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Janus reactors with highly efficient enzymatic CO2 nanocascade at air-liquid interface Song Gao, Munirah Mohammad, Hao-Cheng Yang, Jia Xu, Kang Liang, Jingwei Hou, and Vicki Chen ACS Appl. Mater. Interfaces, Just Accepted Manuscript • DOI: 10.1021/acsami.7b14465 • Publication Date (Web): 21 Nov 2017 Downloaded from http://pubs.acs.org on November 22, 2017

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ACS Applied Materials & Interfaces

Janus reactors with highly efficient enzymatic CO2 nanocascade at air-liquid interface Song Gao1, Munirah Mohammad1, Hao-Cheng Yang2†, Jia Xu3, Kang Liang1,4, Jingwei Hou1,5*and Vicki Chen1 1

UNESCO Centre for Membrane Science and Technology, School of Chemical Engineering,

University of New South Wales, Sydney, 2052, Australia 2

MOE Key Laboratory of Macromolecular Synthesis and Functionalization, Department of

Polymer Science and Engineering, Zhejiang University, 310027, China 3

Key Laboratory of Marine Chemistry Theory and Technology (Ocean University of China),

Ministry of Education, Qingdao, 266100, P. R. China 4

Graduate School of Biomedical Engineering, University of New South Wales, Sydney, 2052,

Australia 5

Department of Materials Science and Metallurgy, University of Cambridge, Cambridge, CB3

0FS, UK

ACS Paragon Plus Environment

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KEYWORDS Multi-phase catalytic reaction; Enzymatic cascade; Janus membrane; CO2 reduction; Carbonic anhydrase, Formate dehydrogenase

ABSTRACT

Though enzymatic cascade reactors have been the subject of intense research over the past few years, their application is still limited by the complicated fabrication protocols, unsatisfactory stability and lack of effective reactor designs. In addition, the spatial positioning of the cascade reactor has so far not been investigated, which is of significant importance for bi-phase catalytic reaction systems. Inspired by the Janus properties of the lipid cellular membrane, here we show a highly efficient Janus gas-liquid reactor for CO2 hydration and conversion. Within the Janus reactor, nanocascades containing the nanoscale compartmentalized carbonic anhydrase (CA) and formic dehydrogenase (FateDH) were positioned at a well-defined gas-liquid interface, with a high substrate concentration gradient. The Janus reactor exhibited 2.5 times higher CO2 hydration efficiency compared with the conventional gas-liquid contactor with pristine membranes, and the formic acid conversion rate can reach approximately 90%. Through this work, we provide evidence that the spatial arrangement of the nanocascade is also crucial to efficient reactions, and the Janus reactor can be a promising candidate for the bi-phase catalytic reactions in environmental, biological and energy aspects.


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1. Introduction Gas-liquid bi-phase catalytic reactions such as methane oxidization, alkane halogenation, organic hydrogenation, hydrogen sulphide removal and CO2 sequestration, are considered as the cornerstones of modern chemical, pharmaceutical and food industries.1–8 Compared with the homogeneous catalytic reactions, the bi-phase reactions are still difficult to control due to the complicated mass transfer process: for the heterogeneous catalytic reaction, the reactant mass transfer in gaseous phase is usually efficient, yet the dissolution and subsequent liquid mass transfer are relatively sluggish. Conventionally, to accelerate the bi-phase or multiphase catalytic reactions, certain treatments to generate high interfacial areas are needed, such as vigorous stirring and aeration, or the application of microfluidic reactors.9–11 However, these approaches may either significantly increase the energy and capital cost, or the fabrication is complicated thus not ready for scale-up. To achieve efficient bi-phase catalytic reactions, both catalyst and reactor design should be carefully considered.12,13 In terms of the catalysts, enzymes are promising candidates as they can perform highly efficient reactions under ambient conditions with high specificity. An additional benefit is their capability to form a multi-stage cascade reaction for more complicated reactions which are otherwise difficult to achieve.14 In nature, the life of eukaryote depends on series of well-orchestrated enzymatic reactions in different organelles, in which different enzymes are compartmentalized to facilitate the metabolic cycles, allowing the efficient shuttle of substrates, products and reducing equivalents (e.g. pyridine nucleotide-based cofactors) across intracellular


