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.

  • Article
  • Published:

Assembly of photo-bioelectrochemical cells using photosystem I-functionalized electrodes

A Corrigendum to this article was published on 28 January 2016

Abstract

The design of photo-bioelectrochemical cells based on native photosynthetic reaction centres is attracting substantial recent interest as a means for the conversion of solar light energy into electrical power. In the natural photosynthetic apparatus, the photosynthetic reaction centres are coupled to biocatalytic transformations leading to CO2 fixation and O2 evolution. Although significant progress in the integration of native photosystems with electrodes for light-to-electrical energy conversion has been achieved, the conjugation of the photosystems to enzymes to yield photo-bioelectrocatalytic solar cells remains a challenge. Here we demonstrate the assembly of integrated photosystem I/glucose oxidase or glucose dehydrogenase photo-bioelectrochemical electrodes. We highlight the photonic wiring of the biocatalysts by means of photosystem I using glucose as fuel. Our results provide a general approach to assemble photo-bioelectrochemical solar cells with wide implications for solar energy conversion, bioelectrocatalysis and sensing.

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

Figure 1: Assembly of an electrically contacted PSI/enzyme photoelectrochemical electrode.
Figure 2: Electrochemical and optical characterization of the stepwise assembly of the PSI/GOx photoelectrochemical electrode.
Figure 3: Energy level diagram corresponding to the redox components of the PSI/GOx photoelectrochemical electrode.
Figure 4: Photocurrent features generated by the PQQ/PSI/Os2+∕3+-polymer/GOx photo-bioelectrochemical electrode.
Figure 5: An electrically wired photo-bioelectrochemical electrode consisting of a Pt-nanocluster/PSI/Os2+∕3+-polymer/GOx assembly and the resulting anodic photocurrents generated by the electrode.

Similar content being viewed by others

References

  1. Hambourger, M. et al. Solar energy conversion in a photoelectrochemical biofuel cell. Dalton Trans. 45, 9979–9989 (2009).

    Article  Google Scholar 

  2. Meunier, C. F., Yang, X. Y., Rooke, J. C. & Su, B. L. Biofuel cells based on the immobilization of photosynthetically active bioentities. ChemCatChem 3, 476–488 (2011).

    Article  Google Scholar 

  3. Andreiadis, E. S., Chavarot-Kerlidou, M., Fontecave, M. & Artero, V. Artificial photosynthesis: from molecular catalysts for light-driven water splitting to photoelectrochemical cells. Photochem. Photobiol. 87, 946–964 (2011).

    Article  Google Scholar 

  4. Tel-Vered, R. & Willner, I. Photo-bioelectrochemical cells for energy conversion, sensing, and optoelectronic applications. ChemElectroChem 1, 1778–1797 (2014).

    Article  Google Scholar 

  5. Nguyen, K. & Bruce, B. D. Growing green electricity: progress and strategies for use of photosystem I for sustainable photovoltaic energy conversion. Biochim. Biophys. Acta 1837, 1553–1566 (2014).

    Article  Google Scholar 

  6. Wang, F., Liu, X. & Willner, I. Integration of photoswitchable proteins, photosynthetic reaction centers and semiconductor/biomolecule hybrids with electrode supports for optobioelectronic applications. Adv. Mater. 25, 349–377 (2013).

    Article  Google Scholar 

  7. Efrati, A. et al. Electrochemical switching of photoelectrochemical processes at CdS QDs and photosystem I-modified electrodes. ACS Nano 6, 9258–9266 (2012).

    Article  Google Scholar 

  8. Terasaki, N. et al. Plugging a molecular wire into photosystem I: reconstitution of the photoelectric conversion system on a gold electrode. Angew. Chem. Int. Ed. 48, 1585–1587 (2009).

    Article  Google Scholar 

  9. Kothe, T. et al. Engineered electron-transfer chain in photosystem 1 based photocathodes outperforms electron-transfer rates in natural photosynthesis. Chem. Eur. J. 20, 11029–11034 (2014).

    Article  Google Scholar 

  10. Yamanoi, Y., Terasaki, N., Miyachi, M., Inoue, Y. & Nishihara, H. Enhanced photocurrent production by photosystem I with modified viologen derivatives. Thin Solid Films 520, 5123–5127 (2012).

