Artificial Thylakoid for the Coordinated Photo-Enzymatic Reduction of

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Artificial Thylakoid for the Coordinated PhotoEnzymatic Reduction of Carbon Dioxide Shaohua Zhang, Jiafu Shi, Yiying Sun, Yizhou Wu, Yishan Zhang, Ziyi Cai, Yixuan Chen, Chun You, Pingping Han, and Zhongyi Jiang ACS Catal., Just Accepted Manuscript • Publication Date (Web): 26 Mar 2019 Downloaded from http://pubs.acs.org on March 26, 2019

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ACS Catalysis

Artificial Thylakoid for the Coordinated Photo-Enzymatic Reduction of Carbon Dioxide Shaohua Zhang,1,3 Jiafu Shi,2* Yiying Sun,1,3 Yizhou Wu,1,3 Yishan Zhang,1,3 Ziyi Cai,1,3 Yixuan Chen,1 Chun You,4 Pingping Han,4 Zhongyi Jiang1,3* 1Key

Laboratory for Green Chemical Technology of Ministry of Education, School of

Chemical Engineering and Technology, Tianjin University, Tianjin 300072, China. 2School

of Environmental Science and Engineering, Tianjin University, Tianjin

300072, China. 3Collaborative

Innovation Center of Chemical Science and Engineering (Tianjin),

Tianjin 300072, China. 4Tianjin

Institute of Industrial Biotechnology, Chinese Academy of Sciences, Tianjin

300308, China.

1

ACS Paragon Plus Environment

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Abstract: Artificial photosynthesis holds promise in producing solar fuels and chemicals. Although encouraging achievements have been made in the development of catalysts for reaction/process modules in artificial photosynthesis, constructing a highly compatible complex reaction system remains a distant prospect. Herein, an artificial thylakoid is proposed and constructed by decorating the inner wall of protamine-titania (PTi) microcapsules with cadmium sulfide quantum dots (CdS QDs) for photobiocoupled reduction of carbon dioxide (CO2) via single enzyme (formate dehydrogenase) and multienzymes (formate/formaldehyde/alcohol dehydrogenases). The size-selective capsule wall compartmentalizes photocatalytic oxidation and biocatalytic reduction, creating well-directed reaction sequences and protecting enzymes from deactivation. The favorable electronic coupling and band structure between CdS and PTi separate holes and electrons to afford NADH regeneration rate of 4226±121 μmol g-1 hour-1 and optimized yield of 93.03±3.84%. The photobiocoupled system achieves formate and methanol outputs of 1500 μM hour-1 and 99 μM hour-1 with single enzyme and multienzymes, respectively. Our study may exploit a method for the construction of complex artificial catalytic systems with multiple reactions. Keywords:

Artificial

thylakoid,

Photobiocatalysis,

Coordination, CO2 conversion

2


Compartmentalization,

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1. INTRODUCTION Natural photosynthesis presents an exquisite model system for the large-scale production of renewable energy (biomass) through the solar-driven reduction of naturally abundant carbon dioxide (CO2), which fuels the life on earth in a highly sustainable way. The “success” of natural photosynthesis arises from the following aspects: 1) the efficient catalysts, primarily chlorophyll for light harvesting, Mn4O5Ca for water splitting and oxygen evolution, ferredoxin-NADP+ reductase for NADPH reduction and RuBisCO for CO2 fixation, and 2) the delicate system implementing the coordinated optimization of different catalytic processes.1 Inspired by natural photosynthesis, a great deal of research efforts on artificial photosynthesis have been dedicated to catalyst development, which is responsible for the high efficiency of an individual reaction/process, and to system construction, which is responsible for the overall efficiency and sustainability of all reactions/processes.2-6 On one hand, some typical heterogeneous/homogeneous catalysts, including inorganic semiconductor photocatalysts,2, catalysts,8,

9

7

Ru/Fe molecular

metal oxide nanocatalysts,10 metal-organic frameworks,11 covalent

organic frameworks12 have displayed superior performance in light harvesting, water splitting and CO2 conversion. On the other hand, the establishment of an efficient system to coordinate the different reactions/processes remains much less explored.4, 6, 13

Currently, three representative artificial photosynthesis systems based on

photocatalysis, photoelectrocatalysis and photobiocoupled catalysis have been constructed for the continuous synthesis of fuels/chemicals.4,

5, 14

Because of the

higher similarity to natural prototypes, photobiocoupled artificial photosynthesis systems that integrate the light-harvesting capability of semiconductor photocatalysts and the CO2-processing capability of biocatalysts would exhibit immense potential in 3


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the product-specific conversion of CO2 with a low carbon footprint and low energy input.15-25 The photocatalysts absorb solar energy to generate reducing equivalents (electrons, NADH and H2), and the biocatalysts utilize the reducing equivalents to convert CO2 into fuels/chemicals with high specificity, stereoselectivity and regioselectivity under ambient conditions. Nonetheless, the low compatibility between photocatalysis and biocatalysis in photobiocoupled systems severely hinders their application efficiency.15, 25-27 Achieving the synergy between photocatalysis and biocatalysis requires 1) the construction of an oriented “highway” to convey the reducing equivalents from photocatalyst to biocatalyst and 2) the creation of a compatible interface between the photocatalyst and biocatalyst.5, 28, 29 To serve such requirements, photoelectrochemical cells (PECs) have been exploited as a feasible strategy to optimize photocatalysis and biocatalysis coordinately.15,

16, 23, 30, 31

In brief, the conducting wire ensures the

oriented transfer of reducing equivalents (primarily electrons) from photoelectrodes to biocatalyst, whereas the flat-sheet semipermeable membrane compartmentalizes photocatalytic oxidation and biocatalytic CO2 reduction and thereby keeps the biocatalyst alive. However, facile and controllable methods for the coordinated optimization of photocatalysis and biocatalysis deserve much intensive exploration. The chloroplast, as the energy conversion center of natural photosynthesis, employs thylakoids to couple photoreaction and bioreaction, which can convert 100-120 Gts of carbon into biomass per year by harvesting 130 terawatts of solar energy (Figure 1).32, 33

The thylakoid compartmentalizes the water oxidation reaction and enzymatic

reaction in a capsular structure, protecting the enzymes from deactivation by photogenerated holes and reactive oxygen species (ROS).34 The downhill electron transfer chain in the thylakoid membrane affords an efficient electron supply and 4


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ACS Catalysis

regenerates reduced β-nicotinamide adenine dinucleotide phosphate (NADPH) to drive the Calvin cycle.35 Inspired by the structure and function of the thylakoid, we designed and prepared an artificial thylakoid by decorating the inner wall of protamine-titania (PTi) microcapsules with CdS QDs to construct a photobiocoupled artificial photosynthesis system. Single enzyme of formate dehydrogenase and multienzymes of formate dehydrogenase, formaldehyde dehydrogenase and alcohol dehydrogenase, which can convert CO2 into formate and methanol, respectively, were adopted as the model biocatalyst to demonstrate the coupling of photocatalysis and biocatalysis.36 The size-selective capsule wall compartmentalized the photocatalytic oxidation and enzymatic CO2 reduction, protecting the enzyme from deactivation by photogenerated holes and ROS. The heterostructure of CdS QDs and amorphous titania facilitated the transfer of the photogenerated electrons across the capsule wall, enabling the highly efficient regeneration of β-nicotinamide adenine dinucleotide (NADH) for subsequent enzymatic CO2 reduction. The photobiocoupled system achieved formate and methanol outputs of 1500 μM hour-1 and 99 μM hour-1 with single enzyme and multienzymes, respectively. Moreover, under light-dark cycles, CO2 was converted to formate with a quantum yield of 0.66±0.13%, comparable to the year-long average determined for natural green plants (~0.2 to 1.6%).17,

18

The

applicability of this system was further demonstrated by coupling CdS/PTi microcapsules with enzyme that do not rely on NADH. Hopefully, our study may offer some inspiration to the rational design and construction of complex artificial photosynthesis systems.

