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Regulation of the electrocatalytic nitrogen cycle based on sequential proton–electron transfer

Nature Catalysis volume 5, pages 798–806 (2022)Cite this article

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Abstract

The selective transformation of nitrogen compounds is a foundation of the modern chemical industry. Existing thermochemical processes largely rely on fossil fuels and innovating electrocatalytic processes that could use renewable energy remains challenging. Here we report the electrochemical regulation of a nitrite reduction network using a molybdenum sulfide catalyst by modulating the thermodynamic driving force of proton and electron transfer. The strategy behind this approach is based on the theory of sequential proton–electron transfer, in which the driving force of proton and electron transfer can be optimized independently. This makes it possible to target the desired reactions with selectivities of up to 80% for NO, 61% for N2O, 36% for N2 and 100% for NH4+, comparable to the highest values reported to date using a specific catalyst optimized for a single target product. Consistency with numerical simulation highlights that sequential proton–electron transfer can be used to rationally regulate the electrochemical nitrogen network.

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Fig. 1: The nitrogen cycle network in natural and industrial processes.
Fig. 2: Model of proton–electron transfer and its application for selective nitrite reduction.
Fig. 3: Characterization of MoS2.
Fig. 4: NO2− reduction to NO, N2O and NH4+ on MoS2 in a wide pH–E space.
Fig. 5: Simulation of the effects of E and pKa on the selectivity of NO2− reduction.
Fig. 6: Mechanism of N–N coupling and catalytic performance for full denitrification.

Data availability

The data that support the findings of this study are available from the corresponding authors upon request. The Python program for numerical simulations can be found at GitHub (https://github.com/HideshiOoka/SI_for_Publications).

References

  1. Chen, J. G. et al. Beyond fossil fuel-driven nitrogen transformations. Science 360, eaar6611 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  2. Lehnert, N., Musselman, B. W. & Seefeldt, L. C. Grand challenges in the nitrogen cycle. Chem. Soc. Rev. 50, 3640–3646 (2021).

    Article  CAS  PubMed  Google Scholar 

  3. Rosca, V., Duca, M., de Groot, M. T. & Koper, M. T. Nitrogen cycle electrocatalysis. Chem. Rev. 109, 2209–2244 (2009).

    Article  CAS  PubMed  Google Scholar 

  4. Kuypers, M. M. M., Marchant, H. K. & Kartal, B. The microbial nitrogen-cycling network. Nat. Rev. Microbiol. 16, 263–276 (2018).

    Article  CAS  PubMed  Google Scholar 

  5. Lehnert, N., Dong, H. T., Harland, J. B., Hunt, A. P. & White, C. J. Reversing nitrogen fixation. Nat. Rev. Chem. 2, 278–289 (2018).

    Article  CAS  Google Scholar 

  6. Erisman, J. W., Sutton, M. A., Galloway, J., Klimont, Z. & Winiwarter, W. How a century of ammonia synthesis changed the world. Nat. Geosci. 1, 636–639 (2008).

    Article  CAS  Google Scholar 

  7. Wang, Y., Wang, C., Li, M., Yu, Y. & Zhang, B. Nitrate electroreduction: mechanism insight, in situ characterization, performance evaluation, and challenges. Chem. Soc. Rev. 50, 6720–6733 (2021).

    Article  CAS  PubMed  Google Scholar 

  8. Duca, M. & Koper, M. T. M. Powering denitrification: the perspectives of electrocatalytic nitrate reduction. Energy Environ. Sci. 5, 9726–9742 (2012).

    Article  CAS  Google Scholar 

  9. van Langevelde, P. H., Katsounaros, I. & Koper, M. T. M. Electrocatalytic nitrate reduction for sustainable ammonia production. Joule 5, 290–294 (2021).