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membranes.15,16 This intriguing arrangement also bring us to the question of reactor design. The principle of the compartmentalization is the nano-scale positional assembly and spatial separation of different biocatalytic reactions, allowing a spatiotemporal control over the cascade reactions.17 Therefore, a growing effort has been made to artificially mimicking the multienzyme cascade for efficient bioconversion.17–21 Nanoparticles, nanofibers, polymersomes and nanoclusters have been applied to build the enzymatic cascades.17,19,22–26 Compared with the free enzyme mixtures, the co-immobilized and compartmentalized cascades usually have much higher catalytic efficiency. Among different enzymatic cascade reactions, the photosynthesis for carbon fixation via dehydrogenases attracts the widest interest due to its potential to mitigate the energy and environmental challenges.27–30 Hitherto, most multi-enzyme cascade reactors require CO2 aeration into the aqueous phase where the immobilized enzymes are suspended. Yet the efficiencies of these systems are largely restricted by the sluggish CO2 hydration and mass transfer in an aqueous phase. Ideally, by strategically positioning the cascade at the gas-liquid interface, it can maximize the substrate concentration gradient as well as its mass transfer efficiency.31–33 Membrane gas-liquid contactors have been investigated for the bi-phase catalytic reaction. Even though the existence of extra physical barrier can improve the mass transfer resistance, membrane can effectively maintain a well-defined gas-liquid interface, with flexible configuration which can be readily scalable.7 It also requires smaller footprint and is easy to operate. Hydrophobic membranes can be applied to maintain a gas-liquid interface, but enzyme immobilization on hydrophobic membranes usually lead to denaturation.34 In nature, carbonic anhydrase (CA) is located on the endothelial membrane of the lung.35 For the lipid bi-layer membrane structure, the hydrophilic section ensures effective enzyme immobilization, and the


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hydrophobic section can maintain a defined liquid-liquid or liquid-gas interphase. The immobilized CA can therefore maintain its superior catalytic efficiency with a high CO2 concentration gradient at the interfacial region.21,34 Inspired by the Janus lipid bi-layer structure, positioning the multi-enzyme cascade nanoreactors at the gas-liquid interface can significantly promote its catalytic efficiency, also allow easier process control. However, such a Janus cascade reactor has not been reported so far. Recently, we have developed a facile and controllable polydopamine (PDA) deposition technique for single side hydrophilic modification of hydrophobic membranes.36–38 Moreover, the abundant catechol as well as amine groups exist on the PDA modified layer can induce the localized biomineralization for biocatalytic cascade immobilization. Herein, we report a facile technique to fabricate a multi-enzyme cascade, and a strategy to assemble the cascade at a welldefined gas-liquid interface with a Janus membrane. Titania nanoparticles with encapsulated CA were prepared via a sol-gel process, followed by the attachment of formate dehydrogenase (FateDH) onto the nanoparticle surface. For the biocatalytic Janus membrane assembly, PDA was first deposited onto one side of polypropylene (PP) membrane to induce the co-precipitation of titania nanoparticle containing CA in-situ. Subsequently, FateDH was immobilized on the modified membrane surface for the second step enzymatic conversion into formic acid. The performance of the Janus membrane including mass transfer, enzyme loading capacity, stability and reusability were systematically analyzed. Eventually, the CO2 hydration and conversion test was carried out with a bi-phase gas-liquid membrane contactor. 2. Experimental Section 2.1 Materials


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Carbonic anhydrase (CA) from bovine erythrocytes (E.C.4.2.1.1), formate dehydrogenase from Candida boidinii (FateDH, E.C.1.2.1.43), titanium bis(ammonium lactate)dihydroxide (TiBALDH, 50 wt.% in aqueous solution), arginine, dopamine hydrochloride, polyethylenimine (PEI, MW=800), Tris(hydroxymethyl) aminomethane (Trizma base) and reduced nicotinamide adenine dinucleotide (NADH, 98 wt.%) were purchased from Sigma-Aldrich Chemical Co. 4Nitrophenyl acetate (p-NPA) from Sigma-Aldrich was applied for CA activity assay. Polypropylene flatsheet membranes (0.22 µm) from Membrana GmbH were used for Janus membrane fabrication. All other chemicals were of the highest purity and used with further purification. 2.2 Synthesis of spatially separated multienzyme nanoparticles The spatially separated multienzyme nanoparticle was constructed via the bio-mineralization process using Ti-BALDH as the precursor. In a typical immobilization procedure, 5.0 mg of carbonic anhydrase (CA) was firstly dissolved in 5.0 mL of 300 mM arginine solution (0.05 M Tris-HCl buffer, pH 6.8), to which 2.5 mL of Ti-BALDH solution (50 mM) was added. The mixture was vigorously stirred at 1,500 RPM. As the titania nanoparticle precipitated around the CA molecules, the solution gradually became cloudy. After a certain period of time, 2.5 mL dopamine hydrochloride (2.5 mg/mL in 50 mM Tris-HCl buffer, pH 6.8) was added and the suspension solution immediately turned into orange, indicating the formation of nanoparticle aggregates. After stirring for another 10 min at 300 RPM, the nanoparticle suspension solution was centrifuged at 7,500 RPM for 20 min at 4°C. All the unreacted chemicals were washed off by centrifugation and re-dispensation for two times in Tris-HCl buffer. The resultant CA-bearing nanoparticles are denoted as CA-TiO2 NPs in this manuscript.


