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Performance evaluation and multidisciplinary analysis of catalytic fixation reactions by material–microbe hybrids

Nature Catalysis (2024)Cite this article

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Abstract

Hybrid systems that integrate synthetic materials with biological machinery offer opportunities for sustainable and efficient catalysis. However, the multidisciplinary and unique nature of the materials–biology interface requires researchers to draw insights from different fields. In this Perspective, using examples from the area of N2 and CO2 fixation, we provide a unified discussion of critical aspects of the material–microbe interface, simultaneously considering the requirements of physical and biological sciences that have a tangible impact on the performance of biohybrids. We first discuss the figures of merit and caveats for the evaluation of catalytic performance. Then, we reflect on the interactions and potential synergies at the materials–biology interface, as well as the challenges and opportunities for a deepened fundamental understanding of abiotic–biotic catalysis.

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Fig. 1: The material–microbe hybrid system.
Fig. 2: Figures of merit for assessing the catalysis of material–microbe hybrids on a radar plot.
Fig. 3: Fundamental questions regarding material–microbe interfaces.

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References

  1. Lewis, N. S. & Nocera, D. G. Powering the planet: chemical challenges in solar energy utilization. Proc. Natl Acad. Sci. USA 103, 15729–15735 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Lu, L. et al. Wastewater treatment for carbon capture and utilization. Nat. Sustain. 1, 750–758 (2018).

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  4. Cestellos-Blanco, S., Zhang, H., Kim, J. M., Shen, Y.-X. & Yang, P. Photosynthetic semiconductor biohybrids for solar-driven biocatalysis. Nat. Catal. 3, 245–255 (2020).

    Article  CAS  Google Scholar 

  5. Fang, X., Kalathil, S. & Reisner, E. Semi-biological approaches to solar-to-chemical conversion. Chem. Soc. Rev. 49, 4926–4952 (2020).

    Article  CAS  PubMed  Google Scholar 

  6. Logan, B. E. et al. Microbial fuel cells: methodology and technology. Environ. Sci. Technol. 40, 5181–5192 (2006).

    Article  CAS  PubMed  Google Scholar 

  7. Lovley, D. R. Bug juice: harvesting electricity with microorganisms. Nat. Rev. Microbiol. 4, 497–508 (2006).

    Article  CAS  PubMed  Google Scholar 

  8. Wheeldon, I. et al. Substrate channelling as an approach to cascade reactions. Nat. Chem. 8, 299–309 (2016).

    Article  CAS  PubMed  Google Scholar 

  9. Guan, X. et al. Maximizing light-driven CO2 and N2 fixation efficiency in quantum dot–bacteria hybrids. Nat. Catal. 5, 1019–1029 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Rodrigues, R. M. et al. Perfluorocarbon nanoemulsion promotes the delivery of reducing equivalents for electricity-driven microbial CO2 reduction. Nat. Catal. 2, 407–414 (2019).

    Article  CAS  Google Scholar 

  11. Liu, C., Sakimoto, K. K., Colon, 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  PubMed  PubMed Central  Google Scholar 

  12. 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 

  13. Göbbels, L. et al. Cysteine: an overlooked energy and carbon source. Sci. Rep. 11, 2139 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  14. Wang, Q., Kalathil, S., Pornrungroj, C., Sahm, C. D. & Reisner, E. Bacteria–photocatalyst sheet for sustainable carbon dioxide utilization. Nat. Catal. 5, 633–641 (2022).

    Article  CAS  Google Scholar 

  15. Bennett, B. D. et al. Absolute metabolite concentrations and implied enzyme active site occupancy in Escherichia coli. Nat. Chem. Biol. 5, 593–599 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Dai, X. & Shen, L. Advances and trends in omics technology development. Front. Med. 9, 911861 (2022).

    Article  Google Scholar 

  17. Rieth, A. J. & Nocera, D. G. Hybrid inorganic–biological systems: Faradaic and quantum efficiency, necessary but not sufficient. Joule 4, 2051–2055 (2020).

