CO2 Photoreduction by Formate Dehydrogenase and a Ru-Complex

Jan 10, 2017 - (c) Ru(bpy)32+ (photosensitizer), MV2+ (electron mediator), and FDH immobilized in PGP50, where efficient formic acid production takes ...
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CO2 Photoreduction by Formate Dehydrogenase and a Ru-Complex in a Nanoporous Glass Reactor Tomoyasu Noji,*,† Tetsuro Jin,‡ Mamoru Nango,†,§ Nobuo Kamiya,† and Yutaka Amao† †

The OCU Advanced Research Institute for Natural Science & Technology (OCARINA), Osaka City University, 3-3-138 Sugimoto, Sumiyoshi-ku, Osaka 558-8585, Japan ‡ Inorganic Functional Materials Research Institute, National Institute of Advanced Industrial Science and Technology (AIST), 1-8-31, Midorigaoka, Ikeda, Osaka 563-8577, Japan § Monozukuri Research Center, Nagoya Institute of Technology, Gokiso-cho, Showa-ku, Nagoya 466-8555, Japan S Supporting Information *

ABSTRACT: In this study, we demonstrated the conversion of CO2 to formic acid under ambient conditions in a photoreduction nanoporous reactor using a photosensitizer, methyl viologen (MV2+), and formate dehydrogenase (FDH). The overall efficiency of this reactor was 14 times higher than that of the equivalent solution. The accumulation rate of formic acid in the nanopores of 50 nm is 83 times faster than that in the equivalent solution. Thus, this CO2 photoreduction nanoporous glass reactor will be useful as an artificial photosynthesis system that converts CO2 to fuel.

KEYWORDS: artificial photosynthesis, nanoporous glass, light-driven formic acid production, solar fuel, ambient conditions

C

light-driven formic acid production system. It is very difficult to only extract formic acid from homogeneous photoreaction solutions containing these ternary redox components. However, there are few reports of reactor systems with immobilized ternary redox components. To solve this problem, we employed porous glass plates (PGPs) in this study as a photoreaction platform for immobilizing the ternary redox components. PGPs are transparent in the visible-NIR region, and have nanopores that penetrate the plates (Figure 1a, b).23−25 Interestingly, the reaction efficiency of a photoreaction system immobilized densely inside the nanopores can increase relative to that of the same photoreaction system in homogeneous solution. For example, the efficiency of the light-induced hydrogen evolution of a device using a PGP with an inner nanopore diameter of 50 nm (PGP50) was 3000 times higher than that of a homogeneous solution system under aerobic conditions.23 The light-induced hydrogen production device was constructed by introducing Ru(bpy)32+/MV2+/ hydrogenase into the nanopores inside PGP50 (Ru(bpy)32+/ MV2+/hydrogenase/PGP50).23 This drastic improvement of the conversion efficiency is caused by the dense accumulation of MV•+ in the nanopores. It is expected that production obtained from a reactor system using PGP50 will be changed to

O2 photoreduction to produce fuel and organic matter has been attracting attention as a strategy for artificial photosystems, which are necessary to realize a sustainable energy society.1−6 To synthesize fuel or organic matter from CO2, various semiconductors, metal-complexes, and solid catalysts have been previously developed.4−10 However, there is room for improvement of the substrate/product specificities of artificial catalysts and conversion efficiencies under ambient pressure/temperature and moderate pH.7,8 Shifting away from specific organic solvents and rare metals that have costs for practical applications is also required.7−10 Interestingly, formate dehydrogenase (FDH), as is an enzyme that can reduce CO2 to formic acid at ordinary temperatures, pressures, and moderate pH with high substrate/product specificities and without a specific solvent or rare metals.11−13 Turnover numbers of up to 6 × 105,14 have been reported for the FDH enzyme. Formic acid is a possible substrate for hydrogen and methanol as fuel.1,2 Therefore, hybrid systems that combine a photosensitizer with FDH have attracted attention as a useful strategy for artificial photosynthesis to convert CO2 to fuel.1,2,13,15−22 Previously, various light-driven formic acid production systems using FDH and the reduced form of methyl viologen (MV•+) as an artificial coenzyme that can be photoreduced by a photosensitizer have been reported.1,17−22 Because MV•+ (and reduced forms of MV derivatives) suppresses the reverse reaction from formic acid to CO2 via FDH,11−13 the ternary redox components (photosensitizer/MV2+/FDH) are a useful © 2017 American Chemical Society

