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Single-cell multimodal imaging uncovers energy conversion pathways in biohybrids

Nature Chemistry volume 15, pages 1400–1407 (2023)Cite this article

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Abstract

Microbe–semiconductor biohybrids, which integrate microbial enzymatic synthesis with the light-harvesting capabilities of inorganic semiconductors, have emerged as promising solar-to-chemical conversion systems. Improving the electron transport at the nano–bio interface and inside cells is important for boosting conversion efficiencies, yet the underlying mechanism is challenging to study by bulk measurements owing to the heterogeneities of both constituents. Here we develop a generalizable, quantitative multimodal microscopy platform that combines multi-channel optical imaging and photocurrent mapping to probe such biohybrids down to single- to sub-cell/particle levels. We uncover and differentiate the critical roles of different hydrogenases in the lithoautotrophic bacterium Ralstonia eutropha for bioplastic formation, discover this bacterium’s surprisingly large nanoampere-level electron-uptake capability, and dissect the cross-membrane electron-transport pathways. This imaging platform, and the associated analytical framework, can uncover electron-transport mechanisms in various types of biohybrid, and potentially offers a means to use and engineer R. eutropha for efficient chemical production coupled with photocatalytic materials.

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Fig. 1: Microbe–semiconductor biohybrids and multimodal imaging platform.
Fig. 2: Roles of hydrogenases in bioplastic formation under lithoautotrophic growth.
Fig. 3: Electron uptake of R. eutropha from photoelectrodes in integrated biohybrids.
Fig. 4: Schematics of dominant electron-transport pathways for bioplastic formation in biohybrid systems.
Fig. 5: Players in electron transport across the microbe–semiconductor interface.

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Data availability

All data are available in the main text or the Supplementary Information. Raw data supporting the findings of this study are available upon reasonable request. Source data are provided with this paper.

Code availability

MATLAB codes for data analysis and simulations supporting the findings of this study are provided with this paper.

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Acknowledgements

This research is supported by the US Department of Energy (Office of Science, Office of Biological and Environmental Research, Biological Systems Science Division, under award no. DE-SC0020179). It uses Cornell Center for Materials Research Shared Facilities supported through the NSF MRSEC programme (DMR-1719875). The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript. We thank C. Brigham at Wentworth Institute of Technology for providing the R. eutropha H16 strain, W. Metcalf at the University of Illinois at Urbana Champaign for E. coli WM3064, O. Lenz at Technische Universität Berlin for R. eutropha ΔhoxH, L. Krzeminski formerly at Cornell University for constructing tagged E. coli strains, and S. Murphy, T. Doerr and A. Schmitz at Cornell University for discussions on genetics.

Author information

Author notes

  1. Bing Fu

    Present address: Department of Biomedical Engineering, City University of Hong Kong, Hong Kong, China

  2. Xianwen Mao

    Present address: Department of Materials Science and Engineering, Institute of Functional Intelligent Materials, and Centre for Advanced 2D Materials, National University of Singapore, Singapore, Singapore

  3. Won Jung

    Present address: Department of Chemistry and Chemical Biology, Harvard University, Cambridge, MA, USA

  4. Danielle H. Francis

    Present address: Friends School of Baltimore, Baltimore, MD, USA

  5. These authors contributed equally: Bing Fu, Xianwen Mao.

Authors and Affiliations

  1. Department of Chemistry and Chemical Biology, Cornell University, Ithaca, NY, USA

    Bing Fu, Xianwen Mao, Youngchan Park, Zhiheng Zhao, Tianlei Yan, Won Jung, Danielle H. Francis, Wenjie Li & Peng Chen

  2. Department of Biological and Environmental Engineering, Cornell University, Ithaca, NY, USA

    Brooke Pian, Farshid Salimijazi & Buz Barstow

  3. Department of Materials Science and Engineering, Cornell University, Ithaca, NY, USA

    Mokshin Suri

  4. Robert F. Smith School of Chemical and Biomolecular Engineering, Cornell University, Ithaca, NY, USA

    Tobias Hanrath

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Contributions

B.F. constructed strains. X.M. synthesized semiconductor materials. B.F. and X.M. designed experiments, performed measurements, wrote codes and analysed data. Y.P., Z.Z. and T.Y. contributed to strain construction, materials synthesis and/or imaging experiments, where Y.P. and Z.Z. contributed equally. W.J. and D.H.F. contributed to cell culturing. W.L. helped with instrument set-up. B.P., F.S. and B.B. contributed to genetic engineering. M.S. and T.H. contributed to discussions on materials synthesis. P.C. conceived and directed the research. B.F., X.M. and P.C. wrote the manuscript.

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Correspondence to Peng Chen.

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Fu, B., Mao, X., Park, Y. et al. Single-cell multimodal imaging uncovers energy conversion pathways in biohybrids. Nat. Chem. 15, 1400–1407 (2023). https://doi.org/10.1038/s41557-023-01285-z

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