    Article  Google Scholar 

  18. Cao, B. et al. Silver nanoparticles boost charge-extraction efficiency in Shewanella microbial fuel cells. Science 373, 1336–1340 (2021).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  20. Popovic, M. Thermodynamic properties of microorganisms: determination and analysis of enthalpy, entropy, and Gibbs free energy of biomass, cells and colonies of 32 microorganism species. Heliyon 5, e01950 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  21. Salimijazi, F. et al. Constraints on the efficiency of engineered electromicrobial production. Joule 4, 2101–2130 (2020).

    Article  CAS  Google Scholar 

  22. Claassens, N. J., Cotton, C. A. R., Kopljar, D. & Bar-Even, A. Making quantitative sense of electromicrobial production. Nat. Catal. 2, 437–447 (2019).

    Article  CAS  Google Scholar 

  23. Fast, A. G. & Papoutsakis, E. T. Stoichiometric and energetic analyses of non-photosynthetic CO2-fixation pathways to support synthetic biology strategies for production of fuels and chemicals. Curr. Opin. Chem. Eng. 1, 380–395 (2012).

    Article  Google Scholar 

  24. Bell, E. L. et al. Biocatalysis. Nat. Rev. Methods Primers 1, 46 (2021).

    Article  CAS  Google Scholar 

  25. Costentin, C. & Savéant, J.-M. Towards an intelligent design of molecular electrocatalysts. Nat. Rev. Chem. 1, 0087 (2017).

    Article  CAS  Google Scholar 

  26. Lu, S. et al. Perfluorocarbon nanoemulsions create a beneficial O2 microenvironment in N2-fixing biological | inorganic hybrid. Chem. Catal. 1, 704–720 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Torella, J. P. et al. Efficient solar-to-fuels production from a hybrid microbial–water-splitting catalyst system. Proc. Natl Acad. Sci. USA 112, 2337–2342 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  Google Scholar 

  29. Zhang, T. et al. Improved cathode materials for microbial electrosynthesis. Energy Environ. Sci. 6, 217–224 (2013).

    Article  CAS  Google Scholar 

  30. 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  PubMed  PubMed Central  Google Scholar 

  31. Sakimoto, K. K., Liu, C., Lim, J. & Yang, P. D. Salt-induced self-assembly of bacteria on nanowire arrays. Nano Lett. 14, 5471–5476 (2014).

    Article  CAS  PubMed  Google Scholar 

  32. Lew, M. D. et al. Three-dimensional superresolution colocalization of intracellular protein superstructures and the cell surface in live Caulobacter crescentus. Proc. Natl Acad. Sci. USA 108, E1102–E1110 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. El-Naggar, M. Y. et al. Electrical transport along bacterial nanowires from Shewanella oneidensis MR-1. Proc. Natl Acad. Sci. USA 107, 18127–18131 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Reguera, G. et al. Extracellular electron transfer via microbial nanowires. Nature 435, 1098–1101 (2005).

    Article  CAS  PubMed  Google Scholar 

  35. Liu, X. et al. Microbial biofilms for electricity generation from water evaporation and power to wearables. Nat. Commun. 13, 4369 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Shi, L. et al. Extracellular electron transfer mechanisms between microorganisms and minerals. Nat. Rev. Microbiol. 14, 651–662 (2016).

    Article  CAS  PubMed  Google Scholar 

  37. Malvankar, N. S. et al. Tunable metallic-like conductivity in microbial nanowire networks. Nat. Nanotechnol. 6, 573–579 (2011).

    Article  PubMed  Google Scholar 

  38. Ho Choi, S., Kim, B. & Frisbie, C. D. Electrical resistance of long conjugated molecular wires. Science 320, 1482–1486 (2008).

    Article  PubMed  Google Scholar 

  39. Bezerra, E. F. S., Carvalho, C. L. C., Gerôncio, E. T. S., Cantanhêde, W. & Luz, R. A. S. in Advances in Bioelectrochemistry Vol. 1 (ed. Crespilho, F. N.) 35–51 (Springer, 2022).