Received: October 7, 2016 Accepted: January 10, 2017 Published: January 10, 2017 3260

DOI: 10.1021/acsami.6b12744 ACS Appl. Mater. Interfaces 2017, 9, 3260−3265

Letter

ACS Applied Materials & Interfaces

mM, 53.9 ± 0.7 mM, and 0.36 ± 0.04 mM (with considering the heterogonous distribution of FDH in nanopores), respectively, corresponding to 18-fold, 18-fold, and 9-fold increases relative to those in the solutions before adsorption. This result suggests that a densely packed light-induced formic acid production system was constructed in the nanopores inside PGP50. Figure 2 shows the light-induced formic acid production per unit of light-receiving area of Ru(bpy)32+/MV2+/FDH/PGP50

Figure 1. Light-induced formic acid production in nanopores. (a) Photographic image of a leaf and Ru(bpy)32+/MV2+/formate dehydrogenase (FDH)-immobilized PGP with nanopores of 50 nm. Scale bar: 5 mm. (b) Schematic of a porous glass plate (PGP) with a nanopore diameter of 50 nm (PGP50). (c) Ru(bpy)32+ (photosensitizer), MV2+ (electron mediator), and FDH immobilized in PGP50, where efficient formic acid production takes place via sequential electron transfer by the redox components.

Figure 2. Time evolution of light-induced formic acid production by Ru(bpy)32+/MV2+/FDH/PGP50 (●) in medium B (0.1 M MESNaOH (pH 6.6), 20 mM EDTA, and 24 mM NaHCO3) and the Ru(bpy)32+/MV2+/FDH solution (■) consisting of medium B containing 0.5 mM Ru(bpy)32+, 3 mM MV2+, and 41 μM FDH. The amounts of Ru(bpy)32+, MV2+, and FDH inside PGP50 are described in the text.

formic acid from hydrogen by immobilizing FDH instead of hydrogenase in PGP50. Herein, we developed a new reactor device, which efficiently accumulates formic acid in comparison with the solution system, by immobilizing the Ru-complex and MV together with FDH in the nanopores inside PGP50 (Figure 1c). Because FDH has a molecular size of about 15 nm,26 it is a sufficiently small protein to penetrate the 50 nm nanopores of PGP50. The size of the nanopores of PGP were regulated to 50 nm by acid leaching of phase-separated borosilicate glass. The synthesized PGP50 was characterized according to previously reported methods (see the Supporting Information).23−25 FDH was immobilized in the nanopores inside PGP50 by immersing PGP50 in a solution containing FDH. Then, Ru(bpy)32+ and MV2+ were immobilized in the nanopores inside PGP50 by immersing FDH-immobilized PGP50 in a solution containing Ru(bpy)32+ and MV2+. The resulting PGP50 with Ru(bpy)32+, MV2+, and FDH immobilized in the nanopores (Ru(bpy)32+/ MV2+/FDH/PGP50) was rinsed. The amounts of Ru(bpy)32+ and MV2+ immobilized in PGP50 were determined to be 3.0 ± 0.1 μmol/g PGP50 and 17.4 ± 0.2 μmol/g PGP50, respectively, from the absorbance of the soaking solution before and after the adsorption procedure using previously reported methods.23 The amount of immobilized FDH was 69 ± 8 nmol/g, as determined from the absorbance of the soaking solution at 280 nm before and after the adsorption procedure (Figure S1). The distribution of FDH inside PGP50 was investigated by measuring the fluorescence of rhodaminelabeled FDH (Rh-FDH) using confocal laser scanning microscopy (see the Supporting Information). The crosssectional profiles of the fluorescence intensity clearly showed that FDH was preferentially adsorbed within a depth of ∼0.3 mm from the surfaces of PGP50 that has a total thickness of 1 mm (Figurse S2 and S3). The concentrations of Ru(bpy)32+, MV2+, and FDH in the nanopores inside PGP50 were 9.3 ± 0.2