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For the co-immobilization of spatially separated formic dehydrogenase (FateDH) on the nanoparticle surface, 10 mg of CA-TiO2 NPs were dispersed into 5 mL FateDH solution (0.05 M Tris-HCl buffer, pH 6.8) for 10 hours under ambient conditions. Subsequently, the suspension solution was centrifuged and washed. 2.3 Fabrication of the Janus enzymatic cascade membranes The Janus membrane fabrication was illustrated in Scheme S1. Specifically, The PP membrane was pre-wetted with pure ethanol, and then floated on the surface of a Tris buffer solution (50 mM, pH 8.5) containing 2 mg/ml dopamine and 2 mg/ml PEI. The reaction was carried out within a petri dish on a 100 RPM shaker at room temperature. The dopamine deposited PP Janus membrane was rinsed with Milli-Q water and ethanol to fully remove the unreacted chemicals. For CA-TiO2 deposition on the membrane surface, the Janus membrane was floated on the TiBALDH reaction solution with the hydrophilic side facing the liquid. The membrane area was 3.14 cm2 and the total reaction liquid volume was 10 ml (50 mM pH 6.8 Tris buffer containing 0.5 mg/ml CA enzyme and 12.5 mM Ti-BALDH). In order to investigate the effect of dopamine and arginine on the deposition process, 0.63 mg/ml dopamine and 0.5 mg/ml arginine were added to the deposition solution, respectively. In terms of the FateDH co-immobilization on the membrane, the CA-containing Janus membranes were floated on the surface of 2.5 mL dopamine hydrochloride (2.5 mg/mL in 50 mM Tris-HCl buffer, pH 6.8) for 3 hours, and then transferred to the surface of 5 mL of 0.5 mg/mL FateDH solution (0.05 M Tris-HCl buffer, pH 6.8) for 5 hours under ambient conditions. 2.4 Characterization


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Nanoparticle and membrane morphologies and the energy disperse X-ray spectra were examined by field emission scanning electron microscopy (FEI Nova Nano SEM 450). Dynamic light scattering (DLS, Malvern Nano) was applied to study the particle size distribution during the biocatalytic nanoparticle formation process. For each test, at least 13 cycles of reading were performed to minimize the error and the average diameter was reported. The particle surface components were characterized by X-ray photoelectron spectroscopy (Thermo ESCALAB250Xi, USA). The Fourier transform infrared spectroscopy (FTIR) analysis was carried out with Spotlight Fourier transform infrared spectrometer. The nitrogen adsorption isotherm was carried out with Micromeritic Tristar 3000 analyzer under liquid nitrogen environment (77K). The contact angle measurement of the Janus membranes was conducted in Attension Theta (Biolin Scientific) with a total drop size of 3.00 µL. 2.5 Activity assay The detailed CA activity assay can be found in our previous publication.39 Briefly, the esterase activity of CA was measured by a colorimetric method with p-NPA at 400 nm. For the free CA enzyme, 0.2 ml of CA solution was mixed with 2.4 ml Tris buffer solution (50 mM, pH 8) and 1.8 ml p-NPA (22 mM in acetonitrile). The mixture gradually changed to yellow colour, indicating the esterase activity of CA. In terms of immobilized CA, 5 mg of biocatalytic nanoparticles or a membrane with 3.14 cm2 was suspended in a mixture of 21.6 Tris buffer and 1.8 ml p-NPA solution. The absorbance was monitored every minute after the solution was quickly filtered through a Millipore 0.1 µm syringe filter. In this work, one unit (U) of CA activity was defined as the amount of CA required to convert 1 µmol of p-NPA per minute.


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To perform the FateDH activity assay, 10 ml Tris-HCl buffer (50 mM, pH 7) was bubbled with CO2 for 1 hour and then mixed with the same volume of 100 mM of NADH solution in Tris-HCl buffer (50 mM, pH 7). Then the co-immobilized nanoparticles or membranes were suspended in the mixture solution under constant stirring of 300 RPM. The reaction temperature was maintained at 37 °C. The NADH concentration was measured with UV-Vis spectrophotometer (Agilent, Cary UV-300), and one unit (U) of the FateDH activity was defined as the 1 µmol NADH consumed per minute throughout this study. 2.6 Gas-liquid contactor performance test In this work, the Janus biocatalytic membrane with co-immobilized enzymes was investigated for its capability for CO2 hydration and conversion within a flatsheet membrane gas-liquid contactor. The flatsheet Janus membrane (18 cm2 effective membrane area) was vertically placed within a membrane cell, with the hydrophilic side facing the liquid side. The gas chamber (~ 30 cm3) was feed with (20:80, v:v) CO2/N2 mixed gas at a flow rate of 8.0 ml/min. The retentate gas composition was continuously monitored with a gas chromatography (Shimadzu GC-2014). Under this condition, the measured CO2 concentration was between 7 - 19% with good reproducibility. For the liquid side (5.4 cm3), 30 ml 50 mM NADH in Tris buffer solution (50 mM, pH 7) was recirculated. The concentration of formic acid was also monitored with the GC. In this work, pristine PP membranes and Janus membranes with free enzymes or co-immobilized nanoparticles were also investigated as the benchmark. 3. Results and discussion 3.1 Fabrication of the CA-containing titania nanoparticle