5


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2. RESULTS AND DISCUSSION

Figure 1. Similarity between natural photosynthesis and artificial thylakoid-enzyme coupled system. (a) PS II and PS I absorb visible light to generate electrons and holes. The electrons are transferred to the stromal side of the thylakoid membrane through the electron transfer chain and then transduced into biomass through reduced β-nicotinamide adenine dinucleotide phosphate (NADPH) in the Calvin cycle. The holes left on the luminal side of the thylakoid membrane oxidize water into oxygen and protons. (b) CdS QDs on the capsule wall absorb visible light to generate electrons and holes. The electrons are transferred to the outer surface of the capsule wall through the heterostructure of CdS and amorphous titania, then transduced to formic acid through reduced β-nicotinamide adenine dinucleotide (NADH) by formate dehydrogenase from Candida boidinii (CbFDH). The holes left on the inner surface of the capsule wall oxidize triethanolamine (TEOA). Note: [M] is [Cp*Rh(bpy)H2O]2+ (Cp* = pentamethylcyclopentadienyl, bpy = 2,2-bipyridyl).37

6


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2.1. Preparation and Characterizations of Artificial Thylakoid.

Figure 2. (a) Schematic preparation process of CdS/PTi microcapsules. (b) SEM image, (c, d) TEM images, (e) HAADF-STEM image and (f-i) EDS elemental mappings of CdS/PTi microcapsules. Scale bars, 3 μm (b); 500 nm (c); 2 nm (d); 20 nm (e); 5 μm (f-i). (j) UV-Vis diffuse reflectance spectra of PTi and CdS/PTi microcapsules. (k) The pore size distribution of CdS/PTi microcapsules determined by N2 adsorption-desorption isotherm curve. Inset was the size of CbFDH measured by Raswin molecular graphics. (l) The diffusion rate of TEOA through HPAN-PTi membrane. HPAN was hydrolyzed polyacrylonitrile ultrafiltration membranes.

To compartmentalize the photocatalytic oxidation and enzymatic CO2 reduction, we prepared an artificial thylakoid by decorating the inner wall of protamine-titania (PTi) microcapsules with CdS QDs (CdS/PTi microcapsules) (Figure 1). As shown in Figure 2a, polystyrene sulfonate doped CaCO3 microspheres (PSS-CaCO3 microspheres) prepared via co-precipitation were chosen as the template for the 7


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deposition of CdS QDs by alternatively immersed into 10 mM CdSO4 and 10 mM Na2S solutions.38 The negatively charged sulfate group on the surface of PSS-CaCO3 microspheres could absorb Cd2+ through electrostatic interaction, and then induce the homogenous deposition of CdS QDs when contacting with S2- (Figure S1a and b). Notably, when silica microspheres were used as the substrate for CdS deposition, merely large CdS aggregates were observed (Figure S1c).39 Then, protamine-titania (PTi) capsule wall was deposited on CdS QDs decorated PSS-CaCO3 microspheres through biomimetic mineralization method developed by our group.38 After the removal of CaCO3 microspheres through EDTA treatment, CdS/PTi microcapsules were formed. The complete removal of CaCO3 microspheres could be verified by the disappearance of Ca element in EDS spectrum of CdS/PTi microcapsules (Figure S2). To achieve the compartmentalization of photocatalytic oxidation and CO2 reduction, CdS/PTi microcapsules should meet the following requirements: (i) the intact capsular structure, (ii) CdS QDs deposited on the inner surface of PTi capsule wall, and (iii) appropriate pore size on PTi capsule wall to prevent the penetration of CbFDH, while allow the penetration of TEOA. First, the structure of CdS/PTi microcapsules was characterized by scanning electron microscopy (SEM) and transmission electron microscopy (TEM). As shown in Figure 2b and 2c, CdS/PTi microcapsules exhibited intact hollow structure with a diameter of ~3 μm and a wall thickness of 181.3±10.9 nm. The intact structure of the capsule wall was insured by excellent surface-coating capability of biomimetic mineralization on PSS-CaCO3 microspheres.38 Then, the position and distribution of CdS QDs were characterized. High-resolution TEM (HRTEM) demonstrated the successful deposition of CdS QDs on the inner surface of PTi capsule wall (Figure S3). The as-deposited CdS QDs exhibited a lattice spacing 8


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ACS Catalysis

of 0.206 nm, corresponding to the (220) plane of the cubic phase of CdS (Figure 2d). This was consistent with the XRD results that CdS QDs was cubic phase and PTi was amorphous (Figure S4). High-angle annular dark-field scanning transmission electron microscopy (HAADF-STEM) and energy-dispersive spectrometry (EDS) elemental mappings revealed nanoparticles (diameter: 3.68±0.68 nm) composed of cadmium and sulfur homogeneously distributed on the inner surface of PTi capsule wall (Figure 2e to 2i). In general, the CdS nanoparticles held a much higher surface energy than bulk CdS (2.5 vs 0.75 J m-2) and therefore required organic capping ligands to inhibit their aggregation.40 These ligands might build a barrier to decelerate the interfacial electron transfer. In our study, the synthesis of CdS QDs was a ligand-free process.41 Sequential mineralization enabled the close contact between CdS QDs and PTi capsule wall, which kept the CdS QDs separated and homogeneously distributed. Such homogeneous distribution of CdS QDs on CdS/PTi microcapsules was quite beneficial for light harvesting. As shown in Figure 2j, the absorption edge of PTi microcapsules extended from ~370 to ~537 nm after the deposition of CdS QDs. The bandgaps of CdS/PTi and PTi microcapsules were determined to be 2.41±0.01 and 3.61±0.02 eV, respectively (Figure S4). The large bandgap and antireflective property of PTi capsule wall allowed the transmission of visible light (＞400 nm) to CdS QDs.42 To compartmentalize photocatalytic oxidation and enzymatic reduction, PTi capsule wall should prevent the penetration of CbFDH but still allow the penetration of TEOA. As shown in Figure 2k, the pore diameter on PTi capsule wall was determined to be ~3.9 nm from the N2 adsorption-desorption isotherm curve. The pore diameter was smaller than the size of CbFDH determined by Raswin molecular graphics (8.71×8.23×4.73 nm3). Obviously, CbFDH could not penetrate PTi capsule 9


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wall into the capsule lumen. This was consistent with our previous work, where the enzyme confined into the capsule lumen could not penetrate PTi capsule wall to the exterior solution.38 Moreover, the pore diameter on PTi capsule wall was at least 6-fold the size of TEOA determined by Chemdraw (Figure S5). This suggested that TEOA could rapidly diffuse into the capsule lumen once consumed. To further demonstrate the penetration and recharging of TEOA inside CdS/PTi microcapsules, we designed a home-made diffusion device (Figure S6a). PTi coated hydrolyzed polyacrylonitrile ultrafiltration membrane (HPAN) was used as the membrane in a diffusion device (Figure S6b).43 The diffusion rate of TEOA through the membrane was accessed by measuring TEOA concentration in PBS buffer. As shown in Figure 2l, TEOA could penetrate HPAN membrane with a rate of 40.04 μM min-1. After depositing one layer of PTi on HPAN (HPAN-PTi1), the diffusion rate was slightly lowered for ~1.3 times to 29.96 μM min-1. This demonstrated that PTi exerted minor diffusion resistance to TEOA molecules. Moreover, with the increase in the thickness of deposition layer of PTi, the diffusion rate of TEOA was only slightly decreased, confirming that TEOA could rapidly passed through the PTi coating. These results demonstrated that CdS/PTi microcapsules could successfully compartmentalize photocatalytic

oxidation

and

enzymatic

10


CO2

reduction.

