Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Biomimetic active sites on monolayered metal–organic frameworks for artificial photosynthesis

Abstract

Enzymes have evolved to catalyse challenging chemical transformations with high efficiency and selectivity. Although a number of artificial systems have been developed to recapitulate the catalytic activity of natural enzymes, they are mostly limited to catalysing relatively simple reactions owing to their ability to mimic only the active metal centres of natural enzymes, without incorporating the proximal amino acids or cofactors. Here we report a metal–organic framework-based artificial enzyme (metal–organic–zyme, MOZ) by integrating active metal centres, proximal amino acids and other cofactors into a tunable metal–organic framework monolayer. We design two libraries of MOZs to perform photocatalytic CO2 reduction and water oxidation reactions. Through tuning the incorporated amino acids in the MOZs, we systematically optimize the activity and selectivity of these libraries. Combining these optimized MOZs into a single system realizes complete artificial photosynthesis in the reaction of (1 + n)CO2 + 2H2O → CH4 + nCO + (2 + n/2)O2.

This is a preview of subscription content, access via your institution

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

Fig. 1: Design of MOZs.
Fig. 2: MOZ construction and optimization for CO2RR.
Fig. 3: Characterization of MOZs.
Fig. 4: Photocatalytic CO2RR by MOZs.
Fig. 5: Photocatalytic WOR by MOZs.
Fig. 6: Artificial photosynthesis by MOZs.

Data availability

Data relating to the characterization data of materials, detection of products, mechanistic studies, computational studies and NMR spectra are available in the Supplementary Information. Crystallographic data for the structures reported in this article have been deposited at the Cambridge Crystallographic Data Centre, under deposition numbers CCDC 2000080 (Ur). Copies of the data can be obtained free of charge via https://www.ccdc.cam.ac.uk/structures/. Cartesian coordinates of optimized structures are available in Supplementary Data 1. All additional data are available from the authors upon reasonable request.

References

  1. Lee, D.-S., Nioche, P., Hamberg, M. & Raman, C. S. Structural insights into the evolutionary paths of oxylipin biosynthetic enzymes. Nature 455, 363–368 (2008).

    Article  CAS  PubMed  Google Scholar 

  2. Berggren, G. et al. Biomimetic assembly and activation of [FeFe]-hydrogenases. Nature 499, 66–69 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Helm, M. L., Stewart, M. P., Bullock, R. M., DuBois, M. R. & DuBois, D. L. A synthetic nickel electrocatalyst with a turnover frequency above 100,000 s−1 for H2 production. Science 333, 863–866 (2011).

    Article  CAS  PubMed  Google Scholar 

  4. Camara, J. M. & Rauchfuss, T. B. Combining acid–base, redox and substrate binding functionalities to give a complete model for the [FeFe]-hydrogenase. Nat. Chem. 4, 26–30 (2012).

    Article  CAS  Google Scholar 

  5. Ott, S., Kritikos, M., Åkermark, B., Sun, L. & Lomoth, R. A biomimetic pathway for hydrogen evolution from a model of the iron hydrogenase active site. Angew. Chem. Int. Ed. Engl. 43, 1006–1009 (2004).

    Article  CAS  PubMed  Google Scholar 

  6. Wu, J. et al. Nanomaterials with enzyme-like characteristics (nanozymes): next-generation artificial enzymes (II). Chem. Soc. Rev. 48, 1004–1076 (2019).

    Article  CAS  PubMed  Google Scholar 

  7. Takezawa, H., Shitozawa, K. & Fujita, M. Enhanced reactivity of twisted amides inside a molecular cage. Nat. Chem. 12, 574–578 (2020).

    Article  CAS  PubMed  Google Scholar 

  8. Rabone, J. et al. An adaptable peptide-based porous material. Science 329, 1053–1057 (2010).

    Article  CAS  PubMed  Google Scholar 

  9. Deng, H. et al. Large-pore apertures in a series of metal–organic frameworks. Science 336, 1018–1023 (2012).

    Article  CAS  PubMed  Google Scholar 

  10. Xiao, D. J. et al. Oxidation of ethane to ethanol by N2O in a metal–organic framework with coordinatively unsaturated iron(II) sites. Nat. Chem. 6, 590–595 (2014).

    Article  CAS  PubMed  Google Scholar 

  11. Nath, I., Chakraborty, J. & Verpoort, F. Metal organic frameworks mimicking natural enzymes: a structural and functional analogy. Chem. Soc. Rev. 45, 4127–4170 (2016).

    Article  CAS  PubMed  Google Scholar 

  12. Furukawa, H., Cordova Kyle, E., O’Keeffe, M. & Yaghi Omar, M. The chemistry and applications of metal–organic frameworks. Science 341, 1230444 (2013).