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Arginine is a basic protein building block. Its amine side groups can enrich titanium bis(ammonium lactate)dihydroxide (Ti-BALDH) hence inducing the hydrolysis of titania precursors.40 On the other hand, CA molecules can also act as biomacromolecular promotors via attracting and concentrating Ti2+ ions onto their surface, and facilitate the formation of a titania inorganic cluster around CA molecules, known as biomineralization.22 A white cloudy suspension solution was immediately formed after the mixture of the arginine, CA and TiBALDH under constant stirring (Figure 1a). The nanoparticle size increases with longer hydrolysis reaction time (Figure 1b). To functionalize the nanoparticle surface for second enzyme co-immobilization, dopamine was added to the particle suspension mixture and reacted for another 10 min, which impose negligible increase to the particle size (Figure 1b), suggesting the thin and uniform PDA coating layer without self-aggregation. The catechol groups from PDA can interact with TiO2 surface through hydrogen bonds and coordination interactions, and they can further react with amine groups from enzyme via Michael addition or Schiff-base reactions to trigger the immobilization of FateDH.41 The dopamine-modified CA-bearing nanoparticles were referred as CA-TiO2 NPs in the subsequent manuscript.


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Figure 1. (a) Schematic diagram of the CA-TiO2 NPs fabrication process; (b) Size of the CAbearing nanoparticles; (c) BET surface area of the CA-TiO2 NPs; (d) SEM image of the CA-TiO2 NPs with 30 min reaction time; (e-g) Activity, enzyme loading and activity recovery for the CATiO2 NPs with different hydrolysis reaction time.

Ideally, the nanoparticles should have both large surface areas and mesoporous structures to ensure high enzyme anchor capability accompanied with efficient mass transfer.34,42,43 Based on the Brunauer, Emmett and Teller (BET) surface area results (Figure 1c), CA-TiO2 NPs prepared with an extended hydrolysis reaction time show lower surface areas, consistent with the growth of nanoparticle size over time. The BET results also illustrate dopamine treatment can effectively stabilize TiO2 nanoparticles mesoporous structure: the structure for CA-TiO2 NPs without dopamine can be damaged during the thermal BET pre-treatment process (150°C under vacuum for 3 h), leading to higher BET surface area (~80 m2/g for all nanoparticles prepared with different hydrolysis time, results not shown). On the other hand, the dopamine treated CA-TiO2 NPs have average Barrett-Joyner-Halenda (BJH) pore diameters between 13.4-9.7 nm (Table S1), indicating the material still possesses mesoporous structure after dopamine treatment, potentially allows the diffusion of substrates to the encapsulated enzymes.44 CA-TiO2 NPs with 30 min reaction time were visualized by SEM (Figure 1d), and the nanoparticle biocatalytic performance was systematically investigated with p-nitrophenyl acetate (p-NPA) as a substrate. Subject to longer hydrolysis time, the biocatalytic nanoparticle yield gradually increases, and then plateaued after 30 min (Figure 1e). Such an observation is in accordance with previous nanoparticle size results, indicating the nanoparticle crystallization and


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growth were almost completed after 30 min of the hydrolysis reaction. During this process, the CA loading in the CA-TiO2 NPs reduces from 71 to 37 µg/mg. In order to fully elucidate the nanoparticle crystallization and growth, a series of benchmark tests were carried out: for the synthesis solution only containing Ti-BALDH, the solution stayed clear for 50 min. With the presence of arginine, the mixture rapidly turned cloudy and the initial nanoparticle size was ~50 nm at 5 min and gradually increased to ~110 nm after 50 min of hydrolysis (results not shown). On the other hand, the mixture of CA and Ti-BALDH stayed clear and transparent during the whole experimental process. As a result, within the CA-TiO2 NPs synthesis solution (a mixture of Ti-BALDH, CA and arginine), the initial formed small TiO2 nanoparticles around arginine would gradually aggregate together to form relatively large nanoparticle clusters for CA encapsulation over time. FT-IR analysis was carried out to probe the presence of enzyme within the CA-TiO2 NPs (Figure S1a). The peak at 1650 cm-1 is originated from amide group on CA. For the CA-TiO2 NPs, it is important to study the spatial distribution of CA in the particles. Based on the nanoparticle surface XPS results (Figure S1b), C and N signals are observed for nanoparticles with and without CA, and the N/C ratios are comparable for both samples. This observation suggests the N peak is mainly originated from the surface polydopamine layer, and most CA molecules are encapsulated within the nanoparticles. In terms of the activity and recovery (Figure 1f), they both experienced constant decrease with nanoparticle size, attributing to the higher mass transfer resistance for the encapsulated enzymes. Considering the mesoporous structure of CA-TiO2 NPs, the substrate (p-NPA) can still efficiently diffuse into the nanoparticles and react with the encapsulated enzymes. In terms of the total activity for each batch of biocatalytic nanoparticles (Figure 1g), the results suggest that the