and the Ru(bpy)32+/MV2+/FDH solution. The light-induced formic acid production without FDH was subtracted (see the SI). Ru(bpy)32+/MV2+/FDH/PGP50 showed significant production of formic acid (Figure 2 (●) and Table 1, Entry 1), which was 9 times higher than that in the Ru(bpy)32+/MV2+/ FDH solution after 3 h of irradiation (Figure 2 (■) and Table 1, Entry 2). The light-induced formic acid production efficiency of Ru(bpy)32+/MV2+/FDH/PGP50 (1.4 ± 0.6 μmol HCOOH/ (m2 s); conversion efficiency, (22 ± 9) × 10−2%; Table 1, Entry Table 1. Rate of Formic Acid Production of Ru(bpy)32+/ MV2+/FDH/PGP50 and Ru(bpy)32+/MV2+/FDH Solution entry a

1 2b 3c

photoreaction system Ru(bpy)32+/MV2+/FDH/PGP50 Ru(bpy)32+/MV2+/FDH solution Ru(bpy)32+/MV2+/hydrogenase/ d PGP50 under aerobic conditions

production

conversion efficiency, φ (× 10−2%)

HCOOH HCOOH H2

22 ± 9e 1.6 ± 0.9e 19 ± 1c

a

Reaction medium composition: medium B (0.1 M MES-NaOH (pH 6.6), 20 mM EDTA·2Na, and 24 mM NaHCO3); reaction volume, 4.4 mL; amount of Ru(bpy)32+/MV2+/FDH/PGP50, 66 mg; area receiving sunlight, 9.7 cm2/g PGP50; PGP50 thickness, 1 mm. b Reaction medium composition: medium B containing 0.5 mM Ru(bpy)32+, 3 mM MV2+, and 41 μM FDH; reaction volume, 0.65 mL in a quartz cell with a 2 mm path length; area receiving sunlight, 5 cm2/mL solution. cEntry 3 corresponds to Entry 5 in Table S1 of ref 23. PGP50 thickness, 1 mm. dRu(bpy)32+/MV2+/hydrogenase/PGP50 is PGP50 adsorbed Ru(bpy)32+, MV2+, and hydrogenase in the nanopores. eφ = 2 × [formic acid production rate (μmol HCOOH/ (m2 s))]/[photon flux density (μmol/(m2 s))]. The photon flux density within the wavelength range of 400−700 nm was 1300 μmol/ (m2 s) (Figure S4). 3261

DOI: 10.1021/acsami.6b12744 ACS Appl. Mater. Interfaces 2017, 9, 3260−3265

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Figure 3. Enhancement mechanism for light-driven formic acid production in the (a) Ru(bpy)32+/MV2+/FDH solution compared with (b) Ru(bpy)32+/MV2+/FDH/PGP50. Although the accumulation rates of MV•+ production in the Ru(bpy)32+/MV2+/FDH solution and Ru(bpy)32+/ MV2+/FDH/PGP50 are ∼1.5% and ∼1% of the photon flux density of a solar simulator within the 400−700 nm wavelength range, respectively, the accumulation rates of MV•+ are 36 and 140 mM/h, respectively. The dense accumulation and stabilization of MV•+ in the nanopores inside PGP50 results in a CO2 reduction efficiency that is 22 times greater than that of the RMF solution. Thus, the light-driven formic acid conversion efficacy of Ru(bpy)32+/MV2+/FDH/PGP50 is 14 times higher than that of the Ru(bpy)32+/MV2+/FDH solution.

