NADH-Free Electroenzymatic Reduction of CO2 by Conductive

Letter Cite This: ACS Catal. 2019, 9, 5584−5589

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NADH-Free Electroenzymatic Reduction of CO2 by Conductive Hydrogel-Conjugated Formate Dehydrogenase Su Keun Kuk,†,⊥ Krishnasamy Gopinath,§,⊥ Raushan K. Singh,§ Tae-Doo Kim,§ Youngjun Lee,§ Woo Seok Choi,† Jung-Kul Lee,*,§ and Chan Beum Park*,† †

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Department of Materials Science and Engineering, Korea Advanced Institute of Science and Technology, 335 Science Road, Daejeon 305-701, Republic of Korea § Department of Chemical Engineering, Konkuk University, 120 Neungdong-ro, Seoul 05029, Republic of Korea S Supporting Information *

ABSTRACT: The electrocatalytic reduction of CO2 under low overpotential and mild conditions using redox enzyme is a propitious route for carbon capture and conversion. Here, we report bioelectrocatalytic CO2 conversion to formate by conjugating a strongly CO2-reductive, W-containing formate dehydrogenase from Clostridium ljungdahlii (ClFDH) to conductive polyaniline (PANi) hydrogel. The ClFDH in the hybrid electrode successfully gained electrons directly from PANi and exhibited high capability for electroenzymatic conversion of CO2 to formate at low overpotential without NADH. We describe a potential electron-transfer pathway in the PANi-ClFDH bioelectrode on the basis of multiple spectroscopic analyses and a QM/MM-based computational study. The 3D-nanostructured PANi hydrogel facilitated rapid electron injection to the active site of ClFDH. In the absence of NADH, the PANi-ClFDH electrode showed stable CO2-to-formate transformation at an overpotential as low as 40 mV, with 1.42 μmol h−1 cm−2 conversion rate, 92.7% faradaic efficiency, and 976 h−1 turnover frequency. KEYWORDS: CO2 reduction, NADH-free biocatalysis, formate dehydrogenase, electrocatalysis, bioelectrode

G

They gain electrons through electron transfer from an electrode to iron−sulfur clusters and a buried metal active site in the enzymes and catalyze CO2 reduction in the absence of NADH. Such type of bioelectrocatalysis does not involve toxic chemical mediators that often cause efficiency losses during electron transfer and can operate in modest cathodic potential range not causing side reactions.15 Thus, the use of NADH-independent FDHs as an electrocatalyst can provide an ideal solution for addressing current issues in biocatalytic CO2 reduction. Nonetheless, the design of bioelectrodes for direct electron transfer to NADH-independent FDHs is still in its infancy, suffering from a low rate of interfacial electron transfer.16 To achieve robust bioelectrocatalytic CO2-toformate conversion, advanced design of 3D scaffold materials for enzyme immobilization and efficient direct electron transfer between FDH and an electrode is essential. Here, we report NADH-free, electroenzymatic CO 2 reduction using a W-containing FDH from Clostridium ljungdahlii (ClFDH) immobilized on a conductive polymer hydrogel electrode, as depicted in Scheme 1. As a scaffold material for efficient electron injection to ClFDH that

reen conversion of CO2 to chemical fuels has attracted huge attention because of global climate issues and energy concerns.1,2 Biocatalytic CO2 reduction is a promising route for CO2 conversion because of exceptional chemoselectivity and stereospecificity as well as high yield at ambient conditions.3−5 Among various redox enzymes, formate dehydrogenase (FDH) converts CO2 to formate by activating thermodynamically unfavorable CO 2 reduction process through the stabilization of intermediates via proton-coupled electron-transfer reactions.6−9 Most FDH applications for CO2 reduction have been made using nicotinamide adenine dinucleotide cofactor (NADH)-dependent FDHs, which were limited by drawbacks such as the high cost and instability of NADH, the need for additional electron mediators, and the efficiency loss due to multistep electron transfer.10,11 Therefore, it is highly desired to activate FDHs through electron transfer to the FDH rather than via hydride transfer from NADH. Direct electron injection to NADH-dependent FDHs consisting of only amino acids has been attempted, but the electron transfer from an electrode to the enzymes for formate production scarcely occurred.12 Recently, NADH-independent FDHs that contain an electro-active metal center such as W or Mo have been identified.13,14 The metal-containing FDHs are efficient electrocatalysts for CO2-to-formate conversion and require a low overpotential compared with other synthetic catalysts. © 2019 American Chemical Society

