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.

Self-organized photosynthetic nanoparticle for cell-free hydrogen production

Nature Nanotechnology volume 5, pages 73–79 (2010)Cite this article

Abstract

There is considerable interest in making use of solar energy through photosynthesis to create alternative forms of fuel. Here, we show that photosystem I from a thermophilic bacterium and cytochrome-c6 can, in combination with a platinum catalyst, generate a stable supply of hydrogen in vitro upon illumination. The self-organized platinization of the photosystem I nanoparticles allows electron transport from sodium ascorbate to photosystem I via cytochrome-c6 and finally to the platinum catalyst, where hydrogen gas is formed. Our system produces hydrogen at temperatures up to 55 °C and is temporally stable for >85 days with no decrease in hydrogen yield when tested intermittently. The maximum yield is ∼ 5.5 µmol H2 h−1 mg−1 chlorophyll and is estimated to be ∼25-fold greater than current biomass-to-fuel strategies. Future work will further improve this yield by increasing the kinetics of electron transfer, extending the spectral response and replacing the platinum catalyst with a renewable hydrogenase.

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

Relevant articles

Open Access articles citing this article.

Access options

Rent or buy this article

Get just this article for as long as you need it

$39.95

Learn more

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

Figure 1: Schematic of the electron flow in the photosystem I catalytic nanoparticle.
Figure 2: Isolation of photosystem I.
Figure 3: Thermal stability of photosystem I monitored by circular dichroism.
Figure 4: Determining the role of each component in PSI-mediated hydrogen evolution.
Figure 5: Thermal and temporal stability of hydrogen evolution.
Figure 6: Peak rates of hydrogen evolution.

References

  1. Tsoskounogiou, M., Ayerides, G. & Tritopoulou, E. The end of cheap oil: current status and prospects. Energy Policy 36, 3797–3806 (2008).

    Article  Google Scholar 

  2. Moore, A. Short-circuiting our fossil fuel habits. Could a more direct harnessing of photosynthesis become an alternative to natural oil, coal and gas? EMBO Rep 6, 205–208 (2005).

    Article  CAS  Google Scholar 

  3. Pimentel, D. & Patzek, T. Ethanol production using corn, switchgrass and wood; biodiesel production using soybean and sunflower. Natural Resources Res. 14, 65–76 (2005).

    Article  CAS  Google Scholar 

  4. Ghirardi, M. L. et al. Microalgae: a green source of renewable H2 . Trends Biotechnol. 8, 506–511 (2000).

    Article  Google Scholar 

  5. Ghirardi, M. L. et al. Hydrogenases and hydrogen photoproduction in oxygenic photosynthetic organisms. Ann. Rev. Plant Biol. 58, 71–91 (2007).

    Article  CAS  Google Scholar 

  6. Deisenhofer, J. & Michel, H. High-resolution structures of photosynthetic reaction centers. Ann. Rev. Biophys. Biophys. Chem. 20, 247–266 (1991).

    Article  CAS  Google Scholar 

  7. Golbeck, J. H. Shared thematic elements in photochemical reaction centers. Proc. Natl Acad. Sci. USA 90, 1642–1646 (1993).

    Article  CAS  Google Scholar 

  8. Iwata, S. & Barber, J. Structure of photosystem II and molecular architecture of the oxygen-evolving centre. Curr. Opin. Struct. Biol. 14, 447–453 (2004).

    Article  CAS  Google Scholar 

  9. Kalman, L., Williams, J. C. & Allen, J. P. Comparison of bacterial reaction centers and photosystem II. Photosynth. Res. 98, 643–655 (2008).

    Article  CAS  Google Scholar 

  10. Grotjohann, I. & Fromme, P. Structure of cyanobacterial photosystem I. Photosynth. Res. 85, 51–72 (2005).

    Article  CAS  Google Scholar 

  11. Nelson, N. & Ben-Shem, A. The structure of photosystem I and evolution of photosynthesis. Bioessays 27, 914–922 (2005).

    Article  CAS  Google Scholar 

  12. Jensen, P. E. et al. Structure, function and regulation of plant photosystem I. Biochim Biophys. Acta 1767, 335–352 (2007).

    Article  CAS  Google Scholar 

  13. Barber, J. Photosystem II: the engine of life. Q. Rev. Biophys. 36, 71–89 (2003).

    Article  CAS  Google Scholar 

  14. Evans, B. R. et al. Enhanced photocatalytic hydrogen evolution by covalent attachment of plastocyanin to photosystem I. Nano Lett. 4, 1815–1819 (2004).

    Article  CAS  Google Scholar 

  15. Millsaps, J. F., Bruce, B. D., Lee, J. W. & Greenbaum, E. Nanoscale photosynthesis: photocatalytic production of hydrogen by platinized photosystem I reaction centers. Photochem. Photobiol. 73, 630–635 (2001).

    Article  CAS  Google Scholar 

  16. Ihara, M. et al. Photoinduced hydrogen production by direct electron transfer from photosystem I cross-linked with cytochrome c(3) to [NiFe]-hydrogenase. Photochem. Photobiol. 82, 1677–1685 (2006).

    Article  CAS  Google Scholar 

  17. Ihara, M. et al. Light-driven hydrogen production by a hybrid complex of a [NiFe]-hydrogenase and the cyanobacterial photosystem I. Photochem. Photobiol. 82, 676–682 (2006).

    Article  CAS  Google Scholar 

  18. Das, R. et al. Integration of photosynthetic protein molecular complexes in solid-state electronic devices. Nano Lett. 4, 1079–1083 (2004).

    Article  CAS  Google Scholar 

  19. Jordan, P. et al. Three-dimensional structure of cyanobacterial photosystem I at 2.5 Å resolution. Nature 411, 909–917 (2001).

    Article  CAS  Google Scholar 

  20. Evans, P. K. & Krogmann, D. W. 3 c-type cytochromes from the red alga Porphyridium cruentum. Archives Biochem. Biophys. 227, 494–510 (1983).

    Article  CAS  Google Scholar 

  21. Ho, K. K., Ulrich, E. L., Krogmann, D. W. & Gomezlojero, C. Isolation of photosynthetic catalysts from cyanobacteria. Biochim. Biophys. Acta 545, 236–248 (1979).

    Article  CAS  Google Scholar 

  22. Nakamura, Y. et al. Complete genome structure of the thermophilic cyanobacterium T. elongatus BP-1. DNA Res. 9, 123–130 (2002).

    Article  CAS  Google Scholar 

  23. Cho, Y. S., Wang, Q. J., Krogmann, D. & Whitmarsh, J. Extinction coefficients and midpoint potentials of cytochrome c(6) from the cyanobacteria Arthrospira maxima, Microcystis aeruginosa and Synechocystis 6803. Biochim. Biophys. Acta-Bioenergetics 1413, 92–97 (1999).

    Article  CAS  Google Scholar 

  24. Anta, J. A., Casanueva, F. & Oskam, G. A numerical model for charge transport and recombination in dye-sensitized solar cells. J. Phys. Chem. B 110, 5372–5378 (2006).

    Article  CAS  Google Scholar 

  25. Duran, R. V., Hervas, M., De la Rosa, M. A. & Navarro, J. A. In vivo photosystem I reduction in thermophilic and mesophilic cyanobacteria: the thermal resistance of the process is limited by factors other than the unfolding of the partners. Biochem. Biophys. Res. Commun. 334, 170–175 (2005).

    Article  CAS  Google Scholar 

  26. Du, H. B., Fairbridge, C., Yang, H. & Ring, Z. The chemistry of selective ring-opening catalysts. Appl. Catalysis A—General 294, 1–21 (2005).

    Article  CAS  Google Scholar 

  27. Hegedus, L. & Mathe, T. Hydrogenation of pyrrole derivatives—Part V. Poisoning effect of nitrogen on precious metal on carbon catalysts. Appl. Catalysis A—General 226, 319–322 (2002).