    Article  PubMed  Google Scholar 

  13. Li, L. et al. Ethane/ethylene separation in a metal–organic framework with iron-peroxo sites. Science 362, 443–446 (2018).

    Article  CAS  PubMed  Google Scholar 

  14. Ji, S. et al. Matching the kinetics of natural enzymes with a single-atom iron nanozyme. Nat. Catal. 4, 407–417 (2021).

    Article  CAS  Google Scholar 

  15. Scott, S., Zhao, H., Dey, A. & Gunnoe, T. B. Nano-apples and orange-zymes. ACS Catal. 10, 14315–14317 (2020).

    Article  CAS  Google Scholar 

  16. Dai, R. et al. Electron crystallography reveals atomic structures of metal–organic nanoplates with M123-O)83-OH)82-OH)6 (M = Zr, Hf) secondary building units. Inorg. Chem. 56, 8128–8134 (2017).

    Article  CAS  PubMed  Google Scholar 

  17. Rao, H., Schmidt, L. C., Bonin, J. & Robert, M. Visible-light-driven methane formation from CO2 with a molecular iron catalyst. Nature 548, 74–77 (2017).

    Article  CAS  PubMed  Google Scholar 

  18. Mariano, R. G., McKelvey, K., White, H. S. & Kanan, M. W. Selective increase in CO2 electroreduction activity at grain–boundary surface terminations. Science 358, 1187–1192 (2017).

    Article  CAS  PubMed  Google Scholar 

  19. García de Arquer, F. P. et al. CO2 electrolysis to multicarbon products at activities greater than 1 A cm−2. Science 367, 661–666 (2020).

    Article  PubMed  Google Scholar 

  20. Morales-Guio, C. G. et al. Improved CO2 reduction activity towards C2+ alcohols on a tandem gold on copper electrocatalyst. Nat. Catal. 1, 764–771 (2018).

    Article  CAS  Google Scholar 

  21. Liu, C., Colón, B. C., Ziesack, M., Silver, P. A. & Nocera, D. G. Water splitting–biosynthetic system with CO2 reduction efficiencies exceeding photosynthesis. Science 352, 1210–1213 (2016).

    Article  CAS  PubMed  Google Scholar 

  22. Smith, P. T., Kim, Y., Benke, B. P., Kim, K. & Chang, C. J. Supramolecular tuning enables selective oxygen reduction catalyzed by cobalt porphyrins for direct electrosynthesis of hydrogen peroxide. Angew. Chem. Int. Ed. Engl. 59, 4902–4907 (2020).

    Article  CAS  PubMed  Google Scholar 

  23. Ju, W. et al. Unraveling mechanistic reaction pathways of the electrochemical CO2 reduction on Fe–N–C single-site catalysts. ACS Energy Lett. 4, 1663–1671 (2019).

    Article  CAS  Google Scholar 

  24. Rao, H., Lim, C.-H., Bonin, J., Miyake, G. M. & Robert, M. Visible-light-driven conversion of CO2 to CH4 with an organic sensitizer and an iron porphyrin catalyst. J. Am. Chem. Soc. 140, 17830–17834 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Costentin, C., Drouet, S., Passard, G., Robert, M. & Savéant, J.-M. Proton-coupled electron transfer cleavage of heavy-atom bonds in electrocatalytic processes. Cleavage of a C–O bond in the catalyzed electrochemical reduction of CO2. J. Am. Chem. Soc. 135, 9023–9031 (2013).

    Article  CAS  PubMed  Google Scholar 

  26. Gotico, P. et al. Second-sphere biomimetic multipoint hydrogen-bonding patterns to boost CO2 reduction of iron porphyrins. Angew. Chem. Int. Ed. Engl. 58, 4504–4509 (2019).

    Article  CAS  PubMed  Google Scholar 

  27. Davethu, P. A. & de Visser, S. P. CO2 reduction on an iron-porphyrin center: a computational study. J. Phy. Chem. A 123, 6527–6535 (2019).

    Article  CAS  Google Scholar 

  28. Zhai, Q. et al. Photocatalytic conversion of carbon dioxide with water into methane: platinum and copper(I) oxide co-catalysts with a core–shell structure. Angew. Chem. Int. Ed. Engl. 52, 5776–5779 (2013).

    Article  CAS  PubMed  Google Scholar 

  29. Xie, S., Wang, Y., Zhang, Q., Deng, W. & Wang, Y. MgO- and Pt-promoted TiO2 as an efficient photocatalyst for the preferential reduction of carbon dioxide in the presence of water. ACS Catal. 4, 3644–3653 (2014).

    Article  CAS  Google Scholar 

  30. Wang, Y. et al. High efficiency photocatalytic conversion of CO2 with H2O over Pt/TiO2 nanoparticles. RSC Adv. 4, 44442–44451 (2014).

    Article  CAS  Google Scholar 

  31. Long, R. et al. Isolation of Cu atoms in Pd lattice: forming highly selective sites for photocatalytic conversion of CO2 to CH4. J. Am. Chem. Soc. 139, 4486–4492 (2017).

    Article  CAS  PubMed  Google Scholar 

  32. Li, R. et al. Integration of an inorganic semiconductor with a metal–organic framework: a platform for enhanced gaseous photocatalytic reactions. Adv. Mater. 26, 4783–4788 (2014).

    Article  CAS  PubMed  Google Scholar 

  33. Duan, L. et al. A molecular ruthenium catalyst with water-oxidation activity comparable to that of photosystem II. Nat. Chem. 4, 418–423 (2012).

    Article  CAS  PubMed  Google Scholar 

  34. Wang, C., Wang, J.-L. & Lin, W. Elucidating molecular iridium water oxidation catalysts using metal–organic frameworks: a comprehensive structural, catalytic, spectroscopic, and kinetic study. J. Am. Chem. Soc. 134, 19895–19908 (2012).

    Article  CAS  PubMed  Google Scholar 

  35. Duan, L., Xu, Y., Zhang, P., Wang, M. & Sun, L. Visible light-driven water oxidation by a molecular ruthenium catalyst in homogeneous system. Inorg. Chem. 49, 209–215 (2010).

    Article  CAS  PubMed  Google Scholar 

  36. Han, J. et al. Metal–organic framework immobilized cobalt oxide nanoparticles for efficient photocatalytic water oxidation. J. Mater. Chem. A 3, 20607–20613 (2015).

    Article  CAS  Google Scholar 

  37. Maeda, K. et al. Photocatalyst releasing hydrogen from water. Nature 440, 295–295 (2006).

    Article  CAS  PubMed  Google Scholar 

  38. Wang, Q. et al. Oxysulfide photocatalyst for visible-light-driven overall water splitting. Nat. Mater. 18, 827–832 (2019).

    Article  CAS  PubMed  Google Scholar 

  39. Kumar, A. et al. Biochar-templated g-C3N4/Bi2O2CO3/CoFe2O4 nano-assembly for visible and solar assisted photo-degradation of paraquat, nitrophenol reduction and CO2 conversion. Chem. Eng. J. 339, 393–410 (2018).

    Article  CAS  Google Scholar 

  40. Jiang, Z. et al. A hierarchical Z‑scheme α-Fe2O3/g-C3N4 hybrid for enhanced photocatalytic CO2 reduction. Adv. Mater. 30, 1706108 (2018).

    Article  Google Scholar 

  41. Wang, J. et al. Exceptional photocatalytic activities for CO2 conversion on AlO bridged g-C3N4/α-Fe2O3 z-scheme nanocomposites and mechanism insight with isotopesZ. Appl. Catal. B 221, 459–466 (2018).

    Article  CAS  Google Scholar 

  42. Bae, K.-L., Kim, J., Lim, C. K., Nam, K. M. & Song, H. Colloidal zinc oxide-copper(I) oxide nanocatalysts for selective aqueous photocatalytic carbon dioxide conversion into methane. Nat. Commun. 8, 1156 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  43. Jin, J., Yu, J., Guo, D., Cui, C. & Ho, W. A hierarchical Z-scheme CdS–WO3 photocatalyst with enhanced CO2 reduction activity. Small 11, 5262–5271 (2015).

    Article  CAS  PubMed  Google Scholar 

  44. Aguirre, M. E., Zhou, R., Eugene, A. J., Guzman, M. I. & Grela, M. A. Cu2O/TiO2 heterostructures for CO2 reduction through a direct Z-scheme: protecting Cu2O from photocorrosion. Appl. Catal. B 217, 485–493 (2017).

    Article  CAS  Google Scholar 

  45. Shen, Y. et al. Artificial trees for artificial photosynthesis: construction of dendrite-structured α-Fe2O3/g-C3N4 Z-scheme system for efficient CO2 reduction into solar fuels. ACS Appl. Energy Mater. 3, 6561–6572 (2020).

    Article  CAS  Google Scholar 

  46. Han, Q. et al. Elegant construction of ZnIn2S4/BiVO4 hierarchical heterostructures as direct Z-scheme photocatalysts for efficient CO2 photoreduction. ACS Appl. Mater. Interfaces 13, 15092–15100 (2021).

    Article  CAS  PubMed  Google Scholar 

  47. Guo, R.-t et al. Photocatalytic reduction of CO2 into CO over nanostructure Bi2S3 quantum dots/g-C3N4 composites with Z-scheme mechanism. Appl. Surf. Sci. 500, 144059 (2020).

    Article  CAS  Google Scholar 

  48. Jiang, Z. et al. Filling metal–organic framework mesopores with TiO2 for CO2 photoreduction. Nature 586, 549–554 (2020).

    Article  CAS  PubMed  Google Scholar 

  49. Liang, L. et al. Infrared light-driven CO2 overall splitting at room temperature. Joule 2, 1004–1016 (2018).

    Article  CAS  Google Scholar 

  50. Wu, L.-Y. et al. Encapsulating perovskite quantum dots in iron-based metal–organic frameworks (MOFs) for efficient photocatalytic CO2 reduction. Angew. Chem. Int. Ed. Engl. 58, 9491–9495 (2019).

    Article  CAS  PubMed  Google Scholar 

  51. Zhu, Y.-Y. et al. Merging photoredox and organometallic catalysts in a metal–organic framework significantly boosts photocatalytic activities. Angew. Chem. Int. Ed. Engl. 57, 14090–14094 (2018).

    Article  CAS  PubMed  Google Scholar 

  52. Zhu, X.-Q., Zhang, M.-T., Yu, A., Wang, C.-H. & Cheng, J.-P. Hydride, hydrogen atom, proton, and electron transfer driving forces of various five-membered heterocyclic organic hydrides and their reaction intermediates in acetonitrile. J. Am. Chem. Soc. 130, 2501–2516 (2008).

    Article  CAS  PubMed  Google Scholar 

  53. Maeda, K. Z-Scheme water splitting using two different semiconductor photocatalysts. ACS Catal. 3, 1486–1503 (2013).

    Article  CAS  Google Scholar 

  54. Sheldrick, G. M. Crystal structure refinement with SHELXL. Acta Crystallogr. C 71, 3–8 (2015).

    Article  Google Scholar 

  55. Dolomanov, O. V., Bourhis, L. J., Gildea, R. J., Howard, J. A. & Puschmann, H. OLEX2: a complete structure solution, refinement and analysis program. J. Appl. Crystallogr. 42, 339–341 (2009).

    Article  CAS  Google Scholar 

  56. Sheldrick, G. M. A short history of SHELX. Acta Crystallogr. A 64, 112–122 (2008).

    Article  CAS  PubMed  Google Scholar 

  57. Quan, Y. et al. Metal–organic layers for synergistic Lewis acid and photoredox catalysis. J. Am. Chem. Soc. 142, 1746–1751 (2020).

    Article  CAS  PubMed  Google Scholar 

  58. Chen, X. et al. Ultrathin, single-crystal WO3 nanosheets by two-dimensional oriented attachment toward enhanced photocatalystic reduction of CO2 into hydrocarbon fuels under visible light. ACS Appl. Mater. Interfaces 4, 3372–3377 (2012).

    Article  CAS  PubMed  Google Scholar 

  59. Lide, D. R. CRC Handbook of Chemistry and Physics Vol. 85 (CRC Press, 2004).

Download references

Acknowledgements

We thank F. Shi for help with scanning transmission electron microscopy. This work made use of Instruments in the Electron Microscopy Core (Research Resources Center, University of Illinois at Chicago). We thank G. Zhang, X. Jiang, C. Wang and F. Shi for helpful discussions. This work was supported by the University of Chicago and National Science Foundation (CHE-2102554). W.S. acknowledges financial support from the China Scholarship Council. Single-crystal diffraction studies were performed at ChemMatCARS, APS, ANL. ChemMatCARS is principally supported by the Divisions of Chemistry (CHE) and Materials Research (DMR), National Science Foundation, under grant NSF/CHE-1346572. Use of the Advanced Photon Source, an Office of Science User Facility operated for the US Department of Energy (DOE) Office of Science by Argonne National Laboratory, was supported by the US DOE under contract DE-AC02-06CH11357.

Author information

Authors and Affiliations

Authors

Contributions

G.L., Y.F., W.S., S.S.V. and W.L. conceived the idea and designed the project. W.L. directed and supervised the research. G.L., Y.F. and E.Y. performed the experimental works. W.S. performed the computational works. G.L., Y.F., W.S., S.S.V. and W.L. wrote the paper, with input from all other co-authors.

Corresponding author

Correspondence to Wenbin Lin.

Ethics declarations

Competing interests

The authors declare no competing interests.

Peer review information

Peer review information

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

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Methods, Notes 1–16, Figs. 1–30, Tables 1–4, NMR spectra and refs.

Supplementary Data 1

Cartesian coordinates of optimized structures.

Supplementary Data 2

Crystal structure of Ur.

Supplementary Data 3

Structure factor of Ur.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Lan, G., Fan, Y., Shi, W. et al. Biomimetic active sites on monolayered metal–organic frameworks for artificial photosynthesis. Nat Catal (2022). https://doi.org/10.1038/s41929-022-00865-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1038/s41929-022-00865-5

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing