Letter | Published:

Bacteria photosensitized by intracellular gold nanoclusters for solar fuel production

Nature Nanotechnologyvolume 13pages900905 (2018) | Download Citation

Abstract

The demand for renewable and sustainable fuel has prompted the rapid development of advanced nanotechnologies to effectively harness solar power. The construction of photosynthetic biohybrid systems (PBSs) aims to link preassembled biosynthetic pathways with inorganic light absorbers. This strategy inherits both the high light-harvesting efficiency of solid-state semiconductors and the superior catalytic performance of whole-cell microorganisms. Here, we introduce an intracellular, biocompatible light absorber, in the form of gold nanoclusters (AuNCs), to circumvent the sluggish kinetics of electron transfer for existing PBSs. Translocation of these AuNCs into non-photosynthetic bacteria enables photosynthesis of acetic acid from CO2. The AuNCs also serve as inhibitors of reactive oxygen species (ROS) to maintain high bacterium viability. With the dual advantages of light absorption and biocompatibility, this new generation of PBS can efficiently harvest sunlight and transfer photogenerated electrons to cellular metabolism, realizing CO2 fixation continuously over several days.

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References

  1. 1.

    Blankenship, R. E. et al. Comparing photosynthetic and photovoltaic efficiencies and recognizing the potential for improvement. Science 332, 805–809 (2011).

  2. 2.

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

  3. 3.

    Sakimoto, K. K., Kornienko, N. & Yang, P. Cyborgian material design for solar fuel production: the emerging photosynthetic biohybrid systems. Acc. Chem. Res. 50, 476–481 (2017).

  4. 4.

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

  5. 5.

    Malvankar, N. S. & Lovley, D. R. Microbial nanowires for bioenergy applications. Curr. Opin. Biotechnol. 27, 88–95 (2014).

  6. 6.

    Liu, C., Colon, 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).

  7. 7.

    Sakimoto, K. K., Wong, A. B. & Yang, P. Self-photosensitization of nonphotosynthetic bacteria for solar-to-chemical production. Science 351, 74–77 (2016).

  8. 8.

    Gronenberg, L. S., Marcheschi, R. J. & Liao, J. C. Next generation biofuel engineering in prokaryotes. Curr. Opin. Chem. Biol. 17, 462–471 (2013).

  9. 9.

    Lovley, D. R. Powering microbes with electricity: direct electron transfer from electrodes to microbes. Environ. Microbiol. Rep. 3, 27–35 (2011).

  10. 10.

    Silhavy, T., Kahne, D. & Walker, S. The bacterial cell envelope. Cold Spring Harb. Perspect. Biol. 2, 1–16 (2010).

  11. 11.

    Chen, L. Y., Wang, C. W., Yuan, Z. & Chang, H. T. Fluorescent gold nanoclusters: recent advances in sensing and imaging. Anal. Chem. 87, 216–229 (2015).

  12. 12.

    Mathew, A. & Pradeep, T. Noble metal clusters: applications in energy, environment, and biology. Part. Part. Syst. Charact. 31, 1–37 (2014).

  13. 13.

    Zhang, X. D. et al. Ultrasmall glutathione-protected gold nanoclusters as next generation radiotherapy sensitizers with high tumor uptake and high renal clearance. Sci. Rep. 5, 8669 (2015).

  14. 14.

    Abbas, M. A., Kamat, P. V. & Bang, J. H. Thiolated gold nanoclusters for light energy conversion. ACS Energy Lett. 3, 840–854 (2018).

  15. 15.

    Abbas, M. A., Kim, T. Y., Lee, S. U., Kang, Y. S. & Bang, J. H. Exploring interfacial events in gold-nanocluster-sensitized solar cells: insights into the effects of the cluster size and electrolyte on solar cell performance. J. Am. Chem. Soc. 138, 390–401 (2016).

  16. 16.

    Wang, J. et al. In vivo self-bio-imaging of tumors through in situ biosynthesized fluorescent gold nanoclusters. Sci. Rep. 3, 1–6 (2013).

  17. 17.

    Durgadas, C. V., Sharma, C. P. & Sreenivasan, K. Fluorescent gold clusters as nanosensors for copper ions in live cells. Analyst 136, 933–940 (2011).

  18. 18.

    Xie, J. et al. Identification of a highly luminescent Au22(SG)18 nanocluster. J. Am. Chem. Soc. 136, 1246–1249 (2014).

  19. 19.

    Zhang, C. et al. Mimicking pathogenic invasion with the complexes of Au22(SG)18-engineered assemblies and folic acid. ACS Nano 12, 4408–4418 (2018).

  20. 20.

    Huang, B., Babcock, H. & Zhuang, X. Breaking the diffraction barrier: super-resolution imaging of cells. Cell 143, 1047–1058 (2010).

  21. 21.

    Medintz, I. L., Uyeda, H. T., Goldman, E. R. & Mattoussi, H. Quantum dot bioconjugates for imaging, labelling and sensing. Nat. Mater. 4, 435–446 (2005).

  22. 22.

    Chithrani, B. D. & Chan, W. C. W. Elucidating the mechanism of cellular uptake and removal of protein-coated gold nanoparticles of different sizes and shapes. Nano. Lett. 7, 1542–1550 (2007).

  23. 23.