1) was 14 times higher than that in the Ru(bpy)32+/MV2+/ FDH solution (0.10 ± 0.06 μmol HCOOH/(m2 s); conversion efficiency, (1.6 ± 0.9) × 10−2%; Table 1, Entry 2). This result suggests that Ru(bpy)32+/MV2+/FDH/PGP50 is a useful reactor device that can exceed the maximum conversion efficiency of solution systems. In the absence of NaHCO3 as a source of CO2, neither Ru(bpy)32+/MV2+/FDH/PGP50 nor the Ru(bpy)32+/MV2+/FDH solution achieved light-induced formic acid production (Figure S5). This result indicates that the formic acid production under irradiation in the presence of NaHCO3 occurred by photoreduction of CO2, which was supplied to the nanopores from the outer medium as dissolved CO2 and HCO3−, via FDH. This results also indicated that oxidation products of EDTA did not influence CO2 source and detection of formic acid. Previously, sacrificial reagents, such as EDTA, were found to be supplied to the nanopores from the outer medium.23 These facts indicate that Ru(bpy)32+/MV2+/ FDH/PGP50 could be incorporated into a flow system that supplies sacrificial reagents as electron donors and CO2. The maximum accumulation rate of formic acid in the nanopores inside PGP50 before diffusing to the outer solution was determined to be 15 ± 7 mM HCOOH/h (estimation methods described in the Supporting Information and Figure 3a), which was at least 83 times higher than that of the Ru(bpy)32+/MV2+/FDH solution (0.18 mM HCOOH/h, see the Supporting Information and Figure 3b). Thus, Ru(bpy)32+/ MV2+/FDH/PGP50, which can densely accumulate formic acid in nanopores, is a useful reactor device. The reaction efficiencies of each elementary step were calculated to investigate the enhancement mechanism for Ru(bpy)32+/MV2+/FDH/PGP50 compared with the Ru(bpy)32+/MV2+/FDH solution and the rate-limiting step (calculation methods are descried in the SI). Figure 3a and b show the reaction efficiencies of each elementary step for the Ru(bpy)32+/MV2+/FDH solution and Ru(bpy)32+/MV2+/ FDH/PGP50, respectively. The accumulation efficiencies of MV•+ with respect to photon flux density for the Ru(bpy)32+/

MV2+/FDH solution and Ru(bpy)32+/MV2+/FDH/PGP50 were ∼1.5% and ∼1%, respectively, from previously reported results (see the Supporting Information).23 These results indicate that the accumulation rate of MV•+ per unit area of Ru(bpy)32+/MV2+/FDH/PGP50 is comparable to that in the Ru(bpy)32+/MV2+/FDH solution. Taking into account the pore volume of PGP50, the accumulation rate of MV•+ in the nanopores inside PGP50 was 140 mM MV•+/h (Figure 3b), which was about 4 times that in solution (36 mM MV•+/h, see the Supporting Information and Figure 3a), indicating that MV•+ is densely and effectively accumulated in the nanopores inside PGP. The accumulation rate of MV•+ of a solution system with the same concentrations of Ru(bpy)32+ and MV2+ to those in the nanopores, was 14 mM MV+•/h, which corresponds to 39% of that of the solution system shown in Figure 3a (data not shown). The accumulation rate of MV•+ concentration was decreased despite with increasing Ru(bpy)32+ and MV2+ concentration. This phenomena is occurred in significantly high Ru(bpy)32+ concentration range. For example, the accumulation rate of MV•+ of a solution system containing 3 mM MV2+ was increased together with Ru(bpy)32+ concentration in the lower Ru(bpy)32+ concentration range until 0.5 mM Ru(bpy)32+, was saturated at about 0.5 mM Ru(bpy)32+, and was gradually decreased in the higher concentration range of more than 0.5 mM Ru(bpy)32+ (data not shown). Absorbance at 453 nm (corresponding to the peak of absorbance band of metal-to-ligand charge transfer of Ru(bpy)32+) of the solution system containing 9.3 mM Ru(bpy)32+ was about 30 with a 2 mm path length. Because significantly high absorbance due to high Ru(bpy) 3 2+ concentration seems to inhibit photoexcitation of Ru(bpy)32+ (self-light-shielding effect), the accumulation rate of MV•+ is decreased in the higher concentration range of more than 0.5 mM Ru(bpy)32+. On the other hand, absorbance at 453 nm of Ru(bpy)32+/MV2+/FDH/PGP50 is about 4 because physical appearance concentration is 3.1 mM Ru(bpy)32+ with considering the thickness of PGP50 is 1 mm (see the 3262