Received: January 11, 2019 Revised: April 21, 2019 Published: May 13, 2019 5584

DOI: 10.1021/acscatal.9b00127 ACS Catal. 2019, 9, 5584−5589

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ACS Catalysis

hydrogel electrode (geometric surface area: 1 cm2) using the dip-coating method (Figures S3b,c). The PANi hydrogel electrode exhibited a continuously connected, hierarchical 3D network of nanofibers with an average diameter of 60 nm (Figure S3d−e). The 3D nanostructure of PANi hydrogel exhibits a short electron diffusion length and effective electrontransfer network,20 which should accelerate the electroenzymatic reaction of the ClFDH. Furthermore, the nanostructure’s open channels allow for better contact with the enzyme and the efficient diffusion of substrates and products. We analyzed the chemical structure of the PANi hydrogel electrode using ATR-FTIR spectroscopy. The ATR-FTIR spectrum in Figure S4 shows two peaks associated with the stretching vibration of the quinoid ring (1580 cm−1) and benzenoid ring (1480 cm−1), which indicates that the PANi hydrogel is a highly conductive emeraldine salt (ES).21 The Brunauer−Emmett−Teller surface area of the PANi electrode was 1.23 m2·g−1, which was 12.3 times higher than that of the carbon cloth electrode (0.10 m2·g−1). To fabricate ClFDH immobilized PANi hydrogel electrode (PANi-ClFDH), we drop-casted ClFDH and used glutaraldehyde as a covalent cross-linking agent between the amine groups in the PANi hydrogel and ClFDH. The immobilization of ClFDH on the PANi electrode was confirmed by ICP-MS analysis. The enzyme density on the PANi-ClFDH electrode was approximately 1.46 nmol cm−2, which was 3.46 times higher than that of the carbon cloth electrode (0.42 nmol cm−2) because of the large surface area of the PANi hydrogel. We compared electrochemical properties of bare PANi and PANi-ClFDH electrodes in a CO2-saturated sodium phosphate buffer (pH 6.5, 50 mM bicarbonate; CO2 purged for 1 h) using PFV analysis. As displayed in the Region 1 of Figure 1a, bare

Scheme 1. Schematic Illustration of ClFDH-PANi Electrode and Direct Electron Transfer from Conductive PANi Hydrogel to ClFDH for Electroenzymatic CO2 Conversion to Formate

possesses high CO2-to-formate reduction activity, we employed a conductive 3D-structured polyaniline (PANi) hydrogel. We demonstrate that the PANi-ClFDH hybrid electrode allows efficient and stable formate production through enhanced enzyme loading and amplified electron injection to the metal center of ClFDH by PANi hydrogel in the absence of NADH. Furthermore, we verify the electron injection from PANi hydrogel to the electron-transfer regions inside ClFDH and suggest a possible electron-transfer pathway in the PANiClFDH. We produced ClFDH as a soluble recombinant enzyme by overexpressing a pET28(a)-clfdh plasmid according to the literature17 and observed a clear band at 79 kDa in the SDSPAGE analysis (Figure S1). Stoichiometric ICP-MS analysis revealed 1.28 ± 0.15 W per ClFDH subunit, indicating that ClFDH contains one W metal center per monomer. The apparent kcat/Km value of ClFDH for CO2 reduction was known to be 183 mM−1 s−1, the highest among all FDHs reported to date.17 For example, ClFDH exhibited a 3-order higher turnover rate (kcat) and 6-order higher catalytic efficiency (kcat/Km) than commercial Candida boidinii FDH (CbFDH)18 for CO2 reduction. To study interfacial electron transfer between ClFDH and the electrode, we employed protein film voltammetry (PFV). PFV analysis of ClFDH on carbon cloth in a CO2-saturated sodium phosphate buffer at pH 6.5 (50 mM bicarbonate; CO2 purged for 1 h) showed a −0.58 V (vs Ag/AgCl) reduction peak potential (Figure S2), which is nearly identical to the thermodynamic reduction potential of CO2 to formate (−0.56 V at pH 6.5).14 The low reduction peak potential implies that ClFDH can efficiently stabilize the CO2•− intermediate during CO2 reduction.19 The PFV wave increased with the driving force, which is a typical response from highly electrocatalytically active metal-dependent enzymes.13 In this case, the electrocatalytic rate is influenced by interfacial electron transfer between the electrode and FDH. This suggests that ClFDH was electrically activated without NADH for CO2 reduction. It is worth noting that no catalytic wave was observed in the absence of CO2 (under N2 purging). The kinetic and PFV analyses strongly suggest that the W-containing ClFDH is a suitable catalyst for CO2 reduction. We assembled CO2-to-formate converting bioelectrodes by immobilizing ClFDH on a conductive polyaniline (PANi) scaffold, as depicted in Figure S3a. We synthesized the PANi

