Enzyme Mediated Increase in Methanol Production from

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Enzyme Mediated Increase in Methanol Production from Photoelectrochemical Cells and CO2 Ke Ma, Omer Yehezkeli, Eunsol Park, and Jennifer N. Cha ACS Catal., Just Accepted Manuscript • DOI: 10.1021/acscatal.6b02524 • Publication Date (Web): 06 Sep 2016 Downloaded from http://pubs.acs.org on September 15, 2016

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Enzyme Mediated Increase in Methanol Production from Photoelectrochemical Cells and CO2 Ke Maa, Omer Yehezkelia, Eunsol Parkb, Jennifer N. Cha*,a,c. a

Department of Chemical and Biological Engineering, bChemistry and Biochemistry and

c

Materials Science and Engineering Program, University of Colorado, Boulder, Boulder, CO,

80309

ABSTRACT: While success has been shown in utilizing photocatalytic systems to reduce CO2 in water, most of these studies have yielded formic acid as the majority product with trace amounts of formaldehyde or methanol. One reason for this is the strong equilibrium of formaldehyde toward the hydrate methanediol. To increase methanol yields from CO2, we show here the combined use of the biological catalyst alcohol dehydrogenase (ADH) from Saccharomyces cerevisiae with CO2 reduction products obtained from photoelectrochemical cells (PEC). We first show that ADH can reduce very low micromolar amounts of formaldehyde in solution. Upon adding ADH to the PEC products, a rapid 3-4 fold gain in methanol production was observed, which we also attribute to the lack of back reaction by the enzyme. Lastly, because formaldehyde dehydrogenase (FalDH) showed very low reactivity with formate, the addition of

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FalDH and ADH to the PEC products demonstrated no difference in methanol yields as compared to ADH alone.

KEYWORDS: enzyme • photoelectrochemistry • CO2 reduction • methanol • formaldehyde

In recent years, extensive research has focused on developing catalytic systems that can generate renewable energy such as methanol and hydrogen from water and solar light. While splitting water to oxygen and hydrogen has been demonstrated successfully,1-8 the reduction of CO2 to a liquid fuel such as methanol has remained significantly more challenging due to required six-electron and proton transfer to CO2.9-11 Previously, photoelectrochemical cells (PECs) or aqueous suspensions of semiconductor powders were used to reduce CO2 into useful fuels. In early work by Halmann et al,12 PECs were constructed by using p-GaP cathodes and silicon anodes to reduce CO2 into formate, formaldehyde, and methanol under applied bias. The approach was further extended by Honda and coworkers who used wide bandgap semiconductors such as TiO2 in aqueous suspensions to generate formaldehyde and methanol.13 In later work, semiconductors including TiO2,14, 15 p-GaP,16, 17 TaON,18 p-type N-doped Ta2O5,19 p-type InP,20 CdS,21,Bi2WO6 hollow microspheres,22 and BiVO423 have been used to photoreduce CO2 to primarily formic acid with low micromolar amounts of methanol as detected by GC-MS. Recently, Bocarsly and coworkers utilized the organohydride pyridine in conjunction with electrochemical and photoelectrochemical cells to under bias, promote the reduction of CO2 to methanol.17 Furthermore, Boston et al showed that combining the photoactive ruthenium(II) trisphenanthroline with pyridine could also reduce CO2 in the presence of the sacrificial electron donors to form millimolar and micromolar amounts of formate and methanol respectively.24


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Lastly, in addition to using purely synthetic systems, research has explored the use of multiple enzymes to reduce CO225-27 which will be discussed more later. To improve enzyme activity, Weaver and co-workers also coupled formate dehydrogenase with p-type InP electrodes to increase CO2 reduction to formate.28 Despite significant effort in recent years, reducing CO2 to methanol has remained a difficult challenge because it requires a 6-electron, 6-proton transfer process. Instead, most catalytic systems produce 2-electron 2-proton products such as formic acid or CO.14,

16, 18-23, 29-33

Furthermore, even if formate could be further reduced to formaldehyde, converting formaldehyde to methanol in water is further hindered by the fast equilibrium of formaldehyde to the hydrate form methanediol,34 adding a rate-limiting step of dehydration back to formaldehyde to allow further reduction.35 To mitigate these challenges, we demonstrate here that a combination of the enzyme alcohol dehydrogenase (ADH) with synthetic photoelectrochemical cells (PEC) significantly increased the production of methanol from CO2 beyond what is typically possible with either inorganic catalysts or enzymes alone. Combining photocatalysts and biocatalysts has received increased attention recently, with much of the research focused on the use of coupled electron transfer.25, 32, 36-44 In this work, we first show that ADH isolated from Saccharomyces cerevisiae easily reduces formaldehyde in the presence of NADH starting from very low micromolar amounts of substrate, which is critical because electrochemical yields of formaldehyde from CO2 are expected to be very low. Furthermore, we demonstrate that the ADH is unique in that while the enzyme can dehydrogenate ethanol and butanol to their respective aldehydes, it cannot dehydrogenate methanol back to formaldehyde. Thus, this enzyme is particularly useful for increasing methanol production from PEC driven CO2 reduction with no possible back reactivity.