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conversion efficiency of light-induced formic acid production using Ru(bpy)32+/MV2+/FDH/PGP50 was comparable to that of Ru(bpy)32+/MV2+/hydrogenase/PGP50 under aerobic conditions ((19 ± 1) × 10−2%; Table 1, Entry 3).23 The ratelimiting step of Ru(bpy)32+/MV2+/hydrogenase/PGP50 was also light-induced charge separation between Ru(bpy)32+ and MV2+.23 These facts indicate that the solar-fuel conversion efficiency of such PGP50 systems would be increased by improving the charge separation yield between the photosensitizer and electron mediator. Furthermore, extending the absorbance of the photosensitizer is also required to improve the conversion efficiency, as Ru(bpy)32+ can only absorb 33% of the light emitted by a solar simulator in the visible region (400−700 nm) (see the Supporting Information). For example, high-efficiency light-driven formic acid production will be achieved by using photosensitizers (zinc tetrakis(4methylpyridyl)porphyrin20 or chlorophyll-a19) that absorb more in the visible region than Ru(bpy)32+. The electron transfer efficiency from MV2+ to FDH will also be improved by using MV2+ derivatives with high affinity for FDH, resulting in an enhanced formic acid production rate.12,13 Turnover number of FDH in nanopores was at least 120 mol HCOOH/mol FDH until irradiation for 3 h. The light-driven formic acid production of the PGP system was stably continued after 3 h (data not shown). This result indicated that FDH was stably reacted in nanopores inside PGP. There is room for improvement of FDH stabilization by a genetic and chemical modifications of FDH applicable to the environment in nanopores inside PGP, and chemical modification of the nanopores inside PGP. Such counterplan will be worked out based on understanding the denaturation mechanism of FDH. In this study, a nanoporous glass reactor with enhanced efficiency for the photoreduction of CO2 to formic acid was developed. This enhancement caused by the dense threedimensional immobilization of the photosensitizer, MV, and FDH in the nanopores inside PGP is expected to be applicable to multiple-step catalytic reactions that use formic acid as the substrate, if the appropriate enzyme/catalyst is immobilized in the nanopores. For instance, alcohol (methanol and ethanol) as a solar fuel are synthesized from organic acid via aldehyde dehydrogenase (AldDH) and alcohol dehydrogenase (ADH)1,2,29,30 by reduction of organic acid to aldehyde and aldehyde to alcohol, respectively, using MV•+ as an artificial coenzyme.1,30 It has been reported that the efficiency of chemical conversion from CO2 to methanol using FDH, AldDH, and ADH was improved by immobilizing these enzymes in a silica sol−gel matrix.29 Therefore, Ru(bpy)32+/ MV2+/FDH/PGP50 may be developed as a light-induced methanol production reactor by immobilizing AldDH and ADH. Moreover, if this system is able to use electrons from light-induced water splitting reactions, similar to photosystem II-immobilized devices,27 Ru(bpy)32+/MV2+/FDH/PGP50 may be useful for developing an artificial photosynthesis system that can extract electrons from water to reduce CO2.