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2.2. Oriented Transfer of Electrons in Artificial Thylakoid.

Figure 3. (a) Photocatalytic regeneration of NADH by CdS/PTi, CdS/PSi, PTi and PSi microcapsules and CdS nanoparticles and (b) the corresponding NADH regeneration rate. NTD means “not detected”. NADH regeneration rate was calculated according to the total mass of the photocatalyst at 10 min. (c) Time-resolved transient PL decay spectra of CdS/PTi and CdS/PSi microcapsules. (d) Photocurrents of CdS/PTi and CdS/PSi microcapsule electrodes measured in aqueous solution containing 0.2 M Na2S and 0.04 M Na2SO3 under AM 1.5 G illumination. (e) XPS valence band (VB) spectra of PTi and CdS/PTi microcapsules. (f) Schematic of the electron transfer process and the photocatalytic regeneration of NADH based on the heterostructured capsule wall. Photocatalytic regeneration of NADH with (g) different light intensities and loadings of CdS/PTi microcapsules, (h) different pH values and TEOA concentrations, and (i) different sacrificial reagents. Reaction conditions for (a): [photocatalyst] = 0.4 g l-1 (CdS) or 1 g l-1 (microcapsules), [NAD+] = 1 mM, [M] = 0.25 mM, [TEOA] = 400 mM, PBS buffer (pH 7.0, 100 mM), RT, visible light illumination (λ = 405±5 nm). (g) [light intensity] = 10-200 mW cm-2, [CdS/PTi] = 1-4 g l-1. (h) pH = 6.0-9.0 (PBS buffer, 100 mM), [TEOA] = 400-1600 mM. (i) Sacrificial reagents: [TEOA] = 400 mM, [EDTA] = 300 mM, [AA] = 400 mM or [PBS] = 100 mM. Error bars represent the standard deviation based on triplicate experiments (n=3). 11


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To demonstrate the oriented transfer of electrons, CdS/PTi microcapsules were exploited for photocatalytic NADH regeneration in PBS buffer containing 400 mM TEOA (pH = 7.0) under visible light illumination (λ = 405±5 nm, LED). [Cp*Rh(bpy)H2O]2+ (Cp* = pentamethylcyclopentadienyl, bpy = 2,2-bipyridyl) was used as the electron mediator to selectively transfer electrons from the surface of CdS/PTi microcapsules to nicotinamide adenine dinucleotide (NAD)+ and thereby regenerate enzymatically active NADH (Figure S7).37,

44

[Cp*Rh(bpy)H2O]2+ was

denoted as [M]. Amazingly, the coupling of PTi and CdS QDs resulted in markedly enhanced NADH regeneration activity. As shown in Figure 3a, PTi microcapsules could not regenerate NADH under visible light illumination due to its large bandgap (3.61 eV). The single-cycle deposition of CdS on PTi microcapsules resulted in a high NADH regeneration rate of 2932±337 μmol g-1 hour-1 (Figure S8 and S9, Table S1). The double-cycle deposition of CdS further enhanced the NADH regeneration rate to 4226±121 μmol g-1 hour-1, which was nearly 190% higher than that of CdS nanoparticles with a diameter of 3.57±0.86 nm (Figure S10). This high NADH regeneration activity might be arisen from the homogeneous distribution of CdS QDs and the strong electronic coupling between CdS and PTi. To demonstrate the electronic interaction between CdS and PTi, silica, a commonly used nonconductive support material, was used to prepare the microcapsules. In brief, CdS QD-decorated protamine-silica (CdS/PSi) microcapsules were prepared through the sequential mineralization of CdS and PSi. SEM, HRTEM, EDS elemental mappings and XRD demonstrated the hollow structure of CdS/PSi microcapsules and the homogeneous distribution of cubic phase CdS QDs on the inner surface of PSi capsule wall (Figure S11). The diameter of CdS QDs, the content of CdS and the 12


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ACS Catalysis

bandgap of CdS/PSi microcapsules were similar to those of CdS/PTi microcapsules (Figure S12).

CdS/PSi microcapsules exhibited a lower NADH regeneration rate

than CdS/PTi microcapsules (3594±353 vs 4226±121 μmol g-1 hour-1). The higher activity of CdS/PTi microcapsules should be arisen from the strong electronic coupling between CdS and PTi, which facilitates rapid interfacial charge transfer. A ~0.2 eV shift of the Cd3d and S2p bands in the XPS spectra was observed after the deposition of CdS QDs on the PTi capsule wall, verifying the strong electronic interaction between CdS and PTi (Figure S13). When we further increased the number of deposition cycles of CdS QDs to three or four, the NADH regeneration rate of the CdS/PTi microcapsules decreased slightly. This result should be attributed to the increased size and aggregation of CdS QDs (Figure S9), which lowered the charge transfer efficiency. However, even CdS(4)/PTi microcapsules still showed much higher NADH regeneration activity than CdS nanoparticles (3844±407 vs 2234±245 μmol g-1 hour-1). Given the above discussion, the markedly enhanced activity of CdS/PTi microcapsules should be owing to efficient charge separation because of the electron transfer from CdS to PTi. To demonstrate the charge transfer behavior, CdS/PTi microcapsules

were

characterized

by

photoluminescence

(PL)

and

photoelectrochemical experiments. As shown in Figure S14, PTi quenched the PL emission peak more efficiently than PSi, suggesting the greatly suppressed charge recombination and enhanced interfacial charge transfer in CdS/PTi microcapsules. From the time-resolved PL decay spectra, CdS/PTi exhibited a shorter PL lifetime than CdS/PSi (τ1: 0.65 vs 1.25 ns, τ2: 16.11 vs 23.60 ns), indicating better charge transfer and separation in the CdS/PTi heterojunction (Figure 3c). The electron transfer rate constant (kET) was calculated to be 2.11 × 107 s-1 by assuming that the 13


