Skip to main content

Thank you for visiting 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.

Bias-free photoelectrochemical water splitting with photosystem II on a dye-sensitized photoanode wired to hydrogenase


Natural photosynthesis stores sunlight in chemical energy carriers, but it has not evolved for the efficient synthesis of fuels, such as H2. Semi-artificial photosynthesis combines the strengths of natural photosynthesis with synthetic chemistry and materials science to develop model systems that overcome nature’s limitations, such as low-yielding metabolic pathways and non-complementary light absorption by photosystems I and II. Here, we report a bias-free semi-artificial tandem platform that wires photosystem II to hydrogenase for overall water splitting. This photoelectrochemical cell integrated the red and blue light-absorber photosystem II with a green light-absorbing diketopyrrolopyrrole dye-sensitized TiO2 photoanode, and so enabled complementary panchromatic solar light absorption. Effective electronic communication at the enzyme–material interface was engineered using an osmium-complex-modified redox polymer on a hierarchically structured TiO2. This system provides a design protocol for bias-free semi-artificial Z schemes in vitro and provides an extended toolbox of biotic and abiotic components to re-engineer photosynthetic pathways.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

Fig. 1: Semi-artificial tandem PEC system for unassisted overall water splitting.
Fig. 2: PF-PEC of tandem PSII–dye photoanode.
Fig. 3: Photocurrent action spectra of tandem PSII–dye photoanode.
Fig. 4: Overall water splitting in semi-artificial PEC cell.


  1. 1.

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

    Article  Google Scholar 

  2. 2.

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

    Article  Google Scholar 

  3. 3.

    Mersch, D. et al. Wiring of photosystem II to hydrogenase for photoelectrochemical water-splitting. J. Am. Chem. Soc. 137, 8541–8549 (2015).

    Article  Google Scholar 

  4. 4.

    Sokol, K. P. et al. Rational wiring of photosystem II to hierarchical indium tin oxide electrodes using redox polymers. Energy Environ. Sci. 9, 3698–3709 (2016).

    Article  Google Scholar 

  5. 5.

    Ort, D. R. et al. Redesigning photosynthesis to sustainably meet global food and bioenergy demand. Proc. Natl Acad. Sci. USA 112, 8529–8536 (2015).

    Article  Google Scholar 

  6. 6.

    Tachibana, Y., Vayssieres, L. & Durrant, J. R. Artificial photosynthesis for solar water-splitting. Nat. Photon. 6, 511–518 (2012).

    Article  Google Scholar 

  7. 7.

    Woolerton, T. W., Sheard, S., Chaudhary, Y. S. & Armstrong, F. A. Enzymes and bio-inspired electrocatalysts in solar fuel devices. Energy Environ. Sci. 5, 7470–7490 (2012).

    Article  Google Scholar 

  8. 8.

    Léger, C. & Bertrand, P. Direct electrochemistry of redox enzymes as a tool for mechanistic studies. Chem. Rev. 108, 2379–2438 (2008).

    Article  Google Scholar 

  9. 9.

    Kato, M., Zhang, J. Z., Paul, N. & Reisner, E. Protein film photoelectrochemistry of the water oxidation enzyme photosystem II. Chem. Soc. Rev. 43, 6485–6497 (2014).

    Article  Google Scholar 

  10. 10.

    Bard, A. J. & Fox, M. A. Artificial photosynthesis: solar splitting of water to hydrogen and oxygen. Acc. Chem. Res. 28, 141–145 (1995).

    Article  Google Scholar 

  11. 11.

    Govindjee, Shevela, D. & Björn, L. O. Evolution of the Z-scheme of photosynthesis: a perspective. Photosynth. Res. 133, 5–15 (2017).

    Article  Google Scholar 

  12. 12.

    Barber, J. & Tran, P. D. From natural to artificial photosynthesis. J. R. Soc. Interface 10, 20120984 (2013).

    Article  Google Scholar 

  13. 13.

    Khetkorn, W. et al. Microalgal hydrogen production—a review. Bioresource Technol. 243, 1194–1206 (2017).

    Article  Google Scholar 

  14. 14.

    Kruse, O., Rupprecht, J., Mussgnug, J. H., Dismukes, G. C. & Hankamer, B. Photosynthesis: a blueprint for solar energy capture and biohydrogen production technologies. Photochem. Photobiol. Sci. 4, 957–969 (2005).

    Article  Google Scholar 

  15. 15.

    Michel, H. The nonsense of biofuels. Angew. Chem. Int. Ed. 51, 2516–2518 (2012).

    Article  Google Scholar 

  16. 16.

    Esper, B., Badura, A. & Rögner, M. Photosynthesis as a power supply for (bio-)hydrogen production. Trends Plant Sci. 11, 543–549 (2006).

    Article  Google Scholar 

  17. 17.

    Hu, S., Xiang, C., Haussener, S., Berger, A. D. & Lewis, N. S. An analysis of the optimal band gaps of light absorbers in integrated tandem photoelectrochemical water-splitting systems. Energy Environ. Sci. 6, 2984–2993 (2013).