    Article  Google Scholar 

  10. MacFarlane, D. R. et al. A roadmap to the ammonia economy. Joule 4, 1186–1205 (2020).

    Article  CAS  Google Scholar 

  11. Braley, S. E., Xie, J., Losovyj, Y. & Smith, J. M. Graphite conjugation of a macrocyclic cobalt complex enhances nitrite electroreduction to ammonia. J. Am. Chem. Soc. 143, 7203–7208 (2021).

    Article  CAS  PubMed  Google Scholar 

  12. Uyeda, C. & Peters, J. C. Selective nitrite reduction at heterobimetallic CoMg complexes. J. Am. Chem. Soc. 135, 12023–12031 (2013).

    Article  CAS  PubMed  Google Scholar 

  13. Guo, Y., Stroka, J. R., Kandemir, B., Dickerson, C. E. & Bren, K. L. A cobalt metallopeptide electrocatalyst for the selective reduction of nitrite to ammonium. J. Am. Chem. Soc. 140, 16888–16892 (2018).

    Article  CAS  PubMed  Google Scholar 

  14. Park, J. et al. In situ electrochemical generation of nitric oxide for neuronal modulation. Nat. Nanotechnol. 15, 690–697 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Kim, D. H. et al. Selective electrochemical reduction of nitric oxide to hydroxylamine by atomically dispersed iron catalyst. Nat. Commun. 12, 1856 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Hao, Y.-C. et al. Promoting nitrogen electroreduction to ammonia with bismuth nanocrystals and potassium cations in water. Nat. Catal. 2, 448–456 (2019).

    Article  CAS  Google Scholar 

  17. Nakajima, K., Toda, H., Sakata, K. & Nishibayashi, Y. Ruthenium-catalysed oxidative conversion of ammonia into dinitrogen. Nat. Chem. 11, 702–709 (2019).

    Article  CAS  PubMed  Google Scholar 

  18. Kamiya, K. et al. Selective reduction of nitrate by a local cell catalyst composed of metal-doped covalent triazine frameworks. ACS Catal. 8, 2693–2698 (2018).

    Article  CAS  Google Scholar 

  19. Chen, G.-F. et al. Electrochemical reduction of nitrate to ammonia via direct eight-electron transfer using a copper–molecular solid catalyst. Nat. Energy 5, 605–613 (2020).

    Article  CAS  Google Scholar 

  20. Kim, J. E. et al. Electrochemical synthesis of glycine from oxalic acid and nitrate. Angew. Chem. Int. Ed. 60, 21943–21951 (2021).

    Article  CAS  Google Scholar 

  21. Wu, Y. S., Jiang, Z., Lin, Z. C., Liang, Y. Y. & Wang, H. L. Direct electrosynthesis of methylamine from carbon dioxide and nitrate. Nat. Sustain. 4, 725–730 (2021).

    Article  Google Scholar 

  22. Lv, C. D. et al. Selective electrocatalytic synthesis of urea with nitrate and carbon dioxide. Nat. Sustain. 4, 868–876 (2021).

    Article  Google Scholar 

  23. Koper, M. T. M. Volcano activity relationships for proton-coupled electron transfer reactions in electrocatalysis. Top. Catal. 58, 1153–1158 (2015).

    Article  CAS  Google Scholar 

  24. Koper, M. T. M. Theory of multiple proton–electron transfer reactions and its implications for electrocatalysis. Chem. Sci. 4, 2710–2723 (2013).

    Article  CAS  Google Scholar 

  25. He, D. et al. Selective electrocatalytic reduction of nitrite to dinitrogen based on decoupled proton-electron transfer. J. Am. Chem. Soc. 140, 2012–2015 (2018).

    Article  CAS  PubMed  Google Scholar 

  26. He, D. et al. Atomic-scale evidence for highly selective electrocatalytic N–N coupling on metallic MoS2. Proc. Natl Acad. Sci. USA 117, 31631–31638 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Liu, T. et al. Accelerating proton-coupled electron transfer of metal hydrides in catalyst model reactions. Nat. Chem. 10, 881–887 (2018).