Figure 1. (a) PFV scan comparison for the initial 3 cycles of the PANi and PANi-ClFDH electrodes in CO2-saturated sodium phosphate buffer (pH 6.5, 50 mM bicarbonate in a 100 mM of sodium phosphate buffer; CO2 purged for 1 h). The voltammetric scan rate is 25 mV s−1. (b) PFV scans of the PANi-ClFDH electrode depends on the scan rates (inset: dependence of the peak current on the square root of scan rate).

PANi electrode exhibited a broad peak around −0.1 V, which is the reduction peak of PANi from ES to leucoemeraldine base (LEB).22 After reduction to LEB, PANi becomes less conductive due to the decrease of conjugated units in semioxidized states (Region 1 of Figure S5a). This change caused the decline of current density of PANi electrode after PANi reduction peak potential and suppressed side reactions such as hydrogen evolution on PANi electrode.23 The presence of ClFDH on the PANi hydrogel induced a negative shift in the PANi reduction peak potential owing to the electronic interactions between PANi and ClFDH. In case of PANiClFDH, CO2 reduction initiated at approximately −0.53 V 5585

DOI: 10.1021/acscatal.9b00127 ACS Catal. 2019, 9, 5584−5589

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ACS Catalysis

donate electrons easily compared to quinoid imines;29 therefore, they can serve as a key site for electron injection to the electrically conductive ClFDH. Second, we analyzed the electronic interactions between PANi and ClFDH using UV−vis spectroscopy. For the analysis, we dispersed the PANi hydrogel in a 100 mM sodium phosphate buffer (pH 6.5) by sonication. The absorption spectrum of the PANi hydrogel exhibited two peaks at 446 nm (2.78 eV) and 820 nm (1.51 eV), which are associated with the electronic excitations of PANi emeraldine salt (Figure 2b).30 The emeraldine salt form of PANi has a half-filled polaron band due to the interactions between polarons in semioxidized states. The 820 nm (1.51 eV) and 446 nm (2.78 eV) peaks indicate the transitions from π band to polaron band and further to π* band, respectively,30 as shown in the inset of Figure 2b. The peak at 446 nm increased substantially in the presence of ClFDH. We infer that the significant increase stemmed from the depletion of electrons in the π* band that is due to electron transfer from PANi to ClFDH. The empty energy states of the π* band in PANi increase the probability of electron transition from the polaron band to the π* band; hence, the absorption peak of PANi at 446 nm increased after the incorporation of ClFDH. The evident changes to the UV−vis spectra suggest that the electrons in the high-energy state in PANi hydrogel can be directly transferred to ClFDH. Lastly, we investigated potential electron-transfer paths within ClFDH using the quantum mechanics/molecular mechanics (QM/MM) e-pathway method.31 Because a crystallographic structure of ClFDH is not available, we adopted the structure of the FDH from Escherichia coli (EcFDH) for the QM/MM e-pathway analysis. EcFDH is a good substitutional FDH for inferring the electron pathway in ClFDH because EcFDH shares a 60.3% sequence identity with ClFDH with a highly conserved active site and Fe4S4 cluster residues (Figure S11).32 We set PANi’s benzenoid amines as electron donors, the Mo active site as an acceptor, and Fe4S4 as a redox center that backfills electrons to the oxidized form of the Mo active site of EcFDH (Figure S12a−c). The electrontransfer regions for this calculation were defined with residues selected within a 12 Å vicinity around Fe4S4, including the surface region and the metal active site (Figure S12d). The defined electron-transfer region included 56 residues (Figure S12e and Table S1). We performed the QM/MM e-pathway calculation to locate key residues along the electron-transfer route and used spin density analysis to map the residues with the highest electron affinity molecular orbitals. According to our QM/MM e-pathway analysis, the benzenoid amines in the PANi hydrogel interact with Lys35 on the surface of the EcFDH and transfer electrons, as shown in Figure S13a. Merging all of the spin density surfaces on EcFDH provided a route that connected the surface to the metal active site in two steps. The first step connects the surface residue (Lys35) to Fe4S4, and the second step connects Fe4S4 to the oxidized Mo6+ (Figure S13b). In addition to the spin plot, we generated a HOMO plot to confirm the highest electron affinity molecular orbital along the electron-transfer pathway in EcFDH (Figure S13c). Considering that 78% of the residues in the transfer region of EcFDH in the QM/MM calculations were identical to those of ClFDH, we propose the following potential electron-transfer pathway inside ClFDH: electrons move through Arg36, Thr37, Asn38, Glu39, Ser41, and Leu42 to Fe4S4; then, the electrons at Fe4S4 are transferred to the

