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.

  • Article
  • Published:

Perfluorocarbon nanoemulsion promotes the delivery of reducing equivalents for electricity-driven microbial CO2 reduction

Nature Catalysis volume 2, pages 407–414 (2019)Cite this article

Subjects

Abstract

Combining inorganic catalysts with CO2-fixing microorganisms has displayed a high efficiency for electricity-driven CO2 reduction. However, the maximum throughput can be limited by the low solubility of mediators, such as H2, that deliver reducing equivalents from the electrodes to the microbes. Here we report that the introduction of a biocompatible perfluorocarbon nanoemulsion as a H2 carrier increases the throughput of CO2 reduction into acetic acid by 190%. With the acetogen Sporomusa ovata as a model system, an average acetate titre of 6.4 ± 1.1 g l−1 (107 mM) was achieved in four days with close to 100% Faradaic efficiency. This is equivalent to a productivity of 1.1 mM h−1, among the highest in bioelectrochemical systems. A mechanistic investigation shows that the non-specific binding of perfluorocarbon nanoemulsions promotes the kinetics of H2 transfer and subsequent oxidation by more than threefold. Introducing nanoscale gas carriers is viable to alleviate throughput bottlenecks in the electricity-driven microbial CO2 reduction into commodity chemicals.

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

Access options

Buy this article

  • Purchase on SpringerLink
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Schematic of the hybrid system that integrates water-splitting catalysts with CO2-fixing microorganisms.
Fig. 2: The introduction of PFC nanoemulsions increases the productivity of CO2 reduction.
Fig. 3: Flow cytometry analysis indicates non-specific binding between the nanoemulsion and bacteria.
Fig. 4: Investigation of the local H2 concentration and transfer kinetics.

Similar content being viewed by others

Data availability

The data that support the plots within this paper and other findings of this study are available from the corresponding author upon reasonable request.

References

  1. Chu, S. & Majumdar, A. Opportunities and challenges for a sustainable energy future. Nature 488, 294–303 (2012).

    Article  CAS  Google Scholar 

  2. Nocera, D. G. Solar fuels and solar chemicals industry. Acc. Chem. Res. 50, 616–619 (2017).

    Article  CAS  Google Scholar 

  3. Jia, J. et al. Heterogeneous catalytic hydrogenation of CO2 by metal oxides: defect engineering—perfecting imperfection. Chem. Soc. Rev. 46, 4631–4644 (2017).

    Article  CAS  Google Scholar 

  4. Dinh, C.-T. et al. CO2 electroreduction to ethylene via hydroxide-mediated copper catalysis at an abrupt interface. Science 360, 783–787 (2018).

    Article  CAS  Google Scholar 

  5. White, J. L. et al. Light-driven heterogeneous reduction of carbon dioxide: photocatalysts and photoelectrodes. Chem. Rev. 115, 12888–12935 (2015).

    Article  CAS  Google Scholar 

  6. Jouny, M., Luc, W. & Jiao, F. High-rate electroreduction of carbon monoxide to multi-carbon products. Nat. Catal. 1, 748–755 (2018).

    Article  Google Scholar 

  7. Li, J. et al. Efficient electrocatalytic CO2 reduction on a three-phase interface. Nat. Catal. 1, 592–600 (2018).

    Article  Google Scholar 

  8. Bushuyev, O. S. et al. What should we make with CO2 and how can we make it? Joule 2, 825–832 (2018).

    Article  CAS  Google Scholar 

  9. Appel, A. M. et al. Frontiers, opportunities, and challenges in biochemical and chemical catalysis of CO2 fixation. Chem. Rev. 113, 6621–6658 (2013).

    Article  CAS  Google Scholar 

  10. 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  Google Scholar 

  11. Kornienko, N., Zhang, J. Z., Sakimoto, K. K., Yang, P. & Reisner, E. Interfacing Nature’s catalytic machinery with synthetic materials for semi-artificial photosynthesis. Nat. Nanotechnol. 13, 890–899 (2018).

    Article  CAS  Google Scholar 

  12. Li, H. et al. Integrated electromicrobial conversion of CO2 to higher alcohols. Science 335, 1596–1596 (2012).

    Article  CAS  Google Scholar 

  13. Sakimoto, K. K., Wong, A. B. & Yang, P. Self-photosensitization of nonphotosynthetic bacteria for solar-to-chemical production. Science 351, 74–77 (2015).

    Article  Google Scholar 

  14. Claassens, N. J., Sousa, D. Z., dos Santos, V. A. P. M., de Vos, W. M. & van der Oost, J. Harnessing the power of microbial autotrophy. Nat. Rev. Microbiol. 14, 692–706 (2016).

