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Project Progress

Moderate external partial pressure of pure oxygen (~ 7-15 bars) was recently shown to reversibly prevent photosynthetic production of oxygen in (prokaryote) cyanobacteria, by a mechanism involving reversal of the water oxidation/O₂ evolution reaction cycle of Photosystem II (PSII). If true, this observation severely limits the range of photoautotrophic metabolism in the universe and on Earth. We investigated this claim by building a high pressure sample chamber used to measure variable fluorescence yield (described in the previous year), and measured the yield of chlorophyll-a variable fluorescence at 10 bar O₂ backpressure. These experiments indicate that high O₂ pressure slowly inactivates cells by a light dependent, Photosystem I-mediated mechanism involving photoreduction of O₂ that forms superoxide and peroxide. Contrary to the literature report, we find no evidence that high O₂ pressure reverses the water oxidation/O₂ evolution reaction cycle or influences the efficiency of this process in any detectable way before the onset of cell inactivation. These results have been observed in cells from both cyanobacteria and higher plants and thus have wide applicability. We may conclude that oxygenic photosynthesis is not constrained to environments of low O₂ partial pressures.

A brief description of the problem and the manuscript are outlined in the IPTAI 2005 annual report to the NASA Astrobiology Institute. The innovation of oxygenic photosynthesis is argued to have transformed the Earth’s atmosphere and been the driving force that led to the evolution of O₂-based respiratory metabolisms. At the heart of this biological innovation is the photosystem II (PSII) enzyme complex with ability to split water into O₂. Previously, it was postulated that the first oxygenic PSII may have originated from an anoxygenic phototroph that lived on ferrous metal complexes for an electron source and later bound and photo-oxidized Mn2+ in the form of bicarbonate complexes (Dismukes 2001, Proceedings of National Academy of Science). To test this hypothesis, both electrochemistry and electron paramagnetic resonance (EPR) spectroscopies were used to characterize Mn2+ bicarbonate complexes that form in solution and their efficacy as electron donors to PSII. The charge and structure of these complexes together with the greatly reduced oxidation potential to Mn₃⁺ explains why bicarbonate stimulates the rate of photo-assembly of the Mn₄CaO_x-cluster during biogenesis of PSII in whole cells. This work supports the hypothesis that carbonate is essential in some PSII’s and could have played a key role in the evolution of oxygenic photosynthesis in the CO₂-rich Archean era.