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highest activity is obtained after 30 min reaction, which is associated with the high particle yield and activity recovery at this condition (Figure 1e&f). As the total nanoparticle activity is very important for FateDH co-immobilization and potential CO2 bio-conversion, the reaction time of 30 min was selected for the subsequent investigation in this work. After immobilization, the storage stability under room temperature is substantially improved, with negligible activity loss over a 20 days’ storage, compared with a 60 % activity loss for free enzymes (Figure S1c). In terms of the reusability (Figure S1d), the CA-TiO2 NPs was tested for 20 catalysis cycles (5 min for each cycle), and the biocatalytic nanoparticles were recycled by filtrating the suspension solution through a 0.1 µm PVDF membrane. The nanoparticles were rinsed by 10 ml Tris buffer to remove the unreacted substrates. After each catalysis cycle, the presence of CA in the wash-off solution was not detectable with the Bradford method, indicating CA molecules can be stably encapsulated within the nanoparticles. The loss of activity during the reusability test can be explained by the potential aggregation during the filtration-resuspension process after each testing cycle. 3.2 Compartmentalized multienzyme nanocascades FateDH enzyme was bonded on to the surface of CA-TiO2 NPs to construct the multi-enzyme cascade. As demonstrated by the surface XPS and FT-IR results (Figure 2a and Figure S2a), the immobilization of FateDH leads to the increase of peak intensity at 1650 cm-1, accompanied with an increase of the surface N/C ratios (0.27 to 0.30), indicating the FateDH is successfully immobilized on the nanoparticle surface. The initial FateDH concentration was further fine-tuned to understand the correlation between FateDH loading and the remaining CA activity (Figure 2b). After immobilization, all


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nanoparticles were rinsed with Milli-Q water for three times to remove the loosely attached enzymes prior to the activity assay. The presence of polydopamine on the CA-TiO2 NPs surface allows its nucleophilic reaction with amine groups in enzymes, resulting in a robust immobilization of FateDH onto the CA-TiO2 NPs surface via covalent bonds. The increase of FateDH loading on nanoparticle is observed with higher initial FateDH concentration, though FateDH can potentially block the substrate diffusion to/from the CA molecules encapsulate within the nanoparticles.20,45 Therefore, in this work, the multi-enzyme nanocascades prepared with 0.5 mg/mL FateDH was used for the subsequent study due to their high CA activity retention.

Figure 2. (a) XPS of the multi-enzyme cascade prepared with 0.5 mg/mL FateDH enzyme solution; (b) FateDH loading on the nanoparticles and the effect on the CA activity; (c) Activity


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comparison between immobilized and free enzymes; (d) Reaction mechanism of the multienzyme nanocascades.

For the multi-enzyme nanoparticles, the conversion of gaseous CO2 to liquid formic acid involves the initial hydration reaction of CO2 to carbonate ions catalysed by CA, followed by reduction reaction to formic acid catalysed by FateDH in an aqueous environment. Reduced nicotinamide adenine dinucleotide (NADH) is the terminal electron donor for the reduction reaction, and the formation of 1 mol of formic acid requires 1 mol NADH.46 The catalytic efficiency of the co-immobilized multi-enzyme nanocascade and the free enzyme mixture was carried out (Figure 2c). Surprisingly, the co-immobilized nanoparticles exhibit substantially higher NADH conversion compared with both free FateDH and FateDH/CA mixture. Normally, the loss of activity is expected after immobilization due to the potential enzyme deformation and reduced accessibility to the active sites.47 However, for the spatially co-immobilized nanoparticles, the diffusion distance for the carbonate ions can be reduced to the nanometer range. The efficient enzymatic assembly line can increase the local concentration of carbonate ions within the nanoparticle, and shift the reaction equilibrium to the product side (Figure 2d), while for the free multi-enzyme system the carbonate generated from CA need to diffuse through a much longer distance to react with FateDH. Similarly, the multi-enzyme nanocascade exhibits satisfactory storage stability (Figure S2b), with nearly 90 % activity retention after 20 days’ storage under room temperature, surpassing the free enzyme mixtures where only 50 % retention was observed. In terms of the reusability (Figure S2c), it relatively stabilizes after two testing cycles. The loss of initial activity can be reasoned from the nanoparticle aggregation as discussed above for the CA-TiO2 NPs.


