Abstract
Photosynthetic water oxidation is a fundamental process that sustains the biosphere. A cluster embedded in the photosystem II protein environment is responsible for the production of atmospheric oxygen. Here, time-resolved x-ray emission spectroscopy (XES) is used to observe the process of oxygen formation in real time. These experiments reveal that the oxygen evolution step, initiated by three sequential laser flashes, is accompanied by rapid (within ) changes to the Mn XES spectrum. However, no oxidation of the core above the all- state is detected to precede bond formation, and the observed changes are therefore assigned to bond-formation dynamics. We propose that bond formation occurs prior to the transfer of the final (fourth) electron from the cluster to the oxidized tyrosine residue. This model resolves the kinetic limitations associated with bond formation and suggests an evolutionary adaptation to avoid releasing harmful peroxide species.
- Received 10 May 2018
- Revised 18 July 2018
DOI:https://doi.org/10.1103/PhysRevX.8.041014
Published by the American Physical Society under the terms of the Creative Commons Attribution 4.0 International license. Further distribution of this work must maintain attribution to the author(s) and the published article’s title, journal citation, and DOI.
Published by the American Physical Society
Physics Subject Headings (PhySH)
Synopsis
Pinning down the Chemistry of Photosynthetic Water Splitting
Published 23 October 2018
A time-resolved x-ray study indicates that certain chemical changes of oxygen atoms during photosynthesis occur in a different order than current models predict.
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Popular Summary
Society is faced with multiple challenges to energy security including increased energy demand, the scarcity of carbon-based fuels, and climate disruption as a result of using those fuels. Finding new ways of generating clean energy is therefore an imperative. Since green plants already do this with unparalleled efficiency, there is significant interest in echoing photosynthesis in artificial devices. Despite intense efforts from the biophysics community to understand this process on a mechanistic level, the final step remains a matter of speculation. In this work, we use very bright, short laser and x-ray pulses to drive photosynthesis and track electronic transitions through the process.
During photosynthesis, green plants use sunlight to extract electrons and protons needed to generate fuel, creating molecular oxygen as a byproduct. The critical step in which two oxygen atoms bond to form is the part that is not understood. Our experiments strongly suggest that this bond forms prior to the transfer of the last electron. We further show that this new catalytic mechanism promotes rearrangement of atoms and the formation of new molecules with the smallest possible waste of energy.
By providing a blueprint for mimicking this biological process, these results will accelerate the development of artificial photosynthesis on a scale large enough to address society’s future energy needs.