An interfacial-intramolecular electron highway for accelerated electrocatalytic CO2 reduction by an O2-tolerant formate dehydrogenase

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An interfacial-intramolecular electron highway for accelerated electrocatalytic CO2 reduction by an O2-tolerant formate dehydrogenase

References

  1. Liu, Z., Wang, K., Chen, Y., Tan, T. & Nielsen, J. Third-generation biorefineries as the means to produce fuels and chemicals from CO2. Nat. Catal. 3, 274–288 (2020).

    Google Scholar 

  2. Gleizer, S. et al. Conversion of Escherichia coli to generate all biomass carbon from CO2. Cell 179, 1255–1263 (2019).

    Google Scholar 

  3. Cai, T. et al. Cell-free chemoenzymatic starch synthesis from carbon dioxide. Science 373, 1523–1527 (2021).

    Google Scholar 

  4. Zheng, T. T. et al. Upcycling CO2 into energy-rich long-chain compounds via electrochemical and metabolic engineering. Nat. Catal. 5, 388–396 (2022).

    Google Scholar 

  5. Cui, H. et al. Converting CO2 to single-cell protein via an integrated electrocatalytic-biosynthetic system. Appl. Catal. B Environ. 350, 123946 (2024).

    Google Scholar 

  6. Wu, R. et al. Enzymatic Electrosynthesis of glycine from CO2 and NH3. Angew. Chem. Int. Ed. 62, e202218387 (2023).

  7. Fang, W. et al. Durable CO2 conversion in the proton-exchange membrane system. Nature 626, 86–91 (2024).

    Google Scholar 

  8. Contaldo, U. et al. Efficient electrochemical CO2/CO interconversion by an engineered carbon monoxide dehydrogenase on a gas-diffusion carbon nanotube-based bioelectrode. ACS Catal. 11, 5808–5817 (2021).

    Google Scholar 

  9. Cobb, S. J. et al. Fast CO2 hydration kinetics impair heterogeneous but improve enzymatic CO2 reduction catalysis. Nat. Chem. 14, 417–424 (2022).

    Google Scholar 

  10. Reda, T., Plugge, C. M., Abram, N. J. & Hirst, J. Reversible interconversion of carbon dioxide and formate by an electroactive enzyme. Proc. Natl. Acad. Sci. USA 105, 10654–10658 (2008).

    Google Scholar 

  11. Robinson, W. E., Bassegoda, A., Reisner, E. & Hirst, J. Oxidation-state-dependent binding properties of the active site in a Mo-containing formate dehydrogenase. J. Am. Chem. Soc. 139, 9927–9936 (2017).

    Google Scholar 

  12. Robinson, W. E., Bassegoda, A., Blaza, J. N., Reisner, E. & Hirst, J. Understanding how the rate of C–H bond cleavage affects formate oxidation catalysis by a Mo-dependent formate dehydrogenase. J. Am. Chem. Soc. 142, 12226–12236 (2020).

    Google Scholar 

  13. Bassegoda, A., Madden, C., Wakerley, D. W., Reisner, E. & Hirst, J. Reversible interconversion of CO2 and formate by a molybdenum-containing formate dehydrogenase. J. Am. Chem. Soc. 136, 15473–15476 (2014).

    Google Scholar 

  14. Li, W. et al. Direct detection of a single [4Fe-4S] cluster in a tungsten-containing enzyme: electrochemical conversion of CO2 into formate by formate dehydrogenase. Carbon Energy 5, e304 (2023).

    Google Scholar 

  15. Chen, H. et al. Fundamentals, applications, and future directions of bioelectrocatalysis. Chem. Rev. 120, 12903–12993 (2020).

    Google Scholar 

  16. Karyakin, A. A. et al. The limiting performance characteristics in bioelectrocatalysis of hydrogenase enzymes. Angew. Chem. Int. Ed. 46, 7244–7246 (2007).

    Google Scholar 

  17. Wang, Y., Kang, Z., Zhang, L. & Zhu, Z. Elucidating the interactions between a [NiFe]-hydrogenase and carbon electrodes for enhanced bioelectrocatalysis. ACS Catal. 12, 1415–1427 (2022).