    Article  CAS  PubMed  Google Scholar 

  28. Ooka, H., McGlynn, S. E. & Nakamura, R. Electrochemistry at deep‐sea hydrothermal vents: utilization of the thermodynamic driving force towards the autotrophic origin of life. ChemElectroChem 6, 1316–1323 (2019).

    Article  CAS  Google Scholar 

  29. Liu, Q. et al. Gram-scale aqueous synthesis of stable few-layered 1T-MoS2: applications for visible-light-driven photocatalytic hydrogen evolution. Small 11, 5556–5564 (2015).

    Article  CAS  PubMed  Google Scholar 

  30. Yang, S. et al. Hierarchical 1T-MoS2 nanotubular structures for enhanced supercapacitive performance. J. Mater. Chem. A 5, 23704–23711 (2017).

    Article  CAS  Google Scholar 

  31. Kwon, I. S. et al. Intercalation of aromatic amine for the 2H-1T′ phase transition of MoS2 by experiments and calculations. Nanoscale 10, 11349–11356 (2018).

    Article  CAS  PubMed  Google Scholar 

  32. Chou, S. S. et al. Understanding catalysis in a multiphasic two-dimensional transition metal dichalcogenide. Nat. Commun. 6, 8311 (2015).

    Article  CAS  PubMed  Google Scholar 

  33. Anderson, L. J., Richardson, D. J. & Butt, J. N. Catalytic protein film voltammetry from a respiratory nitrate reductase provides evidence for complex electrochemical modulation of enzyme activity. Biochemistry 40, 11294–11307 (2001).

    Article  CAS  PubMed  Google Scholar 

  34. Maia, L.B., Moura, I. & Moura, J.J.G. in Future Directions in Metalloprotein and Metalloenzyme Research, Vol. 33 (eds Hanson, G. & Berliner, L.) 55–101 (Springer, 2017).

  35. Boussac, A. et al. The low spin-high spin equilibrium in the S2-state of the water oxidizing enzyme. Biochim. Biophys. Acta Bioenerg. 1859, 342–356 (2018).

    Article  CAS  PubMed  Google Scholar 

  36. Li, Y. et al. Enzyme mimetic active intermediates for nitrate reduction in neutral aqueous media. Angew. Chem. Int. Ed. 59, 9744–9750 (2020).

    Article  CAS  Google Scholar 

  37. Glasser, N. R., Oyala, P. H., Osborne, T. H., Santini, J. M. & Newman, D. K. Structural and mechanistic analysis of the arsenate respiratory reductase provides insight into environmental arsenic transformations. Proc. Natl Acad. Sci. USA 115, E8614–E8623 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Tran, P. D. et al. Coordination polymer structure and revisited hydrogen evolution catalytic mechanism for amorphous molybdenum sulfide. Nat. Mater. 15, 640–646 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Andersen, S. Z. et al. A rigorous electrochemical ammonia synthesis protocol with quantitative isotope measurements. Nature 570, 504–508 (2019).

    Article  CAS  PubMed  Google Scholar 

  40. Suryanto, B. H. R. et al. Challenges and prospects in the catalysis of electroreduction of nitrogen to ammonia. Nat. Catal. 2, 290–296 (2019).

    Article  CAS  Google Scholar 

  41. Yang, H., Gandhi, H., Ostrom, N. E. & Hegg, E. L. Isotopic fractionation by a fungal P450 nitric oxide reductase during the production of N2O. Environ. Sci. Technol. 48, 10707–10715 (2014).

    Article  CAS  PubMed  Google Scholar 

  42. Stein, L. Y. & Yung, Y. L. Production, isotopic composition, and atmospheric fate of biologically produced nitrous oxide. Annu. Rev. Earth Planet. Sci. 31, 329–356 (2003).

    Article  CAS  Google Scholar 

  43. Toyoda, S., Mutobe, H., Yamagishi, H., Yoshida, N. & Tanji, Y. Fractionation of N2O isotopomers during production by denitrifier. Soil Biol. Biochem. 37, 1535–1545 (2005).