    Article  CAS  Google Scholar 

  28. Irandoust, S. & Edvardsson, J. Poisoning of nickel-based catalysts in fat hydrogenation. J. Am. Oil Chemists Soc. 70, 1149–1156 (1993).

    Article  CAS  Google Scholar 

  29. Grimme, R. A., Lubner, C. E., Bryant, D. A. & Golbeck, J. H. Photosystem I/molecular wire/metal nanoparticle bioconjugates for the photocatalytic production of H2. J. Am. Chem. Soc. 130, 6308–6309 (2008).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by a National Science Foundation (NSF) Nanoscience Interdisciplinary Research Team (NIRT) award to B.D.B. (DBI-0403781) and an NSF Sustainable Science Grant (CBET 0828615) award to P.D.F. and B.D.B. A SARIF Award and Science Alliance Award provided additional support to P.D.F. and B.D.B. The authors would like to acknowledge the technical help of J. Dunlap, A. Godman, C. Pacquet, P. Mahbubani and S. Wright, and also thank G. Alexandre, B. Evans, E. Greenbaum, D. Harrell, L. Johnson and B. Mullin for their input.

Author information

Author notes

  1. Ifeyinwa J. Iwuchukwu and Michael Vaughn: These authors contributed equally to this work

Authors and Affiliations

  1. Department of Chemical and Biomolecular Engineering, University of Tennessee, Knoxville, 37996, Tennessee, USA

    Ifeyinwa J. Iwuchukwu, Paul Frymier & Barry D. Bruce

  2. Department of Biochemistry, Cellular and Molecular Biology, University of Tennessee, Knoxville, 37996, Tennessee, USA

    Michael Vaughn, Hugh O'Neill & Barry D. Bruce

  3. Department of Microbiology, University of Tennessee, Knoxville, 37996, Tennessee, USA

    Natalie Myers & Barry D. Bruce

  4. Chemical Sciences Division, Oak Ridge National Laboratory, Oak Ridge, 37831, Tennessee, USA

    Hugh O'Neill

  5. Sustainable Energy and Education Research Center (SEERC), University of Tennessee, Knoxville, 37996, Tennessee, USA

    Paul Frymier & Barry D. Bruce

Authors
  1. Ifeyinwa J. Iwuchukwu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Michael Vaughn
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Natalie Myers
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hugh O'Neill
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Paul Frymier
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Barry D. Bruce
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

I.J.I. performed all the hydrogen evolution experiments, provided data analysis and assisted in manuscript preparation. M.V. grew and maintained T. elongatus, isolated and characterized PSI, assisted in cytochrome-c isolation, conducted thermostability measurements, composed all the figures, provided data analysis and manuscript preparation. N.M. cloned and developed the over-expression system for cytochrome-c and provided cytochrome-c for hydrogen evolution experiments. H.O.N. supervised hydrogen evolution experiments, helped coordinate the hydrogen experimentation, and participated in data analysis and manuscript preparation. P.F. coordinated hydrogen evolution experiments, supported I.J.I. and N.M., and participated in data analysis and manuscript preparation. B.D.B. provided overall coordination of the project, supervised the microbiology, molecular biology and biochemistry, provided support for M.V. and N.M., and participated in data analysis and manuscript preparation as corresponding author.

Corresponding author

Correspondence to Barry D. Bruce.

Supplementary information

Supplementary information

Supplementary information (PDF 1300 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Iwuchukwu, I., Vaughn, M., Myers, N. et al. Self-organized photosynthetic nanoparticle for cell-free hydrogen production. Nature Nanotech 5, 73–79 (2010). https://doi.org/10.1038/nnano.2009.315

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nnano.2009.315

This article is cited by

Search

Advanced search

Quick links

Find nanotechnology articles, nanomaterial data and patents all in one place. Visit Nano by Nature Research