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.

  • Hypothesis
  • Published:

A mechanism for water splitting and oxygen production in photosynthesis

Abstract

Sunlight is absorbed and converted to chemical energy by photosynthetic organisms. At the heart of this process is the most fundamental reaction on Earth, the light-driven splitting of water into its elemental constituents. In this way molecular oxygen is released, maintaining an aerobic atmosphere and creating the ozone layer. The hydrogen that is released is used to convert carbon dioxide into the organic molecules that constitute life and were the origin of fossil fuels. Oxidation of these organic molecules, either by respiration or combustion, leads to the recombination of the stored hydrogen with oxygen, releasing energy and reforming water. This water splitting is achieved by the enzyme photosystem II (PSII). Its appearance at least 3 billion years ago, and linkage through an electron transfer chain to photosystem I, directly led to the emergence of eukaryotic and multicellular organisms. Before this, biological organisms had been dependent on hydrogen/electron donors, such as H2S, NH3, organic acids and Fe2+, that were in limited supply compared with the oceans of liquid water. However, it is likely that water was also used as a hydrogen source before the emergence of PSII, as found today in anaerobic prokaryotic organisms that use carbon monoxide as an energy source to split water. The enzyme that catalyses this reaction is carbon monoxide dehydrogenase (CODH). Similarities between PSII and the iron- and nickel-containing form of this enzyme (Fe-Ni CODH) suggest a possible mechanism for the photosynthetic O–O bond formation.

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

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

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

Figure 1: The S-state cycle showing how the absorption of four photons of light (hv) by P680 drives the splitting of two water molecules and formation of O2 through a consecutive series of five intermediates (S0, S1, S2, S3 and S4).
Figure 2: Comparison of the Mn4Ca2+O5 cluster of PSII with Fe4Ni2+S5 cluster of CODH.
Figure 3: A structurally based diagrammatic comparison of a base nucleophilic attack of a hydroxyl on to an electrophile leading to oxygen atom transfer.
Figure 4: Diagrammatic representation of a mechanistic scheme for water splitting and dioxygen formation in PSII based on the arguments and discussion presented in this communication.

Similar content being viewed by others

References

  1. Fontana, F. Accounts of air extracted from different kinds of water. Phil. Trans. R. Soc. 69, 432–453 (1780).

    Google Scholar 

  2. Byron Smith, R. J., Loganathan, M. & Shantha, M. S. A review of the water gas shift reaction kinetics. Inter. J. Chem. React. Eng. https://doi.org/10.2202/1542-6580.2238 (2010).

  3. Svetlitchnyi, V. et al. A functional Ni-Ni-[4Fe-4S] cluster in the monomeric acetyl-CoA synthase from Carboxydothermus hydrogenoformans. Proc. Natl Acad. Sci. USA 101, 446–451 (2004).

    Google Scholar 

  4. Gong, W. et al. Structure of the α2ε2 Ni-dependent CO dehydrogenase component of the Methanosarcina barkeri acetyl-CoA decarbonylase/synthase complex. Proc. Natl Acad. Sci. USA 105, 9558–9563 (2008).

    Google Scholar 

  5. Kok, B., Forbush, B. & McGloin, M. Cooperation of charges in photosynthetic O2 evolution–I. A linear four-step mechanism. Photochem. Photobiol. 11, 467–475 (1970).

    Google Scholar 

  6. Cox, N. et al. Electronic structure of the oxygen-evolving complex in photosystem II prior to O–O bond formation. Science 345, 804–808 (2014).

    Google Scholar 

  7. Barber, J. Photosystem II: the water splitting enzyme of photosynthesis and the origin of oxygen in our atmosphere. Quart. Rev. Biophys. 49, 1–21 (2016).

    Google Scholar 

  8. Renger, G. Photosynthetic water oxidation to molecular oxygen: apparatus and mechanism. Biochim. Biophys. Acta 1503, 210–228 (2001).

    Google Scholar 

  9. Siegbahn, P. E. Structures and energetics for O2 formation in photosystem II. Acc. Chem. Res. 42, 1871–1880 (2009).

    Google Scholar 

  10. Haumann, M. & Junge, W. Photosynthetic water oxidation: a simplex-scheme of its partial reactions. Biochim. Biophys. Acta 1411, 86–91 (1999).

    Google Scholar 

  11. McEvoy, J. P. & Brudvig, G. W. Water-splitting chemistry of photosystem II. Chem. Rev. 106, 4455–4483 (2006).

    Google Scholar 

  12. Yamanaka, S. et al. Possible mechanisms for the O–O bond formation in oxygen evolution reaction at the CaMn4O5 (H2O)4 cluster of PSII refined to 1.9 Å X-ray resolution. Chem. Phys. Lett. 511, 138–145 (2011).