  40. Jiang, X. C. et al. Probing electron transfer mechanisms in Shewanella oneidensis MR-1 using a nanoelectrode platform and single-cell imaging. Proc. Natl Acad. Sci. USA 107, 16806–16810 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Smart, A. G. Two experiments, two takes on electric bacteria. Phys. Today 63, 18–20 (2010).

    Article  Google Scholar 

  42. Brown, K. A., Dayal, S., Ai, X., Rumbles, G. & King, P. W. Controlled assembly of hydrogenase–CdTe nanocrystal hybrids for solar hydrogen production. J. Am. Chem. Soc. 132, 9672–9680 (2010).

    Article  CAS  PubMed  Google Scholar 

  43. Newman, D. K. & Kolter, R. A role for excreted quinones in extracellular electron transfer. Nature 405, 94–97 (2000).

    Article  CAS  PubMed  Google Scholar 

  44. Baker, L. A. Perspective and prospectus on single-entity electrochemistry. J. Am. Chem. Soc. 140, 15549–15559 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Snowden, M. E. et al. Scanning electrochemical cell microscopy: theory and experiment for quantitative high resolution spatially-resolved voltammetry and simultaneous ion-conductance measurements. Anal. Chem. 84, 2483–2491 (2012).

    Article  CAS  PubMed  Google Scholar 

  46. Mao, X., Liu, C., Hesari, M., Zou, N. & Chen, P. Super-resolution imaging of non-fluorescent reactions via competition. Nat. Chem. 11, 687–694 (2019).

    Article  CAS  PubMed  Google Scholar 

  47. Raj, A., van den Bogaard, P., Rifkin, S. A., van Oudenaarden, A. & Tyagi, S. Imaging individual mRNA molecules using multiple singly labeled probes. Nat. Methods 5, 877–879 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. 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  PubMed  Google Scholar 

  49. Su, Y. et al. Close-packed nanowire–bacteria hybrids for efficient solar-driven CO2 fixation. Joule 4, 800–811 (2020).

    Article  CAS  Google Scholar 

  50. Yang, C. et al. Carbon dots-fed Shewanella oneidensis MR-1 for bioelectricity enhancement. Nat. Commun. 11, 1379 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Zhang, R. et al. Proteomic and metabolic elucidation of solar-powered biomanufacturing by bio–abiotic hybrid system. Chem 6, 234–249 (2020).

    Article  CAS  Google Scholar 

  52. Orth, J. D., Thiele, I., Palsson & B, O. What is flux balance analysis? Nat. Biotechnol. 28, 245–248 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Law, R. C., Lakhani, A., O’Keeffe, S., Ersan, S. & Park, J. O. Integrative metabolic flux analysis reveals an indispensable dimension of phenotypes. Curr. Opin. Biotechnol. 75, 102701 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Kitano, H. Systems biology: a brief overview. Science 295, 1662–1664 (2002).

    Article  CAS  PubMed  Google Scholar 

  55. Yang, P. & Tarascon, J.-M. Towards systems materials engineering. Nat. Mater. 11, 560–563 (2012).

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

C.L. acknowledges support from the National Institute of Health (R35GM138241 and R01ES032668), the Sloan Research Fellowship from the Alfred P. Sloan Foundation and the Jeffery and Helo Zink Endowed Professional Development Term Chair. Whereas the manuscript was written by human researchers, the final text was fed to ChatGPT to check for grammar and spelling issues.

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  1. These authors contributed equally: Xun Guan, Yongchao Xie.

Authors and Affiliations

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

    Xun Guan, Yongchao Xie & Chong Liu

  2. California NanoSystems Institute, University of California Los Angeles, Los Angeles, CA, USA

    Chong Liu

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  1. Xun Guan
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X.G. wrote the initial draught. All the authors contributed to the discussion, reviewing and editing of the manuscript.

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Correspondence to Chong Liu.

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Nature Catalysis thanks Kylie Vincent and Xiulai Chen for their contribution to the peer review of this work.

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Guan, X., Xie, Y. & Liu, C. Performance evaluation and multidisciplinary analysis of catalytic fixation reactions by material–microbe hybrids. Nat Catal (2024). https://doi.org/10.1038/s41929-024-01151-2

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