    Article  CAS  Google Scholar 

  44. Yoshida, N. & Toyoda, S. Constraining the atmospheric N2O budget from intramolecular site preference in N2O isotopomers. Nature 405, 330–334 (2000).

    Article  CAS  PubMed  Google Scholar 

  45. Maia, L. B. & Moura, J. J. How biology handles nitrite. Chem. Rev. 114, 5273–5357 (2014).

    Article  CAS  PubMed  Google Scholar 

  46. Ravel, B. & Newville, M. ATHENA, ARTEMIS, HEPHAESTUS: data analysis for X-ray absorption spectroscopy using IFEFFIT. J. Synchrotron Rad. 12, 537–541 (2005).

    Article  CAS  Google Scholar 

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Acknowledgements

We thank H. Ofuchi at SPring-8 for his assistance with the XAFS measurements. R.N. was supported by a JSPS Grant-in-Aid for Scientific Research (number 26288092). H.O. was supported by Fusion Oriented Research for Disruptive Science and Technology program of Japan Science and Technology Agency (JST). Y.L. was supported by a JSPS Grant-in-Aid for Scientific Research (number 19K15671). N.Y. and S.T. were supported by a JSPS Kiban-S Grant-in-Aid (number 17H06105). S.H.K. was supported by the Creative Materials Discovery Program (NRF-2017M3D1A1039380). The synchrotron radiation experiments were performed at the BL14B2 of SPring-8 with the approval of the Japan Synchrotron Radiation Research Institute (JASRI) (proposal numbers 2021A1664, 2021B1920, 2022A1045 and 2022A1669).

Author information

Authors and Affiliations

  1. Earth-Life Science Institute (ELSI), Tokyo Institute of Technology, Tokyo, Japan

    Daoping He, Yamei Li, Naohiro Yoshida & Ryuhei Nakamura

  2. Biofunctional Catalyst Research Team, RIKEN Center for Sustainable Resource Science (CSRS), Wako, Japan

    Daoping He, Hideshi Ooka, Akira Yamaguchi & Ryuhei Nakamura

  3. Western Seoul Center, Korea Basic Science Institute, Seoul, Republic of Korea

    Yujeong Kim & Sun Hee Kim

  4. Department of Chemistry and Nano Science, Ewha Womans University, Seoul, Republic of Korea

    Yujeong Kim & Sun Hee Kim

  5. School of Materials and Chemical Technology, Tokyo Institute of Technology, Tokyo, Japan

    Akira Yamaguchi & Ryuhei Nakamura

  6. Materials Characterization Support Team, RIKEN Center for Emergent Matter Science (CEMS), Wako, Japan

    Kiyohiro Adachi & Daisuke Hashizume

  7. School of Materials and Chemical Technology, Tokyo Institute of Technology, Yokohama, Japan

    Naohiro Yoshida & Sakae Toyoda

  8. National Institute of Information and Communications Technology, Tokyo, Japan

    Naohiro Yoshida

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  1. Daoping He
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Contributions

D. He and R.N. conceived and designed the experiments. D. He performed the experiments. H.O. performed the theoretical simulations. Y.L., N.Y. and S.T. performed the site-preference isotope measurements. Y.K., A.Y. and S.H.K. performed the EPR measurements. K.A. and D. Hashizume performed the XAFS measurements. D. He, H.O. and R.N. co-wrote the paper. All the authors discussed the results and commented on the manuscript.

Corresponding authors

Correspondence to Daoping He or Ryuhei Nakamura.

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Nature Catalysis thanks Bin Zhang and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Supplementary Information

Supplementary Figs. 1–24, Tables 1–10, note 1 and references

Supplementary Data 1

The code for numerical simulation of the Faradaic efficiency.

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He, D., Ooka, H., Li, Y. et al. Regulation of the electrocatalytic nitrogen cycle based on sequential proton–electron transfer. Nat Catal 5, 798–806 (2022). https://doi.org/10.1038/s41929-022-00833-z

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