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.

  • Letter
  • Published:

Bacteria photosensitized by intracellular gold nanoclusters for solar fuel production

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.

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

Access options

Buy this article

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

Fig. 1: Schematic diagram of the M. thermoacetica/AuNC hybrid system.
Fig. 2: Microscopy images of the M. thermoacetica/AuNC hybrid system.
Fig. 3: Photosynthesis behaviour of different systems.
Fig. 4: Viability measurements.

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

    Article  CAS  Google Scholar 

  2. 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 

  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).

    Article  CAS  Google Scholar 

  4. 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 

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

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  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).

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  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).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Google Scholar 

  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).

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  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).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

Download references

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

Authors and Affiliations

Authors

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.

Corresponding author

Correspondence to Peidong Yang.

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

Reporting Summary

Supplementary Video 1

Video for intracellular AuNCs

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, H., Liu, H., Tian, Z. et al. Bacteria photosensitized by intracellular gold nanoclusters for solar fuel production. Nature Nanotech 13, 900–905 (2018). https://doi.org/10.1038/s41565-018-0267-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

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

This article is cited by

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