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3.3 Janus membranes via single-sided PDA deposition Within a gas-liquid membrane contactor, a hydrophobic membrane should be applied to maintain a well-defined gas-liquid interface.7 However, enzyme immobilization on a hydrophobic support can lead to its denaturation caused by the interaction between the hydrophobic peptide chains and the surface,34 and the hydrophobic surface can limit the intimate contact between immobilized enzyme and liquid. In this work, a series of hydrophilic-hydrophobic Janus membranes were fabricated with single-sided polydopamine (PDA) and polypropyleneimine (PEI) deposition on hydrophobic porous polypropylene (PP) supports. The conjugate structures of PDA can interact with PP via the hydrophobic interactions to form a stable surface functional layer, which can further locally induce the bio-mineralization of the titania nanoparticles on membrane surface for in-situ nanocascade deposition. To achieve the single-sided PDA/PEI deposition, the hydrophobic PP membrane was floated on the PDA/PEI solution surface. Initially, the triple phase contact line formed on the membrane bottom surface, and then the membrane pores were slowly wetted by the deposition solution. As a result, the PDA/PEI modification depth can be adjusted with different deposition time.38 As shown in Figure 3a, the membranes gradually turn brown on the bottom side. Based on the SEM images (Figure 3b and Figure S3), the deposition of PDA/PEI has a negligible effect on the membrane porous structure, indicating the PDA/PEI functional layer is relatively thin.


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Figure 3. (a) Digital pictures of the PDA/PEI modified PP membrane with different deposition time; (b) SEM image of the modified PP membrane; and (c) Cross-sectional EDX of the modified PP membrane.

To investigate the PDA/PEI modification depth across the membrane, the membranes were immersed into silver nitrate solution for 12 h. The catechol groups on PDA can chelate Ag+ ions from solution, and subsequently reduce the ions to form Ag nanoparticles.38 Therefore, the Ag nanoparticle distribution can be regarded as an indicator of the PDA/PEI modification depth. As shown in Figure 3c, for the Janus membrane the modification depth gradually increases with longer deposition time: after 3 h modification, the hydrophilic section occupies around 40 % of the total membrane thickness (the total thickness of the PP membrane is ~150 µm). The most distinct property for Janus membranes is the anisotropic wettability on each side.36 The partial hydrophilization of a hydrophobic membrane can reduce the liquid penetration pressure, which is a crucial factor in maintaining a well-defined gas-liquid interface with membrane


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contactor. The detailed analysis and discussion of transient water contact angle, directional liquid transport and liquid penetration pressure can be found in the supporting information (Figure S4S5, Table S2 and Equation S1-S3). In this work, after 10 h of single-sided PDA/PEI modification, even though the spontaneous liquid transport has occurred from the other side, the Janus membrane can still maintain a 0.3 bar water penetration pressure from the PDA/PEI side. This is preferable for the membrane gas-liquid contactor as it can maintain a stable gas-liquid interface. However, with longer PDA/PEI deposition time, spontaneous wetting would occur on both sides of the membrane. It should be noted that the PDA/PEI coating had very minor effect on the membrane pore size. We also conducted the nitrogen gas permeation test to investigate the change of pore size before and after PDA/PEI modification. Due to the large pore size of the membrane, the feed pressure was maintained at 0.1 bar and the nitrogen permeation rate was monitored with a digital gas flow rate monitor. More detailed experimental procedures can be found in our previous publication.48 The PDA/PEI modified side faced the feed side during the test. As shown in Figure S6, the membrane pore size experienced very minor change after PDA/PEI deposition. 3.4 Immobilization of the multi-enzyme cascade on the Janus membrane Ideally, the nanocascade should be attached to the hydrophilic section of the Janus membrane to ensure an efficient mass transfer within a gas-liquid contactor. To achieve this, the CA-bearing biocatalytic membranes were firstly fabricated and optimized prior to the co-immobilization of FateDH. In this work, as shown in Figure 4a, the Janus membrane was floated onto the CA/TiBALDH sol solution with the hydrophilic side facing downwards, and four different CA immobilization solutions were compared, i.e. CA/Ti-BALDH, CA/Ti-BALDH with arginine,


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CA/Ti-BALDH with dopamine and CA/Ti-BALDH with both arginine and dopamine (Figure 4b). PDA/PEI surface functional layer can enrich the titania sol precursor on the membrane surface through the electrostatic interaction between positively charged amino groups and negatively charged titania acid. The functional layer can also locally concentrate CA due to the interaction between amine groups on the enzyme and the catechol groups on PDA. As a result, a sol-gel reaction can occur on the Janus membrane surface, and the formed titania nanoparticles can insitu encapsulate CA. To achieve an efficient CA immobilization on the membrane surface, the homogeneous nanoparticle nucleation within the bulk solution should be minimized. The addition of arginine in the solution can significantly reduce the apparent CA activity for the biocatalytic membrane. As a result, only the immobilization solutions without arginine were applied for further optimization.