    Article  Google Scholar 

  18. 18.

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

    Article  Google Scholar 

  19. 19.

    Hartmann, V. et al. Redox hydrogels with adjusted redox potential for improved efficiency in Z-scheme inspired biophotovoltaic cells. Phys. Chem. Chem. Phys. 16, 11936–11941 (2014).

    Article  Google Scholar 

  20. 20.

    Kim, Y. et al. Hybrid Z-scheme using photosystem I and BiVO4 for hydrogen production. Adv. Funct. Mater. 25, 2369–2377 (2015).

    Article  Google Scholar 

  21. 21.

    Rao, K. K. et al. Photoelectrochemical responses of photosystem II particles immobilized on dye-derivatized TiO2 films. J. Photochem. Photobiol. B 5, 379–389 (1990).

    Article  Google Scholar 

  22. 22.

    Wang, W. et al. Spatially separated photosystem II and a silicon photoelectrochemical cell for overall water splitting: a natural–artificial photosynthetic hybrid. Angew. Chem. Int. Ed. 55, 9229–9233 (2016).

    Article  Google Scholar 

  23. 23.

    Pinhassi, R. I. et al. Hybrid bio-photo-electro-chemical cells for solar water splitting. Nat. Commun. 7, 12552 (2016).

    Article  Google Scholar 

  24. 24.

    O’Regan, B. & Grätzel, M. A low-cost, high-efficiency solar cell based on dye-sensitised colloidal TiO2 films. Nature 353, 737–740 (1991).

    Article  Google Scholar 

  25. 25.

    Xu, P., McCool, N. S. & Mallouk, T. E. Water splitting dye-sensitized solar cells. Nano Today 14, 42–58 (2017).

    Article  Google Scholar 

  26. 26.

    Warnan, J. et al. A compact diketopyrrolopyrrole dye as efficient sensitizer in titanium dioxide dye-sensitized solar cells. J. Photochem. Photobiol. A 226, 9–15 (2011).

    Article  Google Scholar 

  27. 27.

    Warnan, J. et al. Solar H2 evolution in water with modified diketopyrrolopyrrole dyes immobilised on molecular Co and Ni catalyst–TiO2 hybrids. Chem. Sci. 8, 3070–3079 (2017).

    Article  Google Scholar 

  28. 28.

    Muresan, N. M., Willkomm, J., Mersch, D., Vaynzof, Y. & Reisner, E. Immobilization of a molecular cobaloxime catalyst for hydrogen evolution on a mesoporous metal oxide electrode. Angew. Chem. Int. Ed. 51, 12749–12753 (2012).

    Article  Google Scholar 

  29. 29.

    Lakadamyali, F., Reynal, A., Kato, M., Durrant, J. R. & Reisner, E. Electron transfer in dye-sensitised semiconductors modified with molecular cobalt catalysts: photoreduction of aqueous protons. Chem. Eur. J. 18, 15464–15475 (2012).

    Article  Google Scholar 

  30. 30.

    Knauf, R. R., Brennaman, M. K., Alibabaei, L., Norris, M. R. & Dempsey, J. L. Revealing the relationship between semiconductor electronic structure and electron transfer dynamics at metal oxide−chromophore interfaces. J. Phys. Chem. C 117, 25259–25268 (2013).

    Article  Google Scholar 

  31. 31.

    Li, F. et al. Immobilizing Ru(bda) catalyst on a photoanode via electrochemical polymerization for light-driven water splitting. ACS Catal. 5, 3786–3790 (2015).

    Article  Google Scholar 

  32. 32.

    Willkomm, J. et al. Dye-sensitised semiconductors modified with molecular catalysts for light-driven H2 production. Chem. Soc. Rev. 45, 9–23 (2016).

    Article  Google Scholar 

  33. 33.

    Umena, Y., Kawakami, K., Shen, J.-R. & Kamiya, N. Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å. Nature 473, 55–60 (2011).

    Article  Google Scholar 

  34. 34.

    Rapatskiy, L. et al. Detection of the water-binding sites of the oxygen-evolving complex of photosystem II using W-band 17O electron−electron double resonance-detected NMR spectroscopy. J. Am. Chem. Soc. 134, 16619–16634 (2012).

    Article  Google Scholar 

  35. 35.

    Kuhl, H. et al. Towards structural determination of the water-splitting enzyme: purification, crystallization, and preliminary crystallographic studies of photosystem II from a thermophilic cyanobacterium. J. Biol. Chem. 275, 20652–20659 (2000).

    Article  Google Scholar 

  36. 36.

    Kern, J. et al. Purification, characterisation and crystallisation of photosystem II from Thermosynechococcus elongatus cultivated in a new type of photobioreactor. Biochim. Biophys. Acta Bioenerg. 1706, 147–157 (2005).

    Article  Google Scholar 

  37. 37.

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

    Article  Google Scholar 

  38. 38.