    Kong, L. et al. Biocompatible glutathione-capped gold nanoclusters for dual fluorescent sensing and imaging of copper(ii) and temperature in human cells and bacterial cells. Microchim. Acta. 183, 2185–2195 (2016).

  24. 24.

    Lin, J., Zhang, H., Chen, Z. & Zheng, Y. Penetration of lipid membranes by gold nanoparticles: insights into cellular uptake, cytotoxicity, and their relationship. ACS Nano 4, 5421–5429 (2010).

  25. 25.

    Kornienko, N. et al. Spectroscopic elucidation of energy transfer in hybrid inorganic–biological organisms for solar-to-chemical production. Proc. Natl Acad. Sci. USA 113, 11750–11755 (2016).

  26. 26.

    Deutzmann, J. S., Sahin, M. & Spormann, A. M. Extracellular enzymes facilitate electron uptake in biocorrosion and bioelectrosynthesis. mBio 6, 1–8 (2015).

  27. 27.

    Pyo, K. et al. Ultrabright luminescence from gold nanoclusters: rigidifying the Au(i)-thiolate shell. J. Am. Chem. Soc. 137, 8244–8250 (2015).

  28. 28.

    Das, A. & Ljungdahl, L. G. in Biochemistry and Physiology of Anaerobic Bacteria (eds. Ljungdahl, L. G. et al.) 191–204 (Springer, New York, 2003).

  29. 29.

    Jiang, Y. et al. Light-induced N2O production from a non-heme iron-nitrosyl dimer. J. Am. Chem. Soc. 136, 12524–12527 (2014).

  30. 30.

    Santiago-Gonzalez, B. et al. Permanent excimer superstructures by supramolecular networking of metal quantum clusters. Science 353, 571–575 (2016).

  31. 31.

    Xiong, B., Xu, R., Zhou, R., He, Y. & Yeung, E. S. Preventing UV induced cell damage by scavenging reactive oxygen species with enzyme-mimic Au–Pt nanocomposites. Talanta 120, 262–267 (2014).

  32. 32.

    Gao, Y., Shao, N., Pei, Y., Chen, Z. & Zeng, X. C. Catalytic activities of subnanometer gold clusters (Au16–Au18, Au20, and Au27–Au35) for CO oxidation. ACS Nano 5, 7818–7829 (2011).

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Acknowledgements

This work was supported by Director, Office of Science, Office of Basic Energy Sciences, Chemical Sciences, Geosciences, and Biosciences Division, of the US Department of Energy under contract no. DE-AC02-05CH11231, FWP no. CH030201 (Catalysis Research Program). We thank the imaging facilities at the National Center for Electron Microscopy (NCEM) at the Molecular Foundry and the NMR facility of the College of Chemistry, University of California, Berkeley. Work at the NCEM was supported by the Office of Science, Office of Basic Energy Sciences, of the US Department of Energy under contract no. DE-AC02-05CH11231. Research reported in this publication was supported in part by the National Institutes of Health S10 programme under award no. 1S10OD018136-01. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. H.Z. thanks the Suzhou Industry Park (SIP) fellowship.

Author information

Author notes

  1. These authors contributed equally: Hao Zhang, Hao Liu.

Affiliations

  1. Department of Chemistry, University of California, Berkeley, Berkeley, CA, USA

    • Hao Zhang
    • , Hao Liu
    • , Zhiquan Tian
    • , Dylan Lu
    • , Yi Yu
    • , Kelsey K. Sakimoto
    •  & Peidong Yang
  2. Key Laboratory of Analytical Chemistry for Biology and Medicine (Ministry of Education), College of Chemistry and Molecular Sciences, Wuhan University, Wuhan, P. R. China

    • Zhiquan Tian
  3. Chemistry Sciences Division, Lawrence Berkeley National Laboratory, Berkeley, CA, USA

    • Dylan Lu
    •  & Peidong Yang
  4. School of Physical Science and Technology, ShanghaiTech University, Shanghai, China

    • Yi Yu
  5. Department of Materials Science and Engineering, University of California, Berkeley, Berkeley, CA, USA

    • Stefano Cestellos-Blanco
    •  & Peidong Yang
  6. Kavli Energy NanoSciences Institute, Berkeley, CA, USA

    • Peidong Yang

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Contributions

H.Z., H.L. and P.Y. designed the studies and prepared the manuscript. H.L. synthesized the AuNCs. H.Z. and Z.T. cultured the bacteria and carried out all the photosynthesis experiments. H.L. and S.C.-B. repeated the photosynthesis experiments and confirmed the reproducibility. H.Z. performed the UV–vis absorption, SIM imaging and bacteria enumeration characterization. D.L. and H.Z. conducted photoluminescence emission spectrum measurements. Y.Y. conducted the HAADF-STEM characterization. S.C.-B. helped with the fluorescence reader for the ROS test. K.K.S. provided discussion. All authors discussed the results and commented on the manuscript.

Competing interests

The authors declare no competing interests.

Corresponding author

Correspondence to Peidong Yang.

Supplementary Information

  1. Supplementary Information

    Supplementary Discussion, Supplementary Methods, Supplementary Figures 1–10, Supplementary Tables 1–4 and Supplementary References

  2. Reporting Summary

  3. Supplementary Video 1

    Video for intracellular AuNCs

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DOI

https://doi.org/10.1038/s41565-018-0267-z

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