    Google Scholar 

  13. Jeoung, J. H. & Dobbek, H. Carbon dioxide activation at the Ni,Fe-cluster of anaerobic carbon monoxide dehydrogenase. Science 318, 1461–1464 (2007).

    Google Scholar 

  14. Ferreira, K. N., Iverson, T. M., Maghlaoui, K., Barber, J. & Iwata, S. Architecture of the photosynthetic oxygen-evolving center. Science 303, 1831–1838 (2004).

    Google Scholar 

  15. 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).

    Google Scholar 

  16. Zhang, C. et al. A synthetic Mn4Ca-cluster mimicking the oxygen-evolving center of photosynthesis. Science 348, 690–693 (2015).

    Google Scholar 

  17. Dobbek, H., Svetlitchnyi, V., Gremer, L., Huber, R. & Meyer, O. Crystal structure of a carbon monoxide dehydrogenase reveals a [Ni-4Fe-5S] cluster. Science 293, 1281–1285 (2001).

    Google Scholar 

  18. Pecoraro, V. L., Baldwin, M. J., Caudle, M. T., Hsieh, W. Y. & Law, N. A. A proposal for water oxidation in photosystem II. Pure Appl. Chem. 70, 925–929 (1998).

    Google Scholar 

  19. Limburg, J., Brudvig, G. W. & Crabtree, R. H. O2 evolution and permanganate formation from high-valent manganese complexes. J. Am. Chem. Soc. 119, 2761–2762 (1997).

    Google Scholar 

  20. Hoganson, C. W. & Babcock, G. T. A metalloradical mechanism for the generation of oxygen from water in photosynthesis. Science 277, 1953–1956 (1997).

    Google Scholar 

  21. Dau, H. & Haumann, M. Eight steps preceding O–O bond formation in oxygenic photosynthesis—a basic reaction cycle of the photosystem II manganese complex. Biochim. Biophys. Acta 1767, 472–483 (2007).

    Google Scholar 

  22. Tommos, C. & Babcock, G. T. Oxygen production in nature: a light-driven metalloradical enzyme process. Acc. Chem. Res. 31, 18–25 (1998).

    Google Scholar 

  23. Askerka, M., Wang, J., Vinyard, D. J., Brudvig, G. W. & Batista, V. S. S3 state of the O2-evolving complex of photosystem II: insights from QM/MM, EXAFS, and femtosecond X-ray diffraction. Biochemistry 55, 981–984 (2016).

    Google Scholar 

  24. Limburg, J. et al. A functional model for O–O bond formation by the O2-evolving complex in photosystem II. Science 283, 1524–1527 (1999).

    Google Scholar 

  25. Gao, Y., Åkermark, T., Liu, J., Sun, L. & Åkermark, B. Nucleophilic attack of hydroxide on a MnV oxo complex: a model of the O−O bond formation in the oxygen evolving complex of photosystem II. J. Am. Chem. Soc. 131, 8726–8727 (2009).

    Google Scholar 

  26. Tong, L., Duan, L., Xu, Y., Privalov, T. & Sun, L. Structural modifications of mononuclear ruthenium complexes: a combined experimental and theoretical study on the kinetics of ruthenium-catalyzed water oxidation. Angew. Chem. Int. Ed. 50, 445–449 (2011).

    Google Scholar 

  27. Staehle, R. et al. Water oxidation catalyzed by mononuclear ruthenium complexes with a 2, 2′-bipyridine-6, 6′-dicarboxylate (bda) ligand: how ligand environment influences the catalytic behaviour. Inorg. Chem. 53, 1307–1319 (2014).

    Google Scholar 

  28. Duan, L. et al. A molecular ruthenium catalyst with water-oxidation activity comparable to that of photosystem II. Nat. Chem. 4, 418–423 (2012).

    Google Scholar 

  29. Siegbahn, P. E. M. A structure-consistent mechanism for dioxygen formation in photosystem II. Chemistry 14, 8290–8302 (2008).

    Google Scholar 

  30. Siegbahn, P. E. M. O–O bond formation in the S4 state of the oxygen evolving complex in photosystem II. Chem. Eur. J. 12, 9217–9237 (2006).

    Google Scholar 

  31. Siegbahn, P. E. & Crabtree, R. H. Manganese oxyl radical intermediates and O–O bond formation in photosynthetic oxygen evolution and a proposed role for the calcium cofactor in photosystem II. J. Am. Chem. Soc. 121, 117–127 (1999).

    Google Scholar 

  32. Zimmermann, J. L. & Rutherford, A. W. Electron paramagnetic resonance properties of the S2 state of the oxygen-evolving complex of photosystem II. Biochemistry 25, 4609–4615 (1986).