    Google Scholar 

  18. Becker, J. M. et al. Bioelectrocatalytic CO2 reduction by redox polymer-wired carbon monoxide dehydrogenase gas diffusion electrodes. ACS Appl. Mater. Interfaces 14, 46421–46426 (2022).

    Google Scholar 

  19. Parkin, A., Seravalli, J., Vincent, K. A., Ragsdale, S. W. & Armstrong, F. A. Rapid and efficient electrocatalytic CO2/CO interconversions by carboxydothermus hydrogenoformans CO dehydrogenase I on an electrode. J. Am. Chem. Soc. 129, 10328–10329 (2007).

    Google Scholar 

  20. Hirst, J. Elucidating the mechanisms of coupled electron transfer and catalytic reactions by protein film voltammetry. Biochim. Biophys. Acta Bioenerg. 1757, 225–239 (2006).

    Google Scholar 

  21. Zu, Y., Fee, J. A. & Hirst, J. Breaking and re-forming the disulfide bond at the high-potential, respiratory-type rieske [2Fe-2S] center of thermus thermophilus: characterization of the sulfhydryl state by protein-film voltammetry. Biochemistry 41, 14054–14065 (2002).

    Google Scholar 

  22. Zu, Y. et al. Reduction potentials of rieske clusters: importance of the coupling between oxidation state and histidine protonation state. Biochemistry 42, 12400–12408 (2003).

    Google Scholar 

  23. Badiani, V. M. et al. Elucidating film loss and the role of hydrogen bonding of adsorbed redox enzymes by electrochemical quartz crystal microbalance analysis. ACS Catal. 12, 1886–1897 (2022).

    Google Scholar 

  24. Chemla, Y., Kaufman, F., Amiram, M. & Alfonta, L. Expanding the genetic code of bioelectrocatalysis and biomaterials. Chem. Rev. 124, 11187–11241 (2024).

    Google Scholar 

  25. Badiani, V. M. et al. Engineering electro- and photocatalytic carbon materials for CO2 reduction by formate dehydrogenase. J. Am. Chem. Soc. 144, 14207–14216 (2022).

    Google Scholar 

  26. Alvarez-Malmagro, J. et al. Bioelectrocatalytic activity of W-formate dehydrogenase covalently immobilized on functionalized gold and graphite electrodes. ACS Appl. Mater. Interfaces 13, 11891 (2021).

    Google Scholar 

  27. Liu, W. et al. Bioelectrocatalytic carbon dioxide reduction by an engineered formate dehydrogenase from Thermoanaerobacter kivui. Nat. Commun. 15, 9962 (2024).

    Google Scholar 

  28. Schwarz, F. M., Schuchmann, K. & Muller, V. Hydrogenation of CO2 at ambient pressure catalyzed by a highly active thermostable biocatalyst. Biotechnol. Biofuels 11, 237 (2018).

    Google Scholar 

  29. Dietrich, H. M. et al. Membrane-anchored HDCR nanowires drive hydrogen-powered CO2 fixation. Nature 607, 823–830 (2022).

    Google Scholar 

  30. Schuchmann, K. & Müller, V. Direct and reversible hydrogenation of CO2 to formate by a bacterial carbon dioxide reductase. Science 342, 1382–1385 (2013).

    Google Scholar 

  31. de Bok, F. A. et al. Two W-containing formate dehydrogenases (CO2-reductases) involved in syntrophic propionate oxidation by Syntrophobacter fumaroxidans. Eur. J. Biochem. 270, 2476–2485 (2003).

    Google Scholar 

  32. Böhmer, N., Hartmann, T. & Leimkühler, S. The chaperone FdsC for Rhodobacter capsulatus formate dehydrogenase binds the bis-molybdopterin guanine dinucleotide cofactor. FEBS Lett. 588, 531–537 (2014).

    Google Scholar 

  33. Iliuta, I. & Larachi, F. Direct-air capture conversion of CO2 in fixed-bed microreactors with immobilized formate dehydrogenase and glucose dehydrogenase: Concept feasibility. Chem. Eng. Res. Des. 193, 306–319 (2023).