    Article  CAS  Google Scholar 

  15. Brown, K. A. et al. Light-driven dinitrogen reduction catalyzed by a CdS:nitrogenase MoFe protein biohybrid. Science 352, 448–450 (2016).

    Article  CAS  Google Scholar 

  16. Liao, J. C., Mi, L., Pontrelli, S. & Luo, S. Fuelling the future: microbial engineering for the production of sustainable biofuels. Nat. Rev. Microbiol. 14, 288–304 (2016).

    Article  CAS  Google Scholar 

  17. Cornejo, J. A., Sheng, H., Edri, E., M. Ajo-Franklin, C. & Frei, H. Nanoscale membranes that chemically isolate and electronically wire up the abiotic/biotic interface. Nat. Commun. 9, 2263 (2018).

    Article  Google Scholar 

  18. Rabaey, K. & Rozendal, R. A. Microbial electrosynthesis—revisiting the electrical route for microbial production. Nat. Rev. Microbiol. 8, 706–716 (2010).

    Article  CAS  Google Scholar 

  19. Sakimoto, K. K. et al. Physical biology of the materials–microorganism interface. J. Am. Chem. Soc. 140, 1978–1985 (2018).

    Article  CAS  Google Scholar 

  20. Milton, R. D., Wang, T., Knoche, K. L. & Minteer, S. D. Tailoring biointerfaces for electrocatalysis. Langmuir 32, 2291–2301 (2016).

    Article  CAS  Google Scholar 

  21. Zhang, T. More efficient together. Science 350, 738–739 (2015).

    Article  CAS  Google Scholar 

  22. Liu, C., Sakimoto, K. K., Colón, B. C., Silver, P. A. & Nocera, D. G. Ambient nitrogen reduction cycle using a hybrid inorganic–biological system. Proc. Natl Acad. Sci. USA 114, 6450–6455 (2017).

    Article  CAS  Google Scholar 

  23. Lubitz, W., Ogata, H., Rüdiger, O. & Reijerse, E. Hydrogenases. Chem. Rev. 114, 4081–4148 (2014).

    Article  CAS  Google Scholar 

  24. Liu, C., Nangle, S. N., Colón, B. C., Silver, P. A. & Nocera, D. G. 13C-Labeling the carbon-fixation pathway of a highly efficient artificial photosynthetic system. Faraday Discuss. 198, 529–537 (2017).

    Article  CAS  Google Scholar 

  25. Gevantman, L. H. in CRC Handbook of Chemistry and Physics (ed. Haynes, W. M.) Ch. 5 (CRC Press, 2015).

  26. Watanabe, K., Manefield, M., Lee, M. & Kouzuma, A. Electron shuttles in biotechnology. Curr. Opin. Biotechnol. 20, 633–641 (2009).

    Article  CAS  Google Scholar 

  27. Squires, J. E. Artificial blood. Science 295, 1002–1005 (2002).

    Article  CAS  Google Scholar 

  28. Ju, L. K., Lee, J. F. & Armiger, W. B. Enhancing oxygen transfer in bioreactors by perfluorocarbon emulsions. Biotechnol. Prog. 7, 323–329 (1991).

    Article  CAS  Google Scholar 

  29. Yamamoto, S., Honda, H., Shiragami, N. & Unno, H. Enhancement of autotrophic growth rate of Alcaligenes eutrophus in a medium containing perfluorocarbon under low oxygen partial pressure. Biotechnol. Lett. 14, 733–736 (1992).

    Article  CAS  Google Scholar 

  30. Dissolving Gases in FLUTEC Liquids (F2 Chemicals Ltd, 2005); http://f2chemicals.com/pdf/technical/Gas%20solubility.pdf

  31. Sletten, E. M. & Swager, T. M. Readily accessible multifunctional fluorous emulsions. Chem. Sci. 7, 5091–5097 (2016).

    Article  CAS  Google Scholar 

  32. Sletten, E. M. & Swager, T. M. Fluorofluorophores: fluorescent fluorous chemical tools spanning the visible spectrum. J. Am. Chem. Soc. 136, 13574–13577 (2014).

    Article  CAS  Google Scholar 

  33. Möller, B., Oßmer, R., Howard, B. H., Gottschalk, G. & Hippe, H. Sporomusa, a new genus of gram-negative anaerobic bacteria including Sporomusa sphaeroides spec. nov. and Sporomusa ovata spec nov. Arch. Microbiol. 139, 388–396 (1984).

    Article  Google Scholar 

  34. Nevin, K. P., Woodard, T. L., Franks, A. E., Summers, Z. M. & Lovley, D. R. Microbial electrosynthesis: feeding microbes electricity to convert carbon dioxide and water to multicarbon extracellular organic compounds. MBIO 1, e00103 (2010).