    Google Scholar 

  33. Messinger, J., Badger, M. & Wydrzynski, T. Detection of one slowly exchanging substrate water molecule in the S3 state of photosystem II. Proc. Natl Acad. Sci. USA 92, 3209–3213 (1995).

    Google Scholar 

  34. Vrettos, J. S., Limburg, J. & Brudvig, G. W. Mechanism of photosynthetic water oxidation: combining biophysical studies of photosystem II with inorganic model chemistry. Biochim. Biophys. Acta 1503, 229–245 (2001).

    Google Scholar 

  35. Sproviero, E. M., Gascón, J. A., McEvoy, J. P., Brudvig, G. W. & Batista, V. S. Quantum mechanics/molecular mechanics study of the catalytic cycle of water splitting in photosystem II. J. Am. Chem. Soc. 130, 3428–3442 (2008).

    Google Scholar 

  36. Vinyard, D. J., Khan, S. & Brudvig, G. W. Photosynthetic water oxidation: binding and activation of substrate waters for O–O bond formation. Farad. Discuss. 185, 37–50 (2015).

    Google Scholar 

  37. Hendry, G. & Wydrzynski, T. The two substrate−water molecules are already bound to the oxygen-evolving complex in the S2 state of photosystem II. Biochemistry 41, 13328–13334 (2002).

    Google Scholar 

  38. Nilsson, H., Rappaport, F., Boussac, A. & Messinger, J. Substrate–water exchange in photosystem II is arrested before dioxygen formation. Nat. Commun. 5, 4305 (2014).

    Google Scholar 

  39. Hendry, G. & Wydrzynski, T. 18O isotope exchange measurements reveal that calcium is involved in the binding of one substrate-water molecule to the oxygen-evolving complex in photosystem II. Biochemistry 42, 6209–6217 (2003).

    Google Scholar 

  40. Kern, J. et al. Simultaneous femtosecond X-ray spectroscopy and diffraction of photosystem II at room temperature. Science 340, 491–495 (2013).

    Google Scholar 

  41. Kupitz, C. et al. Serial time-resolved crystallography of photosystem II using a femtosecond X-ray laser. Nature 513, 261–265 (2014).

    Google Scholar 

  42. Suga, M. et al. Native structure of photosystem II at 1.95 Å resolution viewed by femtosecond X-ray pulses. Nature 517, 99–103 (2015).

    Google Scholar 

  43. Young, I. D. et al. Structure of photosystem II and substrate binding at room temperature. Nature 540, 453–457 (2016).

    Google Scholar 

  44. Siegbahn, P. E. Water oxidation mechanism in photosystem II, including oxidations, proton release pathways, O–O bond formation and O2 release. Biochim. Biophys. Acta 1827, 1003–1019 (2013).

    Google Scholar 

  45. Winkler, J. R. & Gray, H. B. in Molecular Electronic Structures of Transition Metal Complexes I (eds Mingos, D. M. P., Day, P. & Dahl, J. P. ) 17–28 (Springer, 2011).

    Google Scholar 

  46. Mukherjee, S. et al. Synthetic model of the asymmetric [Mn3CaO4] cubane core of the oxygen-evolving complex of photosystem II. Proc. Natl Acad. Sci. USA 109, 2257–2262 (2012).

    Google Scholar 

  47. Kanady, S., Tsui, E., Day, M. & Agapie, T. A synthetic model of the Mn3Ca subsite of the oxygen-evolving complex in photosystem II. Science 333, 733–736 (2011).

    Google Scholar 

  48. Suga, M. et al. Light-induced structural changes and the site of O=O bond formation in PSII caught by XFEL. Nature 543, 131–135 (2017).

    Google Scholar 

  49. Fesseler, J., Jeoung, J.-H. & Dobbek, H. How the [NiFe4S4] cluster of CO dehydrogenase activates CO2 and NCO. Angew. Chem. Int. Ed. 54, 8560–8564 (2015).

    Google Scholar 

Download references

Acknowledgements

I want to dedicate this paper to the late G. Babcock, who influenced much of my thinking about the mechanism of water oxidation in PSII over the years. I would also like to thank R. Huber, who in 2007 told me about Fe-Ni CODH after a lecture I gave on PSII at the University of Cardiff, UK. Finally, I most sincerely thank J. Murray, who helped me with the construction of Fig. 2, and R. Malkin, who encouraged me to write this paper after discussing my ideas with him in the quiet and peaceful ambience of Lago d'Orta, Italy in September 2016.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to James Barber.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Barber, J. A mechanism for water splitting and oxygen production in photosynthesis. Nature Plants 3, 17041 (2017). https://doi.org/10.1038/nplants.2017.41

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1038/nplants.2017.41

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