    Google Scholar 

  34. Min, K. et al. Elevated conversion of CO2 to versatile formate by a newly discovered formate dehydrogenase from Rhodobacter aestuarii. Bioresour. Technol. 305, 123155 (2020).

    Google Scholar 

  35. Brouwer, E.-M. et al. Characterization of the oxygen-tolerant formate dehydrogenase from Clostridium carboxidivorans. Front. Microbiol. 15, 1527626 (2025).

    Google Scholar 

  36. Yoshikawa, T. et al. Multiple electron transfer pathways of tungsten-containing formate dehydrogenase in direct electron transfer-type bioelectrocatalysis. Chem. Commun. 58, 6478–6481 (2022).

    Google Scholar 

  37. Jeon, B. W. et al. Enzymatic conversion of CO2 to formate: the potential of tungsten-containing formate dehydrogenase in flow reactor system. J. CO2 Util. 82, 102754 (2024).

    Google Scholar 

  38. Cha, J., Lee, J., Jeon, B. W., Kim, Y. H. & Kwon, I. Real flue gas CO2 hydrogenation to formate by an enzymatic reactor using O2– and CO-tolerant hydrogenase and formate dehydrogenase. Front. Bioeng. Biotechnol. 11, 1265272 (2023).

    Google Scholar 

  39. Lee, J. et al. Molar-scale formate production via enzymatic hydration of industrial off-gases. Nat. Chem. Eng. 1, 354–364 (2024).

    Google Scholar 

  40. Fera, M. -C. et al. Bioelectrocatalytic CO2 reduction to formate by Candida boidinii formate dehydrogenase overcoming NADH dependence with tailored amino-viologen redox polymers. J. CO2 Util. 93, 103041 (2025).

    Google Scholar 

  41. Oliveira, A. R. et al. Toward the mechanistic understanding of enzymatic CO2 reduction. ACS Catal. 10, 3844–3856 (2020).

    Google Scholar 

  42. Kuk, S. K. et al. NADH-free electroenzymatic reduction of CO2 by conductive hydrogel-conjugated formate dehydrogenase. ACS Catal. 9, 5584–5589 (2019).

    Google Scholar 

  43. Oliveira, A. R. et al. An allosteric redox switch involved in oxygen protection in a CO2 reductase. Nat. Chem. Biol. 20, 111–119 (2024).

    Google Scholar 

  44. Yu, T. et al. Enzyme function prediction using contrastive learning. Science 379, 1358–1363 (2023).

    Google Scholar 

  45. Wang, Z. et al. Robust enzyme discovery and engineering with deep learning using CataPro. Nat. Commun. 16, 2736 (2025).

    Google Scholar 

  46. Li, Y. et al. Metabolic regulation of Shewanella oneidensis for microbial electrosynthesis: From extracellular to intracellular. Metab. Eng. 80, 1–11 (2023).

    Google Scholar 

  47. Brondino, C. D. et al. Incorporation of either molybdenum or tungsten into formate dehydrogenase from Desulfovibrio alaskensis NCIMB 13491: EPR assignment of the proximal iron-sulfur cluster to the pterin cofactor in formate dehydrogenases from sulfate-reducing bacteria. J. Biol. Inorg. Chem. 9, 145–151 (2004).

    Google Scholar 

  48. Maia, L. B., Fonseca, L., Moura, I. & Moura, J. J. G. Reduction of carbon dioxide by a molybdenum-containing formate dehydrogenase: a kinetic and mechanistic study. J. Am. Chem. Soc. 138, 8834–8846 (2016).

    Google Scholar 

  49. Cobb, S. J., Dharani, A. M., Oliveira, A. R., Pereira, I. A. C. & Reisner, E. Carboxysome-inspired electrocatalysis using enzymes for the reduction of CO2 at low concentrations. Angew. Chem., Int. Ed. 62, e202218782 (2023).

    Google Scholar 

  50. Yang, J. Y., Kerr, T. A., Wang, X. S. & Barlow, J. M. Reducing CO2 to HCO2− at mild potentials: lessons from formate dehydrogenase. J. Am. Chem. Soc. 142, 19438–19445 (2020).