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Figure 4. (a) Schematic diagram of the CA immobilization process onto the functionalized membrane surface; (b) Comparison of the CA-membrane activity prepared with different immobilization solutions (all membranes are subject to 6 h PDA/PEI deposition and 10 h CA/TiBALDH treatment); (c) Effect of the PDA/PEI deposition time on the membrane activity; (d) Effect of the PDA/PEI deposition time of the CA loading and activity recovery for the membrane prepared with CA/Ti-BALDH solution; (e) Effect of the CA/Ti-BALDH treatment time on the membrane activity; (f) Effect of the CA/Ti-BALDH treatment time of the CA loading and activity recovery for the membrane prepared with CA/Ti-BALDH solution.

We subsequently investigated the effect of PDA/PEI deposition time on the CA biocatalytic membrane performance. All the membrane samples were deposited with PDA/PEI for a fixed time and then followed by 6 h CA/Ti-BALDH solution treatment. As shown in Figure 4c, for both series of membranes, the membrane activities are initially increased and then plateaued. A slightly higher activity is observed with the CA/Ti-BALDH immobilization solution. It should be noted that the addition of dopamine within the immobilization solution can facilitate the


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homogeneous nucleation of nanoparticles, as suggested by the formation of orange suspension (Figure S7). The polymerization of dopamine can assist the attachment of biocatalytic nanoparticles onto the membrane surface, the benefit however can be compromised by the competitive formation of biocatalytic nanoparticles within the solution. In addition, this can also reduce the reproducibility of the biocatalytic membrane: as shown in Figure 4c, relatively large error bars are observed with the immobilization solution containing dopamine. In terms of the CA loading, only the membranes fabricated with CA/Ti-BALDH solution can provide reliable enzyme loading value due to the absence of nanoparticle formation within the solution. As shown in Figure 4d, longer PDA/PEI deposition time can lead to higher CA loading, which can be explained by the PDA/PEI layer can provide more anchor positions for nanoparticles. However, the nanoparticle immobilized deeply inside the membrane pores are less accessible by substrates during the activity assay process, leading to the reduced activity recovery. It should be noted that the CA activity recovery is higher than our previous work where CA was immobilized on titania functionalize membrane surface.39 In this work, the effect of the CA/Ti-BALDH treatment time was also studied for both series of membranes. All membranes were modified with 6 h PDA/PEI prior to the CA/Ti-BALDH treatment. Similarly, with longer CA/Ti-BALDH treatment time, the apparent activities of the membranes are gradually increased and then relatively plateaued, and higher activities are obtained with the membrane fabricated with CA/Ti-BALDH solution without dopamine (Figure 4e). The gradual deposition of CA-containing biocatalytic nanoparticles on the membrane can increase the nanoparticle coverage and subsequently enzyme loading (Figure 5a and Figure S8). However, the increased enzyme loading can be compromised by the aggregation of nanoparticles, leading the lower mass transfer efficiency and activity recovery (Figure 4f). In


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this work, due to their better controllability during the fabrication and higher apparent activity, the CA biocatalytic membrane fabricated with 10 h CA/Ti-BLADH solution (no dopamine/no arginine) was applied for the further study. We also investigated the storage stability and reusability of the CA containing biocatalytic membrane. As shown in Figure 5b-c, compared with the biocatalytic nanoparticles, the membranes experienced more significant loss of the activity during the test, which can be explained by the detachment of the biocatalytic nanoparticles from the membrane surface.

Figure 5. (a) SEM images of the membrane with different CA/Ti-BALDH treatment time; (b) Storage stability; and (c) Reusability for the CA-bearing biocatalytic membrane (6 h PDA/PEI and 10 h CA/Ti-BLADH.


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For the co-immobilization of FateDH, the CA containing membrane fabricated with CA/TiBALDH solution was further functionalized with dopamine by floating the membrane on a 2.5 mg/mL dopamine solution (pH 6.8) for 10 min, after which the membrane was transferred to FateDH solution surface for co-immobilization. With the increase of FateDH concentration within immobilization solution, the enzyme loading on membrane gradually increases, which is accompanied by the loss of CA activity (Figure 6a). It should be noted that the remaining CA activity ratios are lower compared to the multi-enzyme nanoparticles. The nanocascade on membrane surface can be less accessible by the substrates compared to its free form. It is worth to mention that the activity assay substrate, p-NPA, has a much larger molecule size compared to CO2, as a result, the immobilization of FateDH may have less negative effect on the CO2 mass transfer.7 In terms of the activity, similar to the multi-enzyme nanocascade nanoparticles, the membrane fabricated with 0.5 mg/mL FateDH enzyme solution also exhibits significantly higher NADH conversion compared with the free enzyme mixtures (Figure 6b). The improved activity is also originated from the spatially separated CA and FateDH on the membrane surface, which shifts the reaction equilibrium towards the product side. The membrane storage stability and reusability were further investigated (Figure S9), and the results are quite comparable to the multi-enzyme nanoparticles.


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Figure 6. (a) FateDH loading and remaining CA activity for the biocatalytic membranes; and (b) Activity of the multi-enzyme membranes.