    Article  Google Scholar 

  11. Badura, A. et al. Photocurrent generation by photosystem 1 integrated in crosslinked redox hydrogels. Energy Environ. Sci. 4, 2435–2440 (2011).

    Article  Google Scholar 

  12. Maly, J. et al. Direct mediatorless electron transport between the monolayer of photosystem II and poly (mercapto-p-benzoquinone) modified gold electrode—new design of biosensor for herbicide detection. Biosens. Bioelectron. 21, 923–932 (2005).

    Article  Google Scholar 

  13. Kothe, T. et al. Combination of a photosystem 1-based photocathode and a photosystem 2-based photoanode to a Z-scheme mimic for biophotovoltaic applications. Angew. Chem. Int. Ed. 52, 14233–14236 (2013).

    Article  Google Scholar 

  14. Zhao, F., Sliozberg, K., Rögner, M., Plumeré, N. & Schuhmann, W. The role of hydrophobicity of Os-complex-modified polymers for photosystem 1 based photocathodes. J. Electrochem. Soc. 161, H3035–H3041 (2014).

    Article  Google Scholar 

  15. Badura, A. et al. Photo-induced electron transfer between photosystem 2 via cross-linked redox hydrogels. Electroanalysis 20, 1043–1047 (2008).

    Article  Google Scholar 

  16. Greenbaum, E. Platinized chloroplasts: a novel photocatalytic material. Science 230, 1373–1375 (1985).

    Article  Google Scholar 

  17. Gorka, M., Schartner, J., van der Est, A., Rögner, M. & Golbeck, J. H. Light-mediated hydrogen generation in photosystem I: attachment of a naphthoquinone–molecular wire–Pt nanoparticle to the A1A and A1B sites. Biochemistry 53, 2295–2306 (2014).

    Article  Google Scholar 

  18. Yehezkeli, O. et al. Generation of photocurrents by bis-aniline-cross-linked Pt nanoparticle/photosystem I composites on electrodes. J. Phys. Chem. B 114, 14383–14388 (2010).

    Article  Google Scholar 

  19. Feifel, S. C., Stieger, K. R., Lokstein, H., Lux, H. & Lisdat, F. High photocurrent generation by photosystem I on artificial interfaces composed of π-system-modified graphene. J. Mater. Chem. A 3, 12188–12196 (2015).

    Article  Google Scholar 

  20. Gordiichuk, P. I. et al. Solid-state biophotovoltaic cells containing photosystem I. Adv. Mater. 26, 4863–4869 (2014).

    Article  Google Scholar 

  21. Stieger, K. R., Feifel, S. C., Lokstein, H. & Lisdat, F. Advanced unidirectional photocurrent generation via cytochrome c as reaction partner for directed assembly of photosystem I. Phys. Chem. Chem. Phys. 16, 15667–15674 (2014).

    Article  Google Scholar 

  22. Yehezkeli, O. et al. Integrated photosystem II-based photo-bioelectrochemical cells. Nature Commun. 3, 742 (2012).

    Article  Google Scholar 

  23. Efrati, A., Tel-Vered, R., Michaeli, D., Nechushtai, R. & Willner, I. Cytochrome c-coupled photosystem I and photosystem II (PSI/PSII) photo-bioelectrochemical cells. Energy Environ. Sci. 6, 2950–2956 (2013).

    Article  Google Scholar 

  24. Zayats, M., Willner, B. & Willner, I. Design of amperometric biosensors and biofuel cells by the reconstitution of electrically contacted enzyme electrodes. Electroanalysis 20, 583–601 (2008).

    Article  Google Scholar 

  25. Heller, A. Electrical wiring of redox enzymes. Acc. Chem. Res. 23, 128–134 (1990).

    Article  Google Scholar 

  26. Willner, I. Biomaterials for sensors, fuel cells, and circuitry. Science 298, 2407–2408 (2002).

    Article  Google Scholar 

  27. Yehezkeli, O., Tel-Vered, R., Raichlin, S. & Willner, I. Nano-engineered flavin-dependent glucose dehydrogenase/gold nanoparticle-modified electrodes for glucose sensing and biofuel cell applications. ACS Nano 5, 2385–2391 (2011).