(Region 2 of Figure 1a and Figure S5b), indicating electron transfer from the PANi electrode to CO2 via ClFDH. The catalytic wave increased with the cathodic potential; the cathodic current density reached to peak current density (Ipc) of −3.02 mA cm−2 around −1.0 V within the PFV scan window. In contrast, no significant current increase was observed for CO2 reduction on the bare PANi electrode at up to −1.0 V. The persistence of the background current of PANi electrode in the PFV of PANi-ClFDH electrode reflects that ClFDH immobilized and acted as an electrocatalyst on the conductive PANi scaffold.22,24 Note that the use of Pt wire as a counter electrode did not affect the electrochemical measurements (Figure S6). We conducted a PFV analysis of PANiClFDH in the absence of CO2 as a control experiment and confirmed its much lower current density than in the CO2saturated case (Figure S7). These results imply that ClFDH obtains electrons from PANi, reducing the overpotential for CO2 reduction to formate. Figure 1b shows the dependence of PFVs on scan rates. With the increasing scan rate, Ipc increased in a near-perfect linear relationship with respect to the square root of the scan rates (Figure S8). The results demonstrate that the electron transfer in the PANi-ClFDH electrode is a diffusion-controlled process rather than a surface-controlled one.25 We further compared electrocatalytic activities of immobilized ClFDH (on PANi) and free ClFDH (near PANi). As shown in Figure S9, immobilized ClFDH showed a better current generation profile than free one. We estimated catalytic current (icat) of each bioelectrocatalytic system according to the literature.26 The PANi-ClFDH exhibited 1.8-times higher icat than free ClFDH, reflecting enzyme immobilization facilitates efficient electron injection to ClFDH. To explore the possible electron pathway in the PANiClFDH electrode, we probed each step of the electron transfer. First, we analyzed the changes to the PANi hydrogel’s molecular structure upon electron injection through electrical poling. The Raman spectra in Figure 2a show the decrease of

Figure 2. (a) Raman spectra of chemical structure variation of the PANi hydrogel electrode before and after electric polarization at −0.6 V (vsAg/AgCl). (b) UV−vis spectra of PANi and PANi with ClFDH (inset: band structures of emeraldine salt PANi).

peaks for quinoid imines (1475 cm−1, CN stretching in quinoid rings) and the increase of peaks for benzenoid amines (1338 cm−1, C−N stretching in benzenoid rings) after an hour-long electrical poling treatment at −0.6 V (vs Ag/AgCl). The result indicates that quinoid imines of PANi hydrogel were reduced to benzenoid amines after gaining electrons.27,28 Further analysis using ATR-FTIR spectroscopy confirmed the increase of benzenoid amine moieties in the PANi electrode (Figure S10). The benzenoid amines in PANi are known to 5586

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ACS Catalysis oxidized W6+ active site via Ala14, Ile182, His180, Ala178, and molybdopterin guanine dinucleotide (MGD) (Figure 3a).