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Experimentally, the process of CO2 reduction typically results in decreasing amounts of the products formic acid (formate), formaldehyde, and methanol. The reduction potentials for producing formaldehyde and methanol can be significantly lowered in energy if multiple electrons and protons can be transferred simultaneously to CO2.45 However, since a simultaneous 6e-, 6H+ transfer to CO2 to produce methanol is highly difficult to achieve, it is expected that a natural progression of reducing CO2 to formate, formate to formaldehyde and formaldehyde to methanol might ensue. While reducing an aldehyde should be relatively facile, the reduction of formaldehyde in water is particularly challenging due to the equilibrium being greatly favored by ~103 toward the hydrate form methanediol with fast reaction rates.34 This rapid conversion to methanediol also therefore greatly lowers the amount of formaldehyde in solution available for reduction to methanol. Since at best, electrochemical or photoelectrochemical systems produce low millimolar amounts of formate, the amount of formaldehyde is expected to be in the mid to low micromolar range which is a very low reactant concentration for synthetic reductases. However, biological catalysts can perform well at sub-millimolar substrate concentrations due to the low KD values (dissociation constant) between enzymes and reactants.38, 46, 47 Furthermore, if an enzyme could reduce the low amounts of formaldehyde, the equilibrium between methanediol and formaldehyde would shift to producing more formaldehyde and therefore more methanol. In order to test enzyme activity, we first reacted an alcohol dehydrogenase (ADH) from Saccharomyces cerevisiae with varying concentrations of formaldehyde in the presence of NADH in phosphate buffer. The formation of methanol was tracked by 1H NMR spectroscopy and NADH consumption by UV-Vis spectroscopy. Reacting 0.1 unit (3.1 nM) ADH with 50, 100, 250, and 450 µM amounts of formaldehyde caused rapid methanol generation in which the methanol yield matched the conversion of NADH to NAD+ (Figure 1 and Supporting


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Information). Furthermore, even at 50 µM formaldehyde, ~33 µM methanol was formed (~66% yield). If we consider that 50 µM formaldehyde should equilibrate to produce about 80% methanediol (40 µM) and 20% formaldehyde (10 µM), the enzyme not only is efficient at converting low micromolar concentrations of formaldehyde but can also produce amounts of methanol that are greater than the starting amounts of formaldehyde available for reduction. Lastly, as control experiments, ADH was also reacted with CO2 and formic acid which showed neither the production of formic acid or methanol by NMR (Figure S2).

Figure 1. UV-Vis and 1H NMR spectra of ADH combined with different concentrations of formaldehyde in the presence of NADH. UV-Vis measurements showed the consumption of NADH from reacting ADH with (a) 50 µM and (b) 100 µM formaldehyde. 1H NMR spectroscopic measurements showing increase in methanol production from reacting ADH with NADH and (c) 50 µM and (d) 100 µM formaldehyde. (The methanol peak shown before the reaction comes from the commercially purchased formaldehyde) Because most alcohol dehydrogenases are known to undergo reversible oxidation-reduction reactions, the ADH was next tested for its rate of methanol oxidation, which would lower or limit