    Article  Google Scholar 

  35. Liu, C. et al. Nanowire–bacteria hybrids for unassisted solar carbon dioxide fixation to value-added chemicals. Nano Lett. 15, 3634–3639 (2015).

    Article  CAS  Google Scholar 

  36. Aryal, N., Tremblay, P. L., Lizak, D. M. & Zhang, T. Performance of different Sporomusa species for the microbial electrosynthesis of acetate from carbon dioxide. Bioresour. Technol. 233, 184–190 (2017).

    Article  CAS  Google Scholar 

  37. LaBelle, E. V. & May, H. D. Energy efficiency and productivity enhancement of microbial electrosynthesis of acetate. Front. Microbiol. 8, 756 (2017).

    Article  Google Scholar 

  38. Paseka, I. & Velicka, J. Hydrogen evolution and hydrogen sorption on amorphous smooth Me−P(x) (Me = Ni, Co and Fe−Ni) electrodes. Electrochim. Acta 42, 237–242 (1997).

    Article  CAS  Google Scholar 

  39. Jiang, N., You, B., Sheng, M. & Sun, Y. Electrodeposited cobalt–phosphorous-derived films as competent bifunctional catalysts for overall water splitting. Angew. Chem. Int. Ed. 54, 6251–6254 (2015).

    Article  CAS  Google Scholar 

  40. Haas, T., Krause, R., Weber, R., Demler, M. & Schmid, G. Technical photosynthesis involving CO2 electrolysis and fermentation. Nat. Catal. 1, 32–39 (2018).

    Article  Google Scholar 

  41. Bard, A. J. & Faulkner, L. R. Electrochemical Methods: Fundamentals and Applications 2nd edn, Ch. 9 (John Wiley & Sons, Hoboken, 2001).

  42. Konopka, S. J. & McDuffie, B. Diffusion coefficients of ferri- and ferrocyanide ions in aqueous media, using twin-electrode thin-layer electrochemistry. Anal. Chem. 42, 1741–1746 (1970).

    Article  CAS  Google Scholar 

  43. Jeremiasse, A. W., Hamelers, H. V. M., Kleijn, J. M. & Buisman, C. J. N. Use of biocompatible buffers to reduce the concentration overpotential for hydrogen evolution. Environ. Sci. Technol. 43, 6882–6887 (2009).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We acknowledge B. Natinsky for the diffusion ordered spectroscopy experiments. We also thank S. Kosuri for the use of flow cytometry facilities and the Molecular Instrumentation Center at the University of California, Los Angeles for sample characterizations. D.A.E. acknowledges the financial support of an NIH training grant (5T32GM067555-12). J.A.I. is supported by a Eugene V. Cota-Robles fellowship. E.M.S. and C.L. acknowledge start-up funds from the University of California, Los Angeles and the financial support of the Jeffery and Helo Zink Endowed Professional Development Term Chair (to C.L.) and the John D. McTague Career Development Term Chair (to E.M.S.).

Author information

Authors and Affiliations

  1. Department of Chemistry and Biochemistry, University of California, Los Angeles, Los Angeles, CA, USA

    Roselyn M. Rodrigues, Xun Guan, Jesus A. Iñiguez, Daniel A. Estabrook, John O. Chapman, Shuyuan Huang, Ellen M. Sletten & Chong Liu

Authors
  1. Roselyn M. Rodrigues
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xun Guan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jesus A. Iñiguez
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Daniel A. Estabrook
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. John O. Chapman
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Shuyuan Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Ellen M. Sletten
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Chong Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

C.L. supervised the project. C.L. and R.M.R. designed experiments and wrote the paper. R.M.R. conducted and coordinated the majority of the experiments with the assistance of S.H. D.A.E. and J.O.C. prepared the nanoemulsions under supervision of E.M.S. X.G. conducted the RDE experiments. J.A.I. performed experiments of flow cytometry. All the authors discussed the results and assisted during the manuscript preparation.

Corresponding author

Correspondence to Chong Liu.

Ethics declarations

Competing interests

The authors declare no competing interests.

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, Supplementary Discussion, Supplementary Tables 1–4, Supplementary Figures 1–11, Supplementary References

Reporting Summary

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rodrigues, R.M., Guan, X., Iñiguez, J.A. et al. Perfluorocarbon nanoemulsion promotes the delivery of reducing equivalents for electricity-driven microbial CO2 reduction. Nat Catal 2, 407–414 (2019). https://doi.org/10.1038/s41929-019-0264-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41929-019-0264-0

This article is cited by

Search

Advanced search

Quick links

Nature Briefing: Translational Research

Sign up for the Nature Briefing: Translational Research newsletter — top stories in biotechnology, drug discovery and pharma.

Get what matters in translational research, free to your inbox weekly. Sign up for Nature Briefing: Translational Research