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electron transfer process was solely responsible for the enhanced emission decay (Section S1).45 Then, the charge transfer efficiency was evaluated by transient photocurrent response and electrochemical impedance spectroscopy (EIS). Figure 3d showed that all the dark current densities were negligible at -0.37 V (versus Ag/AgCl reference electrode). Under light illumination (AM 1.5), CdS/PTi microcapsules exhibited the highest photocurrent density of 11.3 μA cm−2, which was 2.3 times higher than that of CdS/PSi microcapsules, indicating rapid electron transfer from CdS to the PTi capsule wall. Moreover, CdS/PTi microcapsules exhibited a much smaller semicircle than CdS/PSi microcapsules in 100 mM Na2SO4 electrolyte solution, indicating a lower interfacial charge transfer resistance between CdS and PTi than between CdS and PSi (Figure S15). To further elucidate the charge transfer mechanism, the band structure of CdS/PTi microcapsules was depicted based on XPS VB spectra and tauc plots. As shown in Figure 3e, the VB edges of the CdS/PTi and PTi microcapsules were determined to be 1.18 and 2.94 eV, respectively. The conduction band (CB) edges of CdS/PTi and PTi microcapsules were calculated to be -1.23 and -0.67 eV according to the bandgap (Figure S4). The CB offset of 0.56 eV allowed the efficient interfacial electron transfer from CdS QDs to PTi capsule wall (Figure 3f). Currently, amorphous titania has been widely used as a conductive layer to protect the electrode.42 Herein, the PTi capsule wall prepared by biomimetic mineralization was composed of amorphous titania, which would transfer the electrons through the CB. Therefore, under visible light illumination, the photogenerated electrons on CdS QDs were first delivered to PTi capsule wall and then captured by [M] to regenerate NADH (Figure 3f). Moreover, PTi capsule wall was used to immobilize [M], enabling its recycling (Figure S16). The photocatalytic performance of CdS/PTi microcapsules was then optimized by 14


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altering the light intensity, concentration of CdS/PTi microcapsules, pH, concentration of TEOA and species of sacrificial reagents. With increasing the light intensity, the NADH regeneration rate increased (Figure 3g). At a light intensity of 10 mW cm-2, a quantum yield of 15.0±6.1% was obtained. The high quantum yield for CdS/PTi microcapsules was notable, given that a previous similar system exhibited a quantum yield of 5.8%.46 This result should be arisen from the much better electron transfer in CdS/PTi microcapsules. With four times the normal concentration of CdS/PTi microcapsules, a quantum yield of 37.1±4.2% was observed. At higher concentrations of CdS/PTi microcapsules, the photon flux for each microcapsule decreased, which could inhibit the recombination of photogenerated electrons and holes by decreasing their density. Moreover, an increase in CdS/PTi microcapsules would increase the opportunity for contacting with the mediator. These factors would synergistically increase the quantum yield. As the pH increased from 6.0 to 9.0, the NADH regeneration rate increased (Figure 3h). At pH = 7.5, the highest NADH regeneration yield was 82.1±4.1%, which is likely due to the pH-dependent activity of [M]. A higher concentration of protons would facilitate the oxidation of [M] by protons, which would then tend to produce hydrogen and inhibit the regeneration of NADH. In contrast, a higher concentration of OH- would deprotonate the electron mediator and inhibit the regeneration of NADH. According to the literature,47 [M] exhibited the highest activity at pH 7.5, which is consistent with our observations. With the use of four times the concentration of TEOA, the NADH regeneration yield increased from 70.4±2.0% to 87.1±4.4%, which should be attributable to the higher capability in the removal of holes. Furthermore, three common sacrificial reagents, TEOA, EDTA, and ascorbic acid (AA), were used for NADH regeneration. As shown in Figure 3i, AA acquired higher NADH regeneration 15


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yield than TEOA and EDTA. This should be arisen from the lower redox potential of AA (0.058 V vs NHE at pH 7.0) than TEOA and EDTA (1.07 and 1.17 V vs NHE at pH 7.0), which then caused the more efficient donation of electrons to the VB of CdS.48 Interestingly, EDTA held a similar redox potential with TEOA, however, the NADH regeneration yield enabled by EDTA was much lower than TEOA. This might be explained by different oxidation mechanism and reaction kinetics of the sacrificial reagents. To our knowledge, CdS/PTi microcapsules presented one of the highest NADH regeneration rate reported to date

under optimized conditions (Table

S2).49-51 To demonstrate the feasibility of CdS/PTi microcapsules as artificial thylakoid, water

was

also

used

as

the

sacrificial

reagent

to

regenerate

NADH.

[Ru(tpy)(bpy-NH2)Cl]+ (RuN), a water oxidation catalyst, was immobilized on CdS/PTi microcapsules (CdS/RuN/PTi, Figure S17).52 After 60 min illumination, 18.5% of NAD+ was regenerated, validating the potential of CdS/PTi microcapsules as an artificial thylakoid. The quantum yield for NADH regeneration was calculated to be 1.71±0.17% based on the initial NADH regeneration rate (first 2 minutes). The generated oxygen was detected by a fluorescence based O2 sensor (Neofox, FOSFOR-R probe, Ocean Optics) (Figure S18). The amount of oxygen increased gradually and reached 0.102 μmol after one hour illumination. No oxygen was detected for the reaction solution incubated in darkness (black curve). This demonstrated the successful coupling between water oxidation and NADH regeneration. The ratio between NADH and O2 was calculated to be 3.63:1, which was larger than the theoretical value of 2:1. This might be arisen from the partial reduction of the evolved O2 by photogenerated electrons. H2O2, a common O2 reduction product, was detected in the reaction solution after 30 min illumination 16


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ACS Catalysis

under anaerobic condition (Figure S18), validating the reduction of O2 by photogenerated electrons. To further demonstrate the kinetic coupling of water oxidation with NADH regeneration, time-resolved transient PL decay spectra of CdS/RuN/PTi and CdS/PTi microcapsules were characterized. As shown in Figure S18, the water oxidation catalyst-RuN quenched the luminescence of CdS/PTi and the hole transfer rate constant was calculated to be 1.82×106 s-1. This should be arisen from the integration of CdS quantum dots and RuN on the capsule wall, which facilitated the hole transfer from CdS to RuN. Besides, the electrons could also be transferred from CdS to PTi capsule wall. The spatial charge separation could then promote the accumulation of holes on RuN. All above evidences demonstrated the feasibility of CdS/PTi microcapsules as an artificial thylakoid. 2.3. Compatibility between Artificial Thylakoid and Formate Dehydrogenase.

Figure 4. (a) Schematic of the interaction between CdS/PTi, PTi/CdS microcapsules and CbFDH. (b) Relative activity, (c) circular dichroism (CD) spectra and (d) relative secondary structure content of CbFDH after incubation in PBS buffer containing PTi, CdS/PTi, and PTi/CdS microcapsules under visible light illumination for one hour. (e) Relative activity of CbFDH after incubation in anaerobic PBS buffer containing CdS/PTi and PTi/CdS microcapsules under visible light illumination for one hour. Error bars represent the standard deviation based on duplicate experiments (n = 2). 17


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Page 18 of 41

Conditions for (b, e): [CbFDH] = 1 g l-1, [PTi or CdS/PTi or PTi/CdS] = 0 or 1 g l-1, (anaerobic) PBS buffer (pH = 7.0, 100 mM), [TEOA] = 0 or 400 mM, RT. The sample was incubated in darkness or under visible light illumination (λ = 405±5 nm).

In addition to exhibiting high efficiency in NADH regeneration, the photocatalyst should be compatible with the biocatalyst for the construction of a high-performance photobiocoupled artificial photosynthesis system. First, the poisonous effects of different reagents/semiconductors on the biocatalyst in darkness, including TEOA, [M] and CdS/PTi microcapsules, were evaluated. CbFDH retained its original activity after incubation in darkness for one hour, suggesting that the reagents/semiconductors used for NADH regeneration were compatible with CbFDH in darkness (Figure S19). However, under light illumination, the photogenerated holes generated on semiconductors could easily deactivate enzymes, making the development of biocompatible photocatalysts highly challenging.26,

27

Herein, size-selective PTi

capsule wall successfully confined photogenerated holes and CbFDH in the interior and exterior of CdS/PTi microcapsules. Such compartmental design may elevate the compatibility between CbFDH and photocatalyst by avoiding their direct contact as shown in Figure 4a. To verify the compatibility, CbFDH was incubated with CdS/PTi microcapsules in PBS buffer containing 400 mM TEOA (pH = 7.0) under visible light illumination (λ = 405±5 nm, LED). After illumination for one hour, CbFDH maintained 96.1±5.3% relative activity compared with that of CbFDH incubated in darkness (Figure 4b). As a comparison, CdS QDs were deposited on the outer surface of the PTi capsule wall to prepare PTi/CdS microcapsules (Figure S20). For PTi/CdS microcapsules, the photogenerated holes could directly contact CbFDH (Figure 4a). As shown in Figure 4b, the activity of CbFDH sharply decreased to 71.9±1.4% after incubated with PTi/CdS microcapsules. This indicated that the compartmental design 18


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ACS Catalysis

indeed elevated the compatibility between CdS/PTi microcapsules and CbFDH. To examine the enzyme deactivation mechanism, TEOA and dissolved oxygen were removed from the incubation solution, respectively. After the removal of TEOA, the activity of CbFDH incubated with PTi/CdS microcapsules decreased from 71.9±1.4% to 7.4±1.2%. This sharp decrease in enzymatic activity may be due to the higher concentration of exposed holes and ROS (Figure S21). For CdS/PTi microcapsules, holes and their derived •OH are compartmentalized inside the capsule wall. Considering the rather short half-life of 10-9 s in aqueous solution, hydroxyl radicals (•OH) generated in the capsule lumen should mainly undergo annihilation before contacting CbFDH in solution.27 Hence, 37.2±2.6% of the initial enzymatic activity was retained for CbFDH incubated with CdS/PTi microcapsules. The loss of ~60% activity should be attributable to the superoxide radical (O2 • -) from O2 reduction

and

unannihilated

•OH

from

holes.

The

function

of

the

compartmentalization design was further demonstrated by the changes in the activity of CbFDH incubated with CdS/PTi and PTi/CdS microcapsules in anaerobic PBS buffer. Under anaerobic conditions, the main poisonous species should be holes and their derived •OH (Figure S22). Approximately 90% of the CbFDH was deactivated when the enzyme was in direct contact with these poisonous species (Figure 4e). After compartmentalization of the holes and •OH into the capsule lumen with a semipermeable PTi wall, 55.6±2.7% of the initial activity was retained. These results again indicated the improved compatibility between the photocatalyst and enzyme in our compartmentalization design. FDH from Candida boidinii is homodimers with a total molecular weight of 80.62 kDa.53 The active sites were located at the cleft between two similar domains, each a sandwich of α-helix, parallel β-sheet, and α-helix.36 The two domains, termed the 19


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“NAD+ binding domain” and “catalytic domain”, were linked by two long α-helices. After complexation with NAD+ and formate anions, the clefts were closed to promote hydride transfer. Although the deactivation mechanism is still not clear, we hypothesized that the holes and ROS should significantly disrupt the α-helix of the native CbFDH, resulting in the dissociation of the “NAD+ binding domain” and the “catalytic domain”.53 The Rossmann fold structure of the “NAD+ binding domain” and flavodoxin-like topology of the “catalytic domain” may also be oxidized. The structural changes in CbFDH were monitored by CD spectrometry (Figure 4c). The CD spectrum of CbFDH incubated in darkness exhibited the characteristic bands of α-helical structure at 208.9 and 218.5 nm, corresponding to the π-π* and n-π* amide transitions of the polypeptide chain, respectively.54 After incubation with PTi/CdS microcapsules, the two negative bands at 208.9 and 218.5 nm were markedly altered. In particular, the content of α-helix in CbFDH changed from 48.5% to 14.7% (Figure 4d),55 indicating that the holes and ROS disrupted the α-helix of native CbFDH. For CdS/PTi microcapsules, the shape of the two bands remained the same, and the α-helix content in CbFDH was determined to be 35%. This result suggested that CdS/PTi microcapsules can successfully shield the holes and protect the enzyme. 2.4. Artificial Thylakoid-FDH Coupled System for the Conversion of CO2 to Formate.

20


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ACS Catalysis

Figure 5. (a) Photobiocatalytic formate production with different photocatalysts and CbFDH loading. (b) Formate production with regenerated NADH and commercial NADH. (c) Formate production under dark conditions with different illumination time and corresponding quantum efficiencies. The reaction was conducted in darkness for 2 hours under 0.3 MPa CO2 and 37 °C. (d, f) Photobiocatalytic formate production with light-dark cycles using CbFDH or TsFDH. (e) Biocatalytic conversion of CO2 by CbFDH and TsFDH. Reaction conditions for (a): [photocatalyst] = 0.4 g l-1 (CdS) or 1 g l-1 (microcapsules), [CbFDH] = 2 g l-1 (left three columns) and 0.4-8 g l-1 (right three columns), [NAD+] = 5 mM, [M] = 0.25 mM, [TEOA] = 400 mM, PBS buffer (pH 7.0, 100 mM), [CO2] = 0.3 MPa, 37 °C, visible light illumination (λ = 405±5 nm). Reaction conditions for (b and c): Light stage: [CdS/PTi] = 1 g l-1, [NAD+] = 5 mM, [M] = 0.25 mM, [TEOA] = 400 mM, PBS buffer (pH 7.0, 100 mM), RT, visible light illumination (λ = 405±5 nm). Dark stage: [CbFDH] = 2 g l-1, [CO2] = 0.3 MPa, 37 °C, darkness, 3 hours for (b) and 2 hours for (c). Reaction conditions for (e): [FDH] = 2 g l-1, [NADH] = 0.25 mM, PBS buffer (pH 7.0, 100 mM), saturated CO2, RT. Error bars represent the standard deviation based on duplicate experiments (n = 2).

Based on the above analysis, CdS/PTi microcapsules were coupled with CbFDH to convert CO2 into formate. The photobiocatalytic conversion of CO2 was conducted at a pressure of 0.3 MPa CO2 and 37 °C under visible light illumination (λ = 405±5 nm, LED) for 2 hours. The concentration of formate was determined by a Tracera GC-2010 Plus (Shimadzu Scientific Instruments) equipped with a barrier ion 21


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discharge

detector

(BID)

(Figure

S23).

Page 22 of 41

As

expected,

the

CdS/PTi

microcapsule-CbFDH coupled system produced a much higher concentration of formate than the PTi/CdS microcapsule-CbFDH and CdS nanoparticle-CbFDH coupled systems when using TEOA as the electron donor. As shown in Figure 5a, the CdS/PTi microcapsule-CbFDH coupled system produced 1.73±0.13 mM formate, exceeding the production by the PTi/CdS microcapsule-CbFDH and the CdS nanoparticle-CbFDH coupled systems by 561% and 665%, respectively. This remarkable increase was probably due to the improved NADH regeneration activity and the enzyme compatibility of CdS/PTi microcapsules compared with PTi/CdS microcapsules and CdS nanoparticles. To further optimize the performance of the CdS/PTi microcapsule-CbFDH coupled system, the loading of CbFDH was tuned. When 0.4 g l-1 CbFDH was used, only 0.63±0.09 mM formate was produced. As the loading of CbFDH increased to 1 g l-1, the concentration of formate increased sharply to 3.02±0.23 mM, achieving a formate production rate of 1500 μM hour-1 and a turnover number of 0.6 for NAD+. This should be attributed to the higher activity of the CO2 reduction reaction. When we further increased the loading of CbFDH, the concentration of formate decreased slightly, consistent with previous observations that a high concentration of enzyme reduced NADH regeneration activity by interacting with [M].56 In addition to TEOA, water was also used as the electron donor to convert CO2 into formate by coupling CdS/RuN/PTi microcapsules with CbFDH. After 2 hours illumination, only 0.10±0.02 mM formate was detected in CO2 saturated PBS buffer (data not shown). The lower photobiocatalytic performance should be arisen from the lower NADH regeneration rate and yield when water was used as the electron donor. To further demonstrate the artificial photosynthesis process, a CdS/PTi 22


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ACS Catalysis

microcapsule-CbFDH coupled system was illuminated by visible light (λ = 405±5 nm, LED) with light-dark cycles to mimic day-night cycles in nature. Figure 5b shows that NADH could be regenerated and accumulated during the light stage. In the dark stage, the regenerated NADH was consumed by CbFDH accompanied by the production of formate, which exhibited a similar consumption rate to that of commercial NADH. This finding suggested the formation of enzymatically active 1,4-NADH during the light stage. Interestingly, the amount of consumed NADH was ~1.8 mM, while only ~0.8 mM formate was produced. The additional consumption of NADH should be due to the degradation of NADH during the incubation under 37 °C. Moreover, to investigate the solar energy storage capability of the CdS/PTi microcapsule-CbFDH coupled system, the illumination time of the light stage was tuned. As shown in Figure 5c, as the illumination time increased from 10 min to 30 min, the formate produced in the dark stage increased. This behavior was attributed to the accumulation of higher concentrations of NADH in the light stage with prolonged illumination time, which was beneficial for the production of formate and resulted in a similar quantum yield of 0.73±0.18% for the CdS/PTi microcapsule-CbFDH coupled system. However, when the illumination time was increased to 40 min, the concentration of formate decreased. A possible reason lies in the saturation of NADH in the light stage, which may lead to its degradation with longer illumination times. Subsequently, the CdS/PTi microcapsule-CbFDH coupled system was exposed to several light-dark cycles. To maintain the high efficiency, the durations of the light and dark stages were set as 30 and 60 min, respectively. As expected, the concentration of formate increased continuously during the light-dark cycles (Figure 5d), achieving turnover number of ~75 for CbFDH. This difference was probably caused by the superior photocatalytic performance of CdS/PTi microcapsules, which 23


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helped to store solar energy as NADH in the light stage and enabled the production of formate during light-dark cycles. A quantum yield of 0.40±0.08% was finally achieved, which was on the same order of magnitude as the year-long average determined for plants (~0.2 to 1.6%).17, 18 On the basis of the above discussion, an efficient and compatible photobiocatalytic system with two functional subunits and a size-selective capsular structure was demonstrated. In this system, the two functional subunits could be optimized individually and work synergistically to improve the performance of the photobiocatalytic system or to extend its application scope. For example, formate dehydrogenase from Thiobacillus sp. (TsFDH), which has higher CO2-reducing activity than CbFDH, was coupled with CdS/PTi microcapsules. As shown in Figure 5e, the rate of CO2 conversion for TsFDH was ~5 times higher than that for CbFDH (0.081 vs 0.016 µM s-1). Furthermore, TsFDH was coupled with CdS/PTi microcapsules for the photobiocatalytic conversion of CO2. In comparison with the CbFDH-CdS/PTi coupled system, the TsFDH-CdS/PTi coupled system exhibited a higher quantum efficiency of 0.66±0.13% over three light-dark cycles, manifesting the application potential of this system. 2.5. Artificial Thylakoid-Multienzyme Coupled System for the Conversion of CO2 to Methanol.

Figure 6. (a) Proposed reaction scheme. (b) Photobiocatalytic conversion of CO2 into methanol. Reaction conditions for (b): [CdS/PTi] = 1 g l-1, TsFDH-FaldDH-YADH 24


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ACS Catalysis

complex, [NAD+] = 5 mM, [M] = 1.25 mM, [AA] = 400 mM in Tris-HCl buffer (pH 7.0, 50 mM), [CO2] = 0.05 MPa, RT, and visible light illumination (λ = 405±5 nm). The TsFDH-FaldDH-YADH complex was prepared by adding the solution containing [TsFDH] = 0.5 mg, [FaldDH] = 0.5 mg, [YADH] = 0.1 mg into 500 µL protamine, which was then used to induce the mineralization of silica. TsFDH, FaldDH and YADH were coimmobilized in the silica matrix during the mineralization process, resulting in the formation of the TsFDH-FaldDH-YADH complex.

In comparison with the photocatalytic system, the photobiocatalytic system exhibited high potential in product specificity and diversity owing to the high selectivity, diversity and combinability of biocatalysts. In our study, the product scope was extended to methanol from CO2 by coupling CdS/PTi microcapsules with multienzymes, i.e., formate dehydrogenase from Thiobacillus sp. (TsFDH), formaldehyde dehydrogenase from Pseudomonas sp. (FaldDH) and yeast alcohol dehydrogenase (YADH) (Figure 6a). The TsFDH-FaldDH-YADH “complex” was prepared by co-immobilizing TsFDH, FaldDH and YADH into a silica matrix produced by biomimetic mineralization.57 More than 95% of the initially added enzyme was immobilized in the silica matrix as determined by the Bradford assay. As shown in Figure 6a, CO2 could be reduced into methanol by TsFDH, FaldDH and YADH using NADH provided by CdS/PTi microcapsules. To confirm the photobio (multienzyme)-coupled reactions, deletional control experiments were carried out in which the TsFDH-FaldDH-YADH “complex” or CdS/PTi microcapsules were removed (Figure 6b). In the absence of TsFDH-FaldDH-YADH “complex” or CdS/PTi microcapsules, no accumulation of methanol was observed. Only TsFDH-FaldDH-YADH-CdS/PTi coupled system produced 85.1±6.3 µM methanol with an initial production rate of 99 μM hour-1, suggesting successful implementation of the proposed reaction scheme (Figure 6a). The methanol production rate of this 25


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Page 26 of 41

work was much higher than previous particulate photo-enzymatic systems (Table S3), demonstrating the merits of “artificial thylakoid”.21,

58

This result manifested the

product flexibility of our system by combining CdS/PTi microcapsules with other biocatalysts. Although only C1 products (formate and methanol) were obtained, our system provides a compatible design strategy for photobiocatalytic systems. By developing novel multienzymatic cascade reactions or by coupling with photocatalytic organic synthesis, more valuable products could be expected.

26


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ACS Catalysis

2.6. Artificial Thylakoid-NADH Independent Enzyme Coupled System.

Figure 7. (a) Proposed reaction scheme. (b) Photocatalytic reduction of FMN. (c) Photobiocatalytic oxidation of TMB by alternative visible light illumination. Reaction conditions for (b): [CdS/PTi] = 1 g l-1, [FMN] = 0.1 mM, [TEOA] = 100 mM in anaerobic PBS buffer (pH 7.0, 100 mM), λ = 405±5 nm. (c) Light stage: [CdS/PTi] = 1 g l-1, [FMN] = 0.01 mM (blue curve) and 0 mM (yellow curve), [TEOA] = 100 mM in PBS buffer (pH 7.0, 100 mM), λ = 405±5 nm. Dark stage: [HRP] = 2.26 nM, [TMB] = 0.5 mM. Error bars represent the standard deviation based on duplicate experiments (n = 2).

