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Manganese (Mn) is an essential element for life. Although its concentration is at (sub)nanomolar levels throughout the ocean, it affects the oxygen concentration of the ocean because it is central to the photosynthetic formation of dioxygen, O2, in photosystem center II. Mn inputs into the ocean are from atmospheric transport of particles and their dissolution to form dissolved Mn, and from the flux of dissolved Mn from rivers, sediments and hydrothermal vents. The main removal mechanism is transport of particulate Mn from dust and organic matter to the sediments. The environmental chemistry of manganese centers on its +2, +3 and +4 oxidation states. Most recent data show that Mn(II) is dissolved, that Mn(IV) is particulate MnO2, and that Mn(III) can be particulate or dissolved when bound to organic complexes [denoted as Mn(III)-L]. Mn(II) is oxidized primarily by microbial processes whereas MnO2 is reduced by abiotic and biotic processes. Photochemical processing aids redox cycling in surface waters. In suboxic zones, which are defined as areas with dissolved O2 concentrations below 3 M, both oxidation and reduction processes can occur but usually at different depths. In suboxic zones, dissolved Mn is also released from organic matter during its decomposition and from MnO2 reduction.
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Light-driven formation of manganese oxide by today’s photosystem II supports evolutionarily ancient manganese-oxidizing photosynthesis
Abstract Water oxidation and concomitant dioxygen formation by the manganese-calcium cluster of oxygenic photosynthesis has shaped the biosphere, atmosphere, and geosphere. It has been hypothesized that at an early stage of evolution, before photosynthetic water oxidation became prominent, light-driven formation of manganese oxides from dissolved Mn(2+) ions may have played a key role in bioenergetics and possibly facilitated early geological manganese deposits. Here we report the biochemical evidence for the ability of photosystems to form extended manganese oxide particles. The photochemical redox processes in spinach photosystem-II particles devoid of the manganese-calcium cluster are tracked by visible-light and X-ray spectroscopy. Oxidation of dissolved manganese ions results in high-valent Mn(III,IV)-oxide nanoparticles of the birnessite type bound to photosystem II, with 50-100 manganese ions per photosystem. Having shown that even today’s photosystem II can form birnessite-type oxide particles efficiently, we propose an evolutionary scenario, which involves manganese-oxide production by ancestral photosystems, later followed by down-sizing of protein-bound manganese-oxide nanoparticles to finally yield today’s catalyst of photosynthetic water oxidation.
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- Award ID(s):
- 1716408
- PAR ID:
- 10471521
- Publisher / Repository:
- Nature
- Date Published:
- Journal Name:
- Nature Communications
- Volume:
- 11
- Issue:
- 1
- ISSN:
- 2041-1723
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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The oxygen evolving complex (OEC) of photosystem II is responsible for the four-electron oxidation of water to dioxygen in oxygenic photosynthetic organisms. These organisms use light to drive this thermodynamically uphill process to harvest high-energy electrons from water for cellular energy, generating O2 as a byproduct. While numerous details of the operation of the OEC are well understood, the molecular mechanism of O=O formation remains under debate. Model complex chemistry from our group will be presented wherein we have prepared cluster systems with little or no terminal multidentate ligation in order to generate geometrically flexible and reactive clusters. Two systems will be presented: a series of Ca-Mn-O hemicubane clusters with variable calcium content, and their electrocatalytic activity in activation of water in oxidation reactions, and a Mn cubane cluster with a pendant Mn=O moiety that evolves dioxygen from an oxidation state analagous to the turnover state of the natural systemmore » « less
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null (Ed.)The role of geometric frustration of water molecules in the rate of water oxidation in the nanoconfined interlayer of manganese-oxide layered materials (birnessite, buserite) is examined in a well-controlled experiment. Calcium buserite is prepared, and used in a split-batch synthetic protocol to prepare calcium birnessite, sodium buserite, and sodium birnessite, and partially dehydrated sodium birnessite. Thus, four samples are prepared in which features effecting catalytic efficiency (defect density, average manganese oxidation state) are controlled, and the main difference is the degree of hydration of the interlayer (two layers of water in buserites vs. one layer of water in birnessite). Molecular dynamics simulations predict birnessite samples to exhibit geometric water frustration, which facilitates redox catalysis by lowering the Marcus reorganization energy of electron transfer, while buserite samples exhibit traditional intermolecular hydrogen bonding among the two-layer aqeuous region, leading to slower catalytic behavior akin to redox reactions in bulk water. Water oxdiation activity is investigated using chemical and electrochemical techniques, demonstrating and quantifying the role of water frustration in enhancing catalysis. Calculation and experiment demonstrate dehydrated sodium birnessite to be most effective, and calcium buserite the least effective, with a difference in electrocatlytic overpotential of ∼750 mV and a ∼20-fold difference in turnover number.more » « less
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- Free Publicly Accessible Full Text
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Accepted Manuscript
- Journal Article:
- https://doi.org/10.1038/s41467-020-19852-0