3.5 Gas-liquid membrane contactor with the Janus biocatalytic membrane The schematic diagram of the gas-liquid membrane contactor is shown in Figure 7a. In order to maintain a low transmembrane pressure to prevent the liquid penetration, the average liquid side


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flow rate was maintained at a relatively low level (1.0 ml min-1, the corresponding Reynolds number Re≤200), indicating the liquid flow was in the laminar region. In terms of the gas side, under the testing conditions no gas permeation through the membrane was observed, indicating the membrane can effectively serve as a physical barrier/contactor separating two phases, rather than as a gas distributor generating gas bubbles to the liquid side. With the dissolution of CO2, the CO2 hydration rate gradually decreased due to the accumulated carbonated ions in the liquid phase (Figure S10). As a result, the accumulated CO2 hydration mass within the initial 30 min of reaction was applied as an indicator of the contactor efficiency. For the reactor containing FateDH, the formic acid conversion was calculated by the gross amount of formic acid divided by the gross amount of hydrated CO2 at 30 min. As shown in Figure 7b, without any enzyme both pristine (case 1) and Janus membrane (case 2) exhibit comparable CO2 hydration efficiency. Then the addition of free (case 3) or nanocascade particles (case 4) in the liquid solution can slightly promote the CO2 hydration rate for the Janus membrane. It should be noted that the formic acid conversion rate is much higher for the suspended nanocascades (case 4) when compared with the free enzyme mixture (case 3). The most substantial improvement was observed with the biocatalytic Janus membrane with immobilized nanocascades (case 6): the hydrated CO2 amount is 2.5 times higher compared with Janus membrane without any enzyme (case 2), and the formic acid conversion rate is 89%, suggesting nearly all the hydrated CO2 can effectively converse to formic acid. The biocatalytic Janus membrane also had almost two times higher CO2 hydration amount compared with the free enzyme mixture (case 3). This also align the activity results shown in Figure 6. The ultrahigh efficiency should be attributed to the Janus membrane configuration as well as the compartmentalization of the CA and FateDH enzymes. For the Janus membrane contactor, the immobilized enzymes on the hydrophilic side locate very


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closely to the gas-liquid interface, ensuring a highly efficient mass transfer. Therefore, CO2 can immediately react with CA and subsequently convert to formic acid after it enters the liquid phase. In this work, we also observed that the presence of FateDH enzyme on the Janus membrane can promote the CO2 hydration efficiency, possibly due to the conversion of carbonate ions to formic acid can promote the CO2 hydration reaction. The stability of the biocatalytic Janus membrane was also investigated by using the same membrane for eight cycles (Figure 7c). No obvious efficiency loss was observed.


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Figure 7. (a) Schematic diagram of the gas liquid contactor; (b) Comparison of performance with gas liquid contactors with different configurations; and (c) Reusability of the coimmobilized biocatalytic membrane in gas liquid membrane contactor.

4. Conclusion In this work, we fabricated a series efficient multi-enzyme cascade biocatalytic nanoparticles for CO2 hydration and conversion. They exhibited higher activity compared with free enzyme mixtures, indicating the effectiveness of the compartmentalization. After introducing a Janus membrane fabrication technique via PDA/PEI deposition, we have further demonstrated a novel and facile strategy to construct biomimetic Janus membranes for CO2 hydration and conversion. Biocatalytic nanoparticles containing two cascade enzymes can be immobilized on the hydrophilic side of the Janus membrane, allowing spatiotemporal control over the cascade reactions at the gas-liquid interface. The resultant biocatalytic membrane has 2.5 times higher CO2 hydration efficiency compared with pristine membrane when used in a gas liquid membrane contactor, and it can be reused for eight cycles without losing its efficiency. Our findings underline the intrinsic relationship of multi-enzyme cascade fabrication to the biocatalytic reactor design, and highlight the opportunities that Janus membrane can provide for bi-phase catalytic reaction. Through this work, we envision that the Janus membrane enzymatic cascade can be used for other bio- and chemical reactors, and its satisfactory stability can facilitate the application in industrial bi-phase catalytic processes.


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AUTHOR INFORMATION Corresponding Author *Dr. Jingwei Hou, [email protected] Present Addresses †The author’s current address is Nanoscience & Technology Division, Argonne National Laboratory, Lemont, IL, USA Author Contributions S.Gao, H-C. Yang, and J. Hou conceived this research. The manuscript was written through contributions of all authors. All authors have given approval to the final version of the manuscript. Funding Sources Australian Research Council's Discovery Projects funding scheme (DP150104485) Notes Any additional relevant notes should be placed here. ACKNOWLEDGMENT This research was supported under Australian Research Council's Discovery Projects funding scheme (DP150104485). Dr. Jingwei Hou also would like to acknowledge the MCTL Visiting Fellowship Program.


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SUPPORTING INFORMATION Supporting information is free of charge on the ACS Publication website. BET, FTIR and storage stability for the nanoparticles; SEM, dynamic contact angle, LEP, nitrogen permeance for the Janus membranes.

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