result verifies that the Pt wire counter electrode did not affect the conversion of CO2 to formate in our study. The PANiClFDH electrode produced formate at a 9.43-fold faster rate than a ClFDH-adsorbed carbon cloth electrode (CC-ClFDH) did (Figures S18 and S19). Note that the amount of ClFDH immobilized on the PANi hydrogel was 3.46 times higher than that of CC-ClFDH. In addition, PANi-ClFDH exhibited 2.96fold higher TOF compared with CC-ClFDH (330 h−1). We attribute the high catalytic activity of the PANi-ClFDH electrode to efficient electron injection, facilitated by the nanostructured PANi network. The entrapment of ClFDH in the conductive 3D PANi hydrogel network should shorten the length of the charge transfer to the metal center of the enzyme, which will enhance electron tunneling processes in electron injection.33,34 To determine the effect of surface nanostructure of PANi electrode on electron injection, we estimated the amount of injected electrons per ClFDH by measuring the electron transfer (ET) rate according to the literature.35,36 The ET rate represents electron injection efficiency per enzyme on an electrode, which can be calculated on the basis of the amount of synthesized formate. At −0.6 V of applied voltage, the ET rate of PANi-ClFDH was 0.54 e− s−1 ClFDH−1, whereas that of CC-ClFDH was only 0.20 e− s−1 ClFDH−1, which indicates enhanced electron injection efficiency by the nanostructured PANi-based electrode. We further compared the PANi-ClFDH electrode’s catalytic performance with other NADH-independent FDH-conjugated electrodes (Table S2). The formate generation rate of PANiClFDH was higher than those of the recently reported direct electron-transfer-type bioelectrodes13,14 based on graphite pot electrode, and mediated electron-transfer-type bioelectrode16 using cobaltocene as an electron mediator. Taken together, the nanostructured PANi hydrogel scaffold amplified electron injection into the W-containing FDH for enhanced CO2-toformate converting performance. In summary, we have demonstrated bioelectrocatalytic CO2to-formate conversion through direct electron transfer from conductive hydrogel to ClFDH, a strongly CO2-reductive, Wcontaining FDH, in the absence of NADH. We developed an electroenzymatic platform by conjugating ClFDH to a conductive PANi hydrogel. The conductive 3D nanostructured PANi hydrogel allowed for efficient electron injection to ClFDH. Not relying on NADH, the PANi-ClFDH electrode exhibited robust CO2 reduction by showing prolonged current density at low overpotential. We suggested a possible electrontransfer path in the PANi-ClFDH based on multiple spectroscopic analyses and a QM/MM-based computational study. The PANi-ClFDH electrode generated formate at a rate of 1.42 μmol h−1 cm−2 under −0.6 V bias (40 mV of overpotential), with a faradaic efficiency of 92.7% and a TOF of 976 h−1. Our study provides the basis toward highperformance, cofactor-free FDH electrochemistry, relevant for electroenzymatic conversion of CO2 to value-added chemicals.

Figure 3. (a) Illustration of expected electron-transfer pathway in ClFDH from surface residue to W6+ through Fe4S4 cluster. (b) Relative electron-transfer rate of ClFDH wild-type and mutants (R36A and R36D).

We experimentally validated the mapped possible electrontransfer pathway from PANi to the ClFDH residues through site-directed mutagenesis. Upon mutagenesis of surface residue Arg36 to Ala36 and Asp36, the ClFDH almost lost its catalytic activity (data not shown). Additionally, we found that the electron-transfer rate of mutant ClFDHs decreased significantly to 43.2% (for Ala36) and 32.1% (for Asp36) compared with wild-type ClFDH (Figure 3b). Likewise, we confirmed the electron-transfer pathway in EcFDH by mutagenesis experiments and observed similar losses of catalytic activity and the decrease of electron-transfer rate (Figure S14). These results support our QM/MM e-pathway analyses about FDHs. Upon the application of an electrical bias, the electrons of benzenoid amines at high-energy state in the PANi hydrogel are injected to the W-active center of ClFDH through the surface residue Arg36 and Fe4S4. Overall, our spectroscopic and computational analyses suggest the possible electron transfer in the PANi-ClFDH electrode. We analyzed the CO2-to-formate converting capacity of the PANi-ClFDH electrode at different applied voltages (vs Ag/ AgCl). The PANi-ClFDH successfully converted CO2 to formate during 12 h reactions (Figures 4a, S15, and S16). At −0.6 V (i.e., 40 mV overpotential), formate was produced at a rate of 1.42 μmol h−1 cm−2, with a turnover frequency (TOF) of 976 h−1 and a faradaic efficiency of 92.7%. During the reaction, Pt did not adsorb on the PANi-ClFDH electrode (Figure S17). Furthermore, formate was not detected at all in the absence of ClFDH or CO2, as shown in Figure 4b. The