Although NADH is a widely used cofactor that mediates photocatalyst and biocatalyst, exploring other mediators might further expand the applicability of this photobiocatalytic system. For this purpose, horseradish peroxidase (HRP), a heme-dependent enzyme that does not rely on NADH, was coupled with CdS/PTi microcapsules. Flavin mononucleotide (FMN) was used as the mediator to couple CdS/PTi microcapsules with HRP by producing H2O2 (Figure 7a). Under anaerobic conditions, FMN was completely reduced by CdS/PTi microcapsules (Figure 7b), as demonstrated by the decrease in the characteristic absorption band of FMNOx at ~450 nm.59 27


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Page 28 of 41

Then, we evaluated the H2O2-forming re-oxidation of reduced FMN (FMNRed) to drive HRP-catalyzed dehydrogenation.60 3,3',5,5'-Tetramethylbenzidine (TMB), a commonly used substrate of HRP, was used to evaluate the feasibility of this photobiocatalytic system. The oxidized products of TMB (oxTMB) showed a blue color, which can be easily detected by UV-vis spectrometry. After visible light illumination for 5 min, 2.26 nM HRP and 0.5 mM TMB were added to the ten times-diluted solutions in darkness. Experiments without FMN produced negligible products, while the entire system produced 537.1±36.6 µM oxTMB after incubation in darkness for 220 s. The photobiocatalytic system achieved almost 23,700 turnovers for HRP and 55 turnovers for FMN, which indicated that CdS/PTi microcapsules could be coupled with heme-dependent enzyme (HRP) by using flavin cofactor. 3. CONCLUSIONS In summary, we explored the possibility of using capsular structures as thylakoid mimics to coordinate photocatalytic and biocatalytic reactions for the construction of artificial

photosynthesis

systems.

CdS/PTi

microcapsules

with

CdS

QDs

homogeneously deposited on the inner surface of the PTi capsule wall were successfully prepared through biomimetic mineralization. The strong electronic coupling and favorable band structure between CdS QDs and PTi separated the holes and electrons across the capsule wall and achieved a NADH regeneration activity of 4226±121 μmol g-1 hour-1, among the highest values ever reported. The capsular structure of CdS/PTi microcapsules compartmentalized the photogenerated holes and ROS, thereby protecting FDH from deactivation and thus conferring high compatibility between the photocatalyst and biocatalyst. As a result, the CdS/PTi microcapsule-FDH coupled system converted CO2 into formate with a quantum yield of 0.66±0.13% over several light-dark cycles. Moreover, CdS/PTi microcapsule could 28


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ACS Catalysis

also activate multiple enzymatic reduction of CO2 to methanol. This artificial thylakoid is applicable to the construction of a broad range of complex reaction systems by coupling with enzymes dependent or independent of NADH. 4. EXPERIMENTAL SECTION 4.1. Materials. Formate dehydrogenase from Candida boidinii (CbFDH, F8649, EC.1.2.1.2), yeast alcohol dehydrogenase (YADH, A7011, EC 1.1.1.1), formaldehyde dehydrogenase from Pseudomonas sp. (FaldDH, F1879, EC.1.2.1.46), horseradish peroxidase (HRP, E.C. 1.11.1.7), flavin mononucleotide (FMN), β-Nicotinamide adenine dinucleotide (NAD+), 50 wt % Ti-BALDH, poly(sodium 4-styrenesulfonate) (PSS, Mw=70000 Da), protamine sulfate salt from salmon and 2,2’-bipyridyl were purchased from Sigma-Aldrich.

Cadmium

sulfate,

pentamethylcyclopentadienylrhodium(III)

sodium

sulfide,

chloride

dimer

of

(Cp*RhCl2)2,

ethylenediaminetetraacetic acid (EDTA) and sodium silicate were purchased from Aladdin (Shanghai, China). 4.2. Preparation of CdS/PTi Microcapsules. CdS QDs decorated protamine-titania (CdS/PTi) microcapsules were prepared by a hard template method. CaCO3 microspheres doped with PSS (PSS-CaCO3 microspheres) in ~3 μm diameter were fabricated by co-precipitation.38 CdS QDs were deposited on PSS-CaCO3 microspheres by successive ionic layer adsorption and reaction (SILAR).39, 41 Briefly, PSS-CaCO3 microspheres were first dispersed into 10 mM CdSO4 aqueous solution for 1 min. After water washing for 3 times, the Cd2+ adsorbed microspheres were dispersed into 10 mM Na2S aqueous solution for 1min. After water washing, CdS QDs decorated PSS-CaCO3 microspheres were obtained. The loading amount of CdS was controlled by repeating the SILAR process (0-4 29


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times). CdS QDs decorated PSS-CaCO3 microspheres were then dispersed into 2 g l-1 protamine solution for 10 min. After water washing for 3 times, the microspheres were dispersed into 1.25 wt% Ti-BALDH solution for 10 min. After water washing, the process was repeated one time and two layers of Protamine-Titania (PTi) were deposited on the microspheres. CdS/PTi microcapsules were obtained after removing the CaCO3 microspheres through EDTA treatment. 4.3. Photocatalytic Regeneration of NADH. The photocatalytic regeneration of NADH was conducted using a quartz reactor (3.5

mL)

and

a

300-watt,

405±5

nm

LED-lamp.

[Cp*Rh(bpy)H2O]2+

(Cp*=pentamethylcyclopentadienyl, bpy=2,2-bipyridyl) was used as the electron mediator and was denoted as [M]. First, 100 mM PBS buffer (pH 7.0) contained 1 g l-1 CdS/PTi microcapsules, 1 mM NAD+, 0.25mM [M] and 400 mM TEOA was added in the quartz reactor. After incubating in darkness for 10 min, the quartz reactor was illuminated by 405±5 nm LED-lamp. The light intensity on the quartz reactor was measured to be 200 mW cm-2 by a radiation meter (photoelectric instrument factory of Beijing normal university). The concentration of NADH was determined by measuring the absorbance at 340 nm (Abs 340) using a UV-Vis spectrophotometer. The extinction coefficient for NADH was 6220 M-1 cm-1. 4.4. Compatibility between CdS/PTi Microcapsules and CbFDH. 1 g l-1 CbFDH were incubated with CdS/PTi and PTi/CdS microcapsules under visible-light illumination (λ=405 nm, light intensity=200 mW cm-2) for one hour in (anaerobic) PBS buffer (100 mM, pH=7.0) with or without 400 mM TEOA. The activity of CbFDH was evaluated by adding 0.4 mg CbFDH into 5 mL PBS buffer (100 mM, pH=7.0) containing 133 μM NAD+ and 10 mM formic acid. The activity of CbFDH was detected using a UV-Vis spectrophotometer by measuring the 30


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ACS Catalysis

absorbance at 340 nm. The relative activity was determined by assuming the activity of CbFDH incubated in darkness as 100%. 4.5. Photobiocatalytic Conversion of CO2 into Formate. Photobiocatalytic conversion of CO2 was conducted under 0.3 MPa CO2 and 37 °C in a stainless steel reactor, with a 300-watt, 405±5 nm LED-lamp. The light could pass through the quartz window and reach the reaction solution. The reaction solution contains 5 mM NAD+, 0.25 mM [M], 1 g l-1 CdS/PTi or PTi/CdS microcapsules, 2 g l-1 CbFDH, 400 mM TEOA, and 100 mM PBS buffer (pH 7.0). To keep the same weight of CdS with CdS/PTi microcapsules, 0.4 g l-1 CdS nanoparticles was used. After illuminated for 2 hours, the reaction solution was centrifuged. The formate concentration in the supernatant was determined by a Tracera GC-2010 Plus (Shimadzu Scientific Instruments) equipped with a barrier ion discharge detector (BID). Photobiocatalytic conversion of CO2 with one light-dark cycle was performed. For the light stage, the reaction solution containing 5 mM NAD+, 0.25 mM [M], 1 g l-1 CdS/PTi microcapsules, 400 mM TEOA, and 100 mM PBS buffer (pH 7.0) was added into the quartz reactor. The reaction solution was illuminated by visible light (λ=405±5nm, LED) for 10-40 min. The light intensity on the quartz reactor was 200 mW cm-2. For the dark stage, the above solution was transferred to the stainless steel reactor and 2 g l-1 FDH was added. The reaction was conducted in darkness for 2 hours under 0.3 MPa CO2 and 37 °C. The photobiocatalytic conversion of CO2 with several light-dark cycles was conducted in quartz reactor and stainless steel reactor, alternatively. The reaction conditions for the light and dark stage were the same with one light-dark cycle experiment. 4.6. Quantum Yield Measurement. 31


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The quantum yield for NADH and formate production was calculated according to the following equation (1): quantum yield (%) 

2  mol of NADH or formate mol of absored photons

(1)

NADH regeneration solution contained 1 mM NAD+, 0.25 mM [M], 1 g l-1 CdS/PTi microcapsules, 2 g l-1 FDH, 400 mM TEOA, and 100 mM PBS buffer (pH 7.0). Formate production solution contained 5 mM NAD+, 0.25 mM [M], 1 g l-1 CdS/PTi microcapsules, 2 g l-1 FDH, 400 mM TEOA, and 100 mM PBS buffer (pH 7.0). Solutions in quartz reactor with a pathlength of 10 mm were illuminated by visible light (λ=405±5nm, LED). The photons absorbed by the solutions were determined by comparison of light transmission through solutions with CdS/PTi microcapsules and control solutions with PTi microcapsules. 4.7. Photobiocatalytic Conversion of CO2 into Methanol. TsFDH-FaldDH-YADH complex was prepared by adding 0.5 mg TsFDH, 0.5 mg FaldDH, 0.1 mg YADH into 500 uL protamine. Then, 1 mL Na2SiO3 (30 mM, pH 7.5) was added into the above solution. After incubating for 10 min, the precipitate was collected by centrifugation and washed by deionized water. The enzyme immobilization

efficiency

was

determined

by

Bradford

assay.

TsFDH-FaldDH-YADH complex was added into Tris-HCl buffer (pH 7.0, 50 mM) containing 1 g l-1 CdS/PTi microcapsules, 5 mM NAD+, 1.25 mM [M], 400 mM AA. The photobiocatalytic reaction was conducted under 0.05 MPa CO2 and room temperature in a sealed glass bottle illuminated by a 300-watt, 405±5 nm LED-lamp. The concentration of methanol in the supernatant was determined by a Tracera GC-2010 Plus (Shimadzu Scientific Instruments) equipped with a barrier ion discharge detector (BID). 32


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4.8. Photobiocatalytic Reaction Independent of NADH. Photocatalytic reduction of FMN was conducted under anaerobic condition and room temperature in a sealed glass bottle illuminated by a 300-watt, 405±5 nm LED-lamp. The anaerobic PBS buffer was obtained by purging nitrogen into boiling PBS buffer. After cooling down to the room temperature, the reaction solution containing 1 g l-1 CdS/PTi microcapsules, 0.1 mM FMN, 100 mM TEOA were prepared with anaerobic PBS (pH 7.0, 100 mM) and added into a sealed glass bottle under nitrogen atmosphere. Photobiocatalytic reaction was performed with one light-dark cycle. For the light stage, the reaction solution containing 1 g l-1 CdS/PTi microcapsules, 0.01 mM FMN, 100 mM TEOA was added into a glass bottle. The reaction solution was illuminated by visible light (λ=405±5nm, LED) for 5 min. The light intensity on the quartz reactor was 200 mW cm-2. For the dark stage, the above solution was diluted for ten times and 2.26 nM HRP and 0.5 mM TMB was added. The concentration of oxTMB was detected by UV-vis spectrometer by measuring the absorbance at 652 nm (Abs 652). ASSOCIATED CONTENT Supporting Information. The Supporting Information is available free of charge at DOI:XXX. The preparation of HPAN-PTi membrane, PTi/CdS microcapsules, CdS/PSi microcapsules and [Cp*Rh(bpy)H2O]2+; The cloning, expression and purification of TsFDH; Electrochemical and photoelectrochemical measurements; preparation and immobilization of [Ru(tpy)(bpy-NH2)Cl]+; Schematic preparation process and SEM image of CdS QDs decorated PSS-CaCO3 microspheres; EDS spectra of PSS-CaCO3 microspheres and CdS/PTi microcapsules; TEM image of CdS/PTi microcapsules; XRD patterns and tauc plots of CdS/PTi and PTi microcapsules; The size of TEOA; 33


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Schematic of a home-made diffusion device and the preparation process of HPAN-PTi membrane; Schematic of photocatalytic NADH regeneration; Schematic preparation process and characterizations of CdS/PTi microcapsules with different deposition cycles of CdS; Characterizations of CdS nanoparticles, CdS/PSi microcapsules and PTi/CdS microcapsules; Cd 3d and S 2p high-resolution XPS spectra of CdS/PTi microcapsules and CdS nanoparticles; PL spectra and EIS spectra of CdS/PTi and CdS/PSi microcapsules; Immobilization of [M] in CdS/PTi microcapsules; Photocatalytic regeneration of NADH using water as the electron donor; The activity of CbFDH after incubated with TEOA, [M] and CdS/PTi microcapsules in PBS buffer for an hour in darkness; Relative amount of •OH radicals generated by CdS/PTi and PTi/CdS microcapsules under visible-light illumination; Schematic of the enzyme deactivation by CdS/PTi and PTi/CdS microcapsules under anaerobic condition; Standard plot of formate detected by Tracera GC-2010 Plus; NADH regeneration performance of different microcapsules; Comparison of the NADH regeneration performance by different photocatalysts; Comparison of the efficiencies for the CO2 to methanol conversion in various photo-enzymatic systems; The calculation of average PL lifetime and electron transfer rate. AUTHOR INFORMATION Corresponding Author: *Jiafu Shi, Email: [email protected] *Zhongyi Jiang, Email: [email protected] Notes The authors declare no competing financial interests. ACKNOWLEDGMENT

34


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This work was supported by the National Natural Science Funds of China (91534126, 21776213, 21621004), the National Science Fund for Distinguished Young Scholars (21125627) and Open Funding Project of the National Key Laboratory of Biochemical Engineering (2015KF-03). REFERENCES 1.

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TOC figure

41


Artificial Thylakoid for the Coordinated Photo-Enzymatic Reduction of

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