    Google Scholar 

  51. Steinhilper, R., Höff, G., Heider, J. & Murphy, B. J. Structure of the membrane-bound formate hydrogenlyase complex from Escherichia coli. Nat. Commun. 13, 5395 (2022).

    Google Scholar 

  52. Page, C. C., Moser, C. C., Chen, X. X. & Dutton, P. L. Natural engineering principles of electron tunnelling in biological oxidation-reduction. Nature 402, 47–52 (1999).

    Google Scholar 

  53. Cellini, A. et al. Directed ultrafast conformational changes accompany electron transfer in a photolyase as resolved by serial crystallography. Nat. Chem. 16, 24 (2024).

    Google Scholar 

  54. Winkler, J. R. & Gray, H. B. Long-range electron tunneling. J. Am. Chem. Soc. 136, 2930–2939 (2014).

    Google Scholar 

  55. Kurisu, G. et al. Structure of the electron transfer complex between ferredoxin and ferredoxin-NADP+ reductase. Nat. Struct. Biol. 8, 117–121 (2001).

    Google Scholar 

  56. Volbeda, A., Darnault, C., Renoux, O., Nicolet, Y. & Fontecilla-Camps, J. C. The crystal structure of the global anaerobic transcriptional regulator FNR explains its extremely fine-tuned monomer-dimer equilibrium. Sci. Adv. 1, e1501086 (2015).

    Google Scholar 

  57. Cui, H. et al. Rapid and oriented immobilization of laccases on electrodes via a methionine-rich peptide. ACS Catal. 11, 2445–2453 (2021).

    Google Scholar 

  58. 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 275, 1305–1308 (1997).

    Google Scholar 

  59. Edwardes Moore, E. et al. Understanding the local chemical environment of bioelectrocatalysis. Proc. Natl. Acad. Sci. USA 119, e2114097119 (2022).

    Google Scholar 

  60. Nguyen, L. -T., Schmidt, H. A., von Haeseler, A. & Minh, B. Q. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol. Biol. Evol. 32, 268–274 (2014).

    Google Scholar 

  61. Letunic, I. & Bork, P. Interactive Tree of Life (iTOL) v6: recent updates to the phylogenetic tree display and annotation tool. Nucleic Acids Res. 52, 78–82 (2024).

    Google Scholar 

  62. Jin, M. et al. Unique organizational and functional features of the cytochrome c maturation system in Shewanella oneidensis. PLoS ONE 8, e75610 (2013).

    Google Scholar 

  63. Melchor, S. & Dobado, J. A. CoNTub: An algorithm for connecting two arbitrary carbon nanotubes. J. Chem. Inf. Comput. Sci. 44, 1639–1646 (2004).

    Google Scholar 

  64. Li, C. & Chou, T. -W. Elastic moduli of multi-walled carbon nanotubes and the effect of van der Waals forces. Compos. Sci. Technol. 63, 1517–1524 (2003).

    Google Scholar 

  65. Wang, H., Michielssens, S., Moors, S. L. C. & Ceulemans, A. Molecular dynamics study of dipalmitoylphosphatidylcholine lipid layer self-assembly onto a single-walled carbon nanotube. Nano Res. 2, 945–954 (2009).

    Google Scholar 

  66. Zhang, M. et al. Engineering a binding peptide for oriented immobilization and efficient bioelectrocatalytic oxygen reduction of multicopper oxidases. ACS Appl. Mater. Interfaces 17, 2355–2364 (2025).

    Google Scholar 

  67. Edwardes Moore, E. et al. A Semi-artificial photoelectrochemical tandem leaf with a CO2-to-formate efficiency approaching 1%. Angew. Chem. Int. Ed. 60, 26303 (2021).

    Google Scholar 

  68. Miller, M. et al. Interfacing formate dehydrogenase with metal oxides for the reversible electrocatalysis and solar-diven reduction of carbon dioxide. Angew. Chem. Int. Ed. 58, 4601–4605 (2019).

    Google Scholar 

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