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methanol yields. To study this, ADH was reacted with 500 µM methanol and NAD+, and UV Vis and 1H NMR spectroscopy were used to measure NADH production and methanol consumption, respectively. As shown in Figure S3, combining ADH and methanol led to no detectable amounts of NADH by UV-Vis, and, correspondingly, no decrease in the proton peak for methanol was observed. No detectable increase in NADH or decrease in methanol was observed even after 12 h. However when ethanol or butanol was used instead as the substrate, the ADH performed as expected and quickly converted NAD+ to NADH (Figure S4). In order to explain this phenomena, the Michaelis constant (KM) of ADH with methanol which is defined as the concentration at which the rate of the enzyme reaction is half the maximum reaction rate was measured to be 148 mM (Figure S5). Based on this result, we determined that while ADH can in fact oxidize methanol back to formaldehyde, the substrate concentration needed was substantially higher than what could be produced from CO2 reduction, enabling the use of the enzyme for increasing methanol production from CO2. To study this, we next utilized a photoelectrochemical cell (PEC) to reduce CO2 prior to adding the enzyme. This was done because many hours of photoirradiation are typically needed to produce low micromolar or millimolar amounts of products from CO2.18, 19, 30, 48 The PEC was built from a NiO/CdTe photocathode and a Pt counter electrode. CdTe nanoparticles (NPs) were first synthesized using published procedures.49 The bandgap of the CdTe was determined previously to be ~2 eV and the conduction band of the CdTe was measured to be -1.53 V vs. Ag/AgCl through electrochemical studies, which is sufficient enough to reduce CO2.48 To produce the photocathode, NiO was first deposited on ITO to act as a hole collector, then a CdTe paste was brushed onto the NiO layer and the substrates were calcined. In order to increase CO2 reduction, a diffusional catalyst, CpRh(bpy)Cl2 was utilized in conjunction with the PECs to


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improve product yields by ~85 fold.48 This particular metal complex was also chosen because it had been shown in previous reports to be an effective hydride donor at neutral pH and while not interfering with enzyme activity37, 40, 41, 50-52 We next coupled the NiO/CdTe cathode to a Pt anode, and CO2 was then bubbled into the electrochemical cell containing 0.4 mM organocatalyst CpRh(bpy)Cl2 in 0.1 M phosphate buffer (pH 6.8). After 17 h photoirradiation, ~2 mM of formate and ~10 µM of methanol were detected by 1H NMR spectroscopy (Figure 2). Formaldehyde was difficult to detect because the expected methanediol peak was obscured by the large water peak. Nevertheless, a small amount of methanol would indicate that at least small amounts of formaldehyde or methanediol were present in the product mixture.

Figure 2. 1H NMR spectra result of PEC reaction after 16 h photoirradiation and (insert) the methanol peak before and after reacting ADH with the PEC product solutions. Before adding ADH, 10 µM methanol was measured and after the addition of enzyme, 47 µM methanol was detected. After photoirradiation, 10 units (0.4 µM) of ADH and 1.8 mM NADH were next added to 374 µL of the PEC product solution in the dark, and methanol formation was monitored by 1H NMR spectroscopy. While the PEC product solution initially showed 10 µM methanol, addition of the


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enzyme increased the methanol concentration by ~5 fold to 47 µM methanol within 30 min (Figure 2). This not only showed that formaldehyde and/or methanediol was present in the PEC product mixture, but also that the ADH was able to convert very low concentrations of formaldehyde to methanol. To determine the amount of methanol generated in real time a calibration curve of peak area versus methanol concentration was built (Figure S6). Enzyme reactions over 30 min – 1 h showed a gradual 4-5 fold increase in methanol production (Figure 3). Although the total amount of methanol from CO2 reduction clearly depends on the PEC performance, over multiple runs with different PEC reactions, addition of ADH generally showed an average gain of 3.22 fold in methanol concentration within 30 min (Figure 3 and S7). Since each PEC reaction can generate varying amounts of product (formate, formaldehyde, methanol) from one run to the next, the observed deviations in methanol yields before and after adding the enzyme are not unexpected. As described earlier, because the ADH cannot oxidize methanol, the methanol yield remained constant with no later decreases due to back reactions.

Figure 3. Comparison of methanol production from PEC reaction before and after adding ADH. Error bars indicate 1 standard error from 5 replicate experiments.


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Figure 4. 1H NMR spectra of measuring methanol formation over time upon adding (a) ADH to the PEC product solution and (b) FalDH and ADH to a different aliquot of the exact same PEC production solution shown in (a). At time zero, the PEC product solutions showed 24 µM methanol. The addition of (b) FalDH and ADH yielded 103 µM methanol and (a) ADH alone gave 96 µM methanol. In addition to studying the ADH enzyme with the PEC driven CO2 reactions, we also tested other enzymes such as formate dehydrogenase (FDH) and formaldehyde dehydrogenase (FalDH), since previous reports stated that using a tandem series of enzymes could produce measurable amounts of methanol from CO2.25-27 It must be noted that these studies however primarily used gas chromatography to detect methanol directly from buffered solutions that in some cases also contained the different enzymes which can often be difficult to do. For our studies, we first combined 1 unit of FDH with a saturated CO2 solution in buffer and measured formate production by 1H NMR spectroscopy. As shown in Figure S6, only 80 µM formate was produced after 12 h. This result matched the NAD+ conversion by UV Vis spectroscopy (Figure S8), which showed extremely slow enzyme kinetics. We next reacted 1 or 3 units of FalDH with 500 µM to 20mM formate and NADH and monitored their conversion by 1H NMR and UV Vis spectroscopy respectively. As shown in Figure S6, little NADH conversion to NAD+ was observed even after 5 h. These results were also confirmed by analysis of NMR, which showed no decrease in the formate peak (Figure S9). While lowering the pH to 5 might be expected to


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push the formate reduction by FalDH by protonating formate, FalDH activity did not improve significantly at pH 5 (Figure S9). In contrast, when the FalDH was mixed with NAD+ and formaldehyde, the NADH peak clearly increased in 1 h, indicating that formaldehyde is easily oxidized to formic acid (Figure S9). Although both FDH and FalDH demonstrated low conversion efficiencies as hydrogenases, we next also tested all three enzymes, FDH, FalDH and ADH in the presence of CO2 and a 1.8mM of NADH. However, as shown in Figure S10, using all three enzymes simultaneously only produced sub-100 µM amounts of formate and no methanol. Finally, since the PEC reactions could generate measurable millimolar amounts of formate from CO2, we also tested the addition of FaldH and ADH to the PEC product mixture in order to see if this could increase the production of methanol. However, due to the low reactivity of FalDH with formate, as shown in Figure 4, using both FalDH and ADH showed no difference in methanol production as compared to when ADH was used alone. We have demonstrated in this work the novel use of biological catalysts with photoelectrochemical cells to increase the production of methanol by CO2 reduction in water. While many synthetic catalysts have been studied to push CO2 reduction, these processes produce mainly formic acid or formate, with very low levels of methanol. Furthermore, although formaldehyde should be a product of CO2 reduction, the equilibrium causes it to primarily exist in its hydrate form, methanediol, decreasing the amount of available aldehyde for reduction. Because biological catalysts are known to work highly effectively with low substrate concentrations, we first showed that an alcohol dehydrogenase could reduce formaldehyde down to 50 µM formaldehyde. Furthermore, we demonstrated that the ADH is an ideal catalyst for increasing methanol production from CO2 as it could not undergo back reaction to oxidize


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methanol back to formaldehyde. By combining ADH with products generated from photoelectrochemical cells, we were able to induce 3-4 fold gains in methanol production from CO2 and water. Other enzymes such as FDH and FalDH showed poor activity in reducing CO2 or formate, respectively, and that combinations of FDH, FalDH and ADH could therefore only yield ~80 µM formate with no methanol. Due to this low activity of FalDH with formate, using both FalDH and ADH with the PEC generated reduced CO2 products showed no improvement over ADH alone. These results also are cost advantageous since out of the three enzymes, ADH is markedly lower in price (76 USD/30 kUN) as compared to the FDH (176 USD/50 UN) or FalDH (138 USD/5 UN). This work thus demonstrates the power of combinations of biological catalysts with synthetic photosystems to ultimately increase the generation of liquid fuel from CO2 and water.

ASSOCIATED CONTENT AUTHOR INFORMATION Corresponding Author * [email protected] Author Contributions The manuscript was written through contributions of all authors. All authors have given approval to the final version of the manuscript. Funding Sources


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The research was primarily supported by the U.S. Dept of Energy (DOE), Office of Science, Basic Energy Sciences (BES) under Award # DE-SC0006398 (synthesis, assembly). In addition the research was supported by the National Institute of Health (1R21EB020911-01). Supporting Information. The following files are available free of charge. Experiment details and additional figures (PDF) ACKNOWLEDGMENT The research was primarily supported by the U.S. Dept of Energy (DOE), Office of Science, Basic Energy Sciences (BES) under Award # DE-SC0006398 (synthesis, assembly). In addition the research was supported by the National Institute of Health (1R21EB020911-01). REFERENCES (1) Maeda, K.; Teramura, K.; Lu, D.; Takata, T.; Saito, N.; Inoue, Y.; Domen, K. Nature 2006, 440, 295-295. (2) Gray, H. B. Nat. Chem. 2009, 1, 7-7. (3) Ma, K.; Yehezkeli, O.; Domaille, D. W.; Funke, H. H.; Cha, J. N. Angew. Chem., Int. Ed. 2015, 54, 11490-11494. (4) Maeda, K. ACS Catal. 2013, 3, 1486-1503. (5) Zhou, P.; Yu, J.; Jaroniec, M. Adv. Mater. 2014, 26, 4920-4935. (6) Walter, M. G.; Warren, E. L.; McKone, J. R.; Boettcher, S. W.; Mi, Q.; Santori, E. A.; Lewis, N. S. Chem. Rev. 2011, 111, 5815-5815.


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