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