    Senge, M. O., Ryan, A. A., Letchford, K. A., MacGowan, S. A. & Mielke, T. Chlorophylls, symmetry, chirality, and photosynthesis. Symmetry 6, 781–843 (2014).

    Article  Google Scholar 

  39. 39.

    Beranek, R. (Photo)electrochemical methods for the determination of the band edge positions of TiO2-based nanomaterials. Adv. Phys. Chem. 2011, 80–83 (2011).

    Article  Google Scholar 

  40. 40.

    Zhang, J. Z. et al. Competing charge transfer pathways at the photosystem II–electrode interface. Nat. Chem. Biol. 12, 1046–1052 (2016).

    Article  Google Scholar 

  41. 41.

    Razeghifard, R. & Wydrzynski, T. J. Artificial Photosynthesis: From Basic Biology to Industrial Application (Wiley, Hoboken, 2007).

  42. 42.

    Reisner, E., Powell, D. J., Cavazza, C., Fontecilla-Camps, J. C. & Armstrong, F. A. Visible light-driven H2 production by hydrogenases attached to dye-sensitized TiO2 nanoparticles. J. Am. Chem. Soc. 131, 18457–18466 (2009).

    Article  Google Scholar 

  43. 43.

    Wombwell, C., Caputo, C. A. & Reisner, E. [NiFeSe]-hydrogenase chemistry. Acc. Chem. Res. 48, 2858–2865 (2015).

    Article  Google Scholar 

  44. 44.

    Hambourger, M. et al. [FeFe]-hydrogenase-catalyzed H2 production in a photoelectrochemical biofuel cell. J. Am. Chem. Soc. 130, 2015–2022 (2008).

    Article  Google Scholar 

  45. 45.

    Coridan, R. H. et al. Methods for comparing the performance of energy-conversion systems for use in solar fuels and solar electricity generation. Energy Environ. Sci. 8, 2886–2901 (2015).

    Article  Google Scholar 

  46. 46.

    Cai, P. et al. Co-assembly of photosystem II/reduced graphene oxide multilayered biohybrid films for enhanced photocurrent. Nanoscale 7, 10908–10911 (2015).

    Article  Google Scholar 

  47. 47.

    Dotan, H., Mathews, N., Hisatomi, T., Grätzel, M. & Rothschild, A. On the solar to hydrogen conversion efficiency of photoelectrodes for water splitting. J. Phys. Chem. Lett. 5, 3330–3334 (2014).

    Article  Google Scholar 

  48. 48.

    Hatchikian, E. C., Bruschi, M. & Le Gall, J. Characterisation of the periplasmic hydrogenase from Desulfovibrio gigas. Biochem. Biophys. Res. Commun. 82, 451–461 (1978).

    Article  Google Scholar 

  49. 49.

    Porra, R. J., Thompson, W. A. & Kriedemann, P. E. Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim. Biophys. Acta Bioenerg. 975, 384–394 (1989).

    Article  Google Scholar 

Download references


This work was supported by an ERC Consolidator Grant MatEnSAP (682833), the UK Engineering and Physical Sciences Research Council (EP/L015978/1 and EP/G037221/1, nanoDTC and a DTA studentship), the Christian Doppler Research Association, the OMV Group and a Royal Society Newton International Fellowship (NF160054), the Cluster of Excellence RESOLV (EXC 1069) funded by the Deutsche Forschungsgemeinschaft and the European Union’s Horizon 2020 MSCA ITN-EJD 764920 PHOTOBIOCAT. The HAADF–STEM was carried out at the National Center of Electron Microscopy (NCEM), which is supported by the Office of Science, Office of Basic Energy Sciences of the US Department of Energy under Contract no. DE-AC02-05CH11231. Work at the Molecular Foundry was supported by the Office of Science, Office of Basic Energy Sciences of the US Department of Energy under Contract no. DE-AC02-05CH11231. We thank J. Fontecilla-Camps and C. Cavazza for providing the H2ase enzyme, V. Hartmann for his contribution to the PSII preparation and N. Plumeré, C. Creissen, S. Kalathil and N. Heidary for valuable discussions.

Author information




K.P.S., W.E.R., J.Z.Z. and E.R. conceived the research. K.P.S. prepared and characterized the electrodes and performed the electrochemical experiments. W.E.R. helped with the experiment design and supported the electrochemical experiments. J.W. synthesized the dpp dye. N.K. carried out the HAADF–STEM and RRDE measurements. M.M.N. provided the PSII samples. A.R. synthesized the POs polymer. K.P.S., W.E.R., N.K., J.Z.Z. and E.R. analysed the data. All the authors contributed to the creation of the manuscript. E.R. supervised the work.

Corresponding author

Correspondence to Erwin Reisner.

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 Table 1, Supplementary Figures 1–19

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Sokol, K.P., Robinson, W.E., Warnan, J. et al. Bias-free photoelectrochemical water splitting with photosystem II on a dye-sensitized photoanode wired to hydrogenase. Nat Energy 3, 944–951 (2018).

Download citation

Further reading


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