Supporting Information). If an effective light-pass length of PGP50 is regarded to be 0.33 mm, a physical appearance concentration is corresponding to the concentration in nanopores (detail explanation was described in the Supporting Information). Therefore, the photoreaction with 3 times the physical appearance concentration can be carried out in nanopores with mitigating the self-light-shilding effect to 33% of Ru(bpy) 3 2+ concentration in nanopores. Thus, the accumulation rate of MV•+ concentration inside the nanopores is faster than that in the Ru(bpy)32+/MV2+/FDH solution shown in Figure 3a and a solution system with concentrations mimicked those in nanopores, although the overall accumulation rate of the amount of MV•+ is similar to the solution system shown in Figure 3a. This fact indicates that the electron transfer efficiency from MV•+ to FDH is accelerated in the nanopores inside PGP50 compared with that in the Ru(bpy)32+/MV2+/FDH solution. The conversion efficiencies from MV•+ to formic acid in the Ru(bpy)32+/MV2+/FDH solution and Ru(bpy)32+/MV2+/ FDH/PGP50 were 1% and 22%, respectively (see the Supporting Information and Figure 3a, b). This result clearly suggests that the overall light-driven formic acid production efficiency of Ru(bpy)32+/MV2+/FDH/PGP50 was improved compared with that of the Ru(bpy)32+/MV2+/FDH solution because the electron transfer efficiency from MV•+ to FDH increased 22-fold. In other words, the PGP system was able to increase the rate of the process that was rate limiting in the Ru(bpy)32+/MV2+/FDH solution. In the nanopores inside Ru(bpy)32+/MV2+/FDH/PGP50, MV•+ accumulated 4 times faster than in the Ru(bpy)32+/ MV2+/FDH solution, and the FDH concentration was 9-fold that in the Ru(bpy)32+/MV2+/FDH solution. The collisional reaction between MV•+ and FDH may be accelerated in the narrow nanopores compared with that in the Ru(bpy)32+/ MV2+/FDH solution because there is a high density of substrate and enzyme in the nanopores. For example, the photoreduction rate of an electron acceptor by photosystem II in nanopores inside PGPs was 16 times higher than that in the solution system because of the high density of photosystem II and the electron acceptor in the nanopores.27 Furthermore, MV•+ in the central region inside PGP is hardly oxidized because the accumulation rate of MV•+ is faster than the inflow velocity of dissolved oxygen from the outer solution into the nanopores.23 Even if oxygen enters the nanopores, MV•+ near the surface of the plate reduces oxygen to reactive oxygen species (ROS).23,28 As a consequence, the oxygen concentration in the central region inside PGP is significantly low,23,28 and CO2 photoreduction via FDH occurs further away from the plate surfaces (Figure S6). Moreover, it has been reported that the formic acid production activity of FDH is about 20 times higher when the reduced form of methyl viologen (MV•+) is employed as an artificial coenzyme than when nicotinamide adenine dinucleotide (NADH) is employed as a natural coenzyme because the reverse reaction is suppressed.11−13 Because of the dense immobilization of FDH, dense and effective accumulation and stabilization of MV•+ inside the nanopores, as well as suppression of the reverse reaction of FDH using MV•+, the electron transfer efficiency from MV•+ to CO2 via FDH in Ru(bpy)32+/MV2+/FDH/PGP50 is greater than that in the Ru(bpy)32+/MV2+/FDH solution. The light-induced charge separation (∼1% (MV•+/photon)) between Ru(bpy)32+ and MV2+ is the rate-limiting step in Ru(bpy)32+/MV2+/FDH/PGP50 (Figure 3b). The overall

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ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acsami.6b12744. Experimental details, estimations, Figures S1−S6 (PDF) 3263

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AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]. ORCID

Tomoyasu Noji: 0000-0001-9468-2038 Nobuo Kamiya: 0000-0002-9056-7558 Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS T.N. thanks the Takahashi Industrial and Economic Research Foundation, the Koyanagi Foundation, the Iwatani Naoji Foundation, the Japan Prize Foundation, and the Strategic Research Grant-in-Aid for Young Scientists at Osaka City University for funding. M.N. thanks AOARD for funding. This work was partially supported by a Grant-in-Aid for Scientific Research on Innovative Areas “Artificial photosynthesis (AnApple)” (No. 2406) from the Japan Society for the Promotion of Science (JSPS). We thank Professors Takehisa Dewa and Masaharu Kondo for assistance with the measurements of Rh-FDH immobilized in PGP50 using confocal laser scanning microscopy.

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DOI: 10.1021/acsami.6b12744 ACS Appl. Mater. Interfaces 2017, 9, 3260−3265

Letter

ACS Applied Materials & Interfaces

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NOTE ADDED AFTER ASAP PUBLICATION This paper was published on the Web on January 17, 2017. An additional affiliation was added to the paper, and the corrected version was reposted on January 20, 2017.

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DOI: 10.1021/acsami.6b12744 ACS Appl. Mater. Interfaces 2017, 9, 3260−3265