    Article  Google Scholar 

  28. Willner, I. & Katz, E. Integration of layered redox proteins and conductive supports for bioelectronic applications. Angew. Chem. Int. Ed. 39, 1180–1218 (2000).

    Article  Google Scholar 

  29. Heller, A. Miniature biofuel cells. Phys. Chem. Chem. Phys. 6, 209–216 (2004).

    Article  Google Scholar 

  30. Zebda, A. et al. Mediatorless high-power glucose biofuel cells based on compressed carbon nanotube-enzyme electrodes. Nature Commun. 2, 370 (2011).

    Article  Google Scholar 

  31. Schuhmann, W., Ohara, T. J., Schmidt, H. L. & Heller, A. Electron transfer between glucose oxidase and electrodes via redox mediators bound with flexible chains to the enzyme surface. J. Am. Chem. Soc. 113, 1394–1397 (1991).

    Article  Google Scholar 

  32. Degani, Y. & Heller, A. Direct electrical communication between chemically modified enzymes and metal electrodes. 2. Methods for bonding electron-transfer relays to glucose oxidase and D-amino-acid oxidase. J. Am. Chem. Soc. 110, 2615–2620 (1988).

    Article  Google Scholar 

  33. Willner, I., Riklin, A., Shoham, B., Rivenzon, D. & Katz, E. Development of novel biosensor enzyme electrodes: glucose oxidase multilayer arrays immobilized onto self-assembled monolayers on electrodes. Adv. Mater. 5, 912–915 (1993).

    Article  Google Scholar 

  34. Gregg, B. A. & Heller, A. Redox polymer films containing enzymes. 1. A redox-conducting epoxy cement: synthesis, characterization, and electrocatalytic oxidation of hydroquinone. J. Phys. Chem. 95, 5970–5975 (1991).

    Article  Google Scholar 

  35. Rajagopalan, R., Aoki, A. & Heller, A. Effect of quaternization of the glucose oxidase “wiring” redox polymer on the maximum current densities of glucose electrodes. J. Phys. Chem. 100, 3719–3727 (1996).

    Article  Google Scholar 

  36. Xiao, Y., Patolsky, F., Katz, E., Hainfeld, J. F. & Willner, I. “Plugging into enzymes”: nanowiring of redox enzymes by a gold nanoparticle. Science 299, 1877–1881 (2003).

    Article  Google Scholar 

  37. Katz, E., Sheeney-Haj-Ichia, L. & Willner, I. Electrical contacting of glucose oxidase in a redox-active rotaxane configuration. Angew. Chem. Int. Ed. 43, 3292–3300 (2004).

    Article  Google Scholar 

  38. Patolsky, F., Weizmann, Y. & Willner, I. Long-range electrical contacting of redox enzymes by SWCNT connectors. Angew. Chem. Int. Ed. 43, 2113–2117 (2004).

    Article  Google Scholar 

  39. Nechushtai, R., Muster, P., Binder, A., Liveanu, V. & Nelson, N. Photosystem I reaction center from the thermophilic cyanobacterium Mastigocladus laminosus. Proc. Natl Acad. Sci. USA 80, 1179–1183 (1983).

    Article  Google Scholar 

Download references

Acknowledgements

This research is supported by the German–Israeli programme (DIP) and by the Minerva Center for Biohybrid Complex Systems.

Author information

Authors and Affiliations

Authors

Contributions

A.E. planned and performed the experiments. D.M. and R.N. purified and provided the PSI. S.A. and W.S. synthesized and provided the Os2+∕3+-polyvinylimidazole complex. I.W. planned and supervised the experiments. All authors discussed the results and participated in the formulation of the manuscript.

Corresponding author

Correspondence to Itamar Willner.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Efrati, A., Lu, CH., Michaeli, D. et al. Assembly of photo-bioelectrochemical cells using photosystem I-functionalized electrodes. Nat Energy 1, 15021 (2016). https://doi.org/10.1038/nenergy.2015.21

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1038/nenergy.2015.21

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing