPA/SnTPyP fibers, respectively; assembled mechanism for SnTPyP; photochemical characterization (fluorescence and EPR) of Fmoc-L-Lys/DOPA/SnTPyP fibers; (photo)stability of the hybrid fibers (PDF)

AUTHOR INFORMATION Corresponding Author

*E-mail: [email protected]. ORCID

Kai Liu: 0000-0002-8233-2310 Qianli Zou: 0000-0003-0464-4156 Xuehai Yan: 0000-0002-0890-0340 Notes

The authors declare no competing financial interest.

ACKNOWLEDGMENTS We acknowledge financial support from the National Natural Science Foundation of China (21522307, 21473208, 91434103, and 21773248), the Talent Fund of the Recruitment Program of Global Youth Experts, and the Key Research Program of the Frontier Sciences of the Chinese Academy of Sciences (QYZDB-SSW-JSC034). REFERENCES (1) Nisbet, E. G.; Sleep, N. H. The Habitat and Nature of Early Life. Nature 2001, 409, 1083−1091. (2) Schirrmeister, B. E.; de Vos, J. M.; Antonelli, A.; Bagheri, H. C. Evolution of Multicellularity Coincided with Increased Diversification of Cyanobacteria and the Great Oxidation Event. Proc. Natl. Acad. Sci. U. S. A. 2013, 110, 1791−1796. (3) Dau, H.; Zaharieva, I. Principles, Efficiency, and Blueprint Character of Solar-energy Conversion in Photosynthetic Water Oxidation. Acc. Chem. Res. 2009, 42, 1861−1870. (4) Umena, Y.; Kawakami, K.; Shen, J. R.; Kamiya, N. Crystal Structure of Oxygen-Evolving Photosystem II at a Resolution of 1.9 Å. Nature 2011, 473, 55−60. (5) Guskov, A.; Kern, J.; Gabdulkhakov, A.; Broser, M.; Zouni, A.; Saenger, W. Cyanobacterial Photosystem II at 2.9-Å Resolution and the Role of Quinones, Lipids, Channels and Chloride. Nat. Struct. Mol. Biol. 2009, 16, 334−342. (6) Ferreira, K. N.; Iverson, T. M.; Maghlaoui, K.; Barber, J.; Iwata, S. Architecture of the Photosynthetic Oxygen-Evolving Center. Science 2004, 303, 1831−1838. (7) Croce, R.; Van Amerongen, H. Natural Strategies for Photosynthetic Light Harvesting. Nat. Chem. Biol. 2014, 10, 492−501. (8) Herrero, C.; Lassalle-Kaiser, B.; Leibl, W.; Rutherford, A. W.; Aukauloo, A. Artificial Systems Related to Light Driven Electron Transfer Processes in PSII. Coord. Chem. Rev. 2008, 252, 456−468. (9) Barber, J. Photosynthetic Energy Conversion: Natural and Artificial. Chem. Soc. Rev. 2009, 38, 185−196. (10) Blankenship, R. E. Early Evolution of Photosynthesis. Plant Physiol. 2010, 154, 434−438. (11) Wydrzynski, T.; Hillier, W.; Conlan, B. Engineering Model Proteins for Photosystem II Function. Photosynth. Res. 2007, 94, 225− 233. (12) Maeda, K.; Domen, K. Development of Novel Photocatalyst and Cocatalyst Materials for Water Splitting under Visible Light. Bull. Chem. Soc. Jpn. 2016, 89, 627−648. 12847

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