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ASSOCIATED CONTENT

S Supporting Information *

Figure 4. (a) Effect of applied voltage on formate generation rate and faradaic efficiency by PANi-ClFDH electrode. Conditions: pH 6.5, 50 mM bicarbonate in a 100 mM of sodium phosphate buffer; CO2 purged for 1 h. (b) Control experiments of PANi-ClFDH electrode under −0.6 V applied bias (vs Ag/AgCl, i.e., 40 mV overpotential) for 12 h.

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acscatal.9b00127. Experimental procedures, supporting figures, and supporting tables (PDF) 5587

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AUTHOR INFORMATION

Corresponding Authors

*E-mail: [email protected]. *E-mail: [email protected]. ORCID

Jung-Kul Lee: 0000-0001-7384-5301 Chan Beum Park: 0000-0002-0767-8629 Author Contributions ⊥

S.K.K. and K.G. contributed equally to this work.

Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This work was supported by the National Research Foundation (NRF) via the Basic Science Research Program (NRF-2017R1A2B3011676) and the Creative Research Initiative Center (NRF-2015 R1A3A2066191), Republic of Korea.

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DOI: 10.1021/acscatal.9b00127 ACS Catal. 2019, 9, 5584−5589

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ACS Catalysis (30) Xia, Y. N.; Wiesinger, J. M.; Macdiarmid, A. G.; Epstein, A. J. Camphorsulfonic Acid Fully Doped Polyaniline Emeraldine Salt Conformations in Different Solvents Studied by an Ultraviolet-Visible near-Infrared Spectroscopic Method. Chem. Mater. 1995, 7, 443−445. (31) Lucas, M. F.; Rousseau, D. L.; Guallar, V. Electron Transfer Pathways in Cytochrome c Oxidase. Biochim. Biophys. Acta, Bioenerg. 2011, 1807, 1305−1313. (32) Boyington, J. C.; Gladyshev, V. N.; Khangulov, S. V.; Stadtman, T. C.; Sun, P. D. Crystal Structure of Formate Dehydrogenase H: Catalysis Involving Mo, Molybdopterin, Selenocysteine, and an Fe4S4 Cluster. Science 1997, 275, 1305−1308. (33) Ueda, A.; Kato, D.; Kurita, R.; Kamata, T.; Inokuchi, H.; Umemura, S.; Hirono, S.; Niwa, O. Direct Electron Transfer with Enzyme on a Nanostructured Carbon Film Fabricated with a Maskless Top-Down UV/Ozone Process. J. Am. Chem. Soc. 2011, 133, 4840−4846. (34) de Poulpiquet, A.; Ciaccafava, A.; Lojou, E. New Trends in Enzyme Immobilization at Nanostructured Interfaces for Efficient Electrocatalysis in Biofuel Cells. Electrochim. Acta 2014, 126, 104− 114. (35) Kothe, T.; Poller, S.; Zhao, F. Y.; Fortgang, P.; Rogner, M.; Schuhmann, W.; Plumere, N. Engineered Electron-Transfer Chain in Photosystem 1 Based Photocathodes Outperforms Electron-Transfer Rates in Natural Photosynthesis. Chem. - Eur. J. 2014, 20, 11029− 11034. (36) Lubner, C. E.; Applegate, A. M.; Knorzer, P.; Ganago, A.; Bryant, D. A.; Happe, T.; Golbeck, J. H. Solar Hydrogen-Producing Bionanodevice Outperforms Natural Photosynthesis. Proc. Natl. Acad. Sci. U. S. A. 2011, 108, 20988−20991.

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DOI: 10.1021/acscatal.9b00127 ACS Catal. 2019, 9, 5584−5589