scholarly journals Light-driven formation of high-valent manganese oxide by photosystem II supports evolutionary role in early bioenergetics

2020 ◽  
Author(s):  
Petko Chernev ◽  
Sophie Fischer ◽  
Jutta Hoffmann ◽  
Nicholas Oliver ◽  
Robert L. Burnap ◽  
...  
Keyword(s):  
Photosystem Ii ◽  
Water Oxidation ◽  
Early Stage ◽  
Oxygenic Photosynthesis ◽  
Oxide Nanoparticles ◽  
Mn Oxide ◽  
Oxide Particles ◽  
High Valent ◽  
Photosynthetic Water Oxidation ◽  
Mn Oxides

AbstractWater oxidation and concomitant O2-formation by the Mn4Ca 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, photosynthetic formation of Mn oxides from dissolved Mn(2+) ions may have played a key role in bioenergetics and possibly facilitated early geological manganese deposits. The biochemical evidence for the ability of photosystems to form extended Mn oxide particles, lacking until now, is provided herein. We tracked the light-driven redox processes in spinach photosystem II (PSII) particles devoid of the Mn4Ca clusters by UV-vis and X-ray spectroscopy. We find that oxidation of aqueous Mn(2+) ions results in PSII-bound Mn(III,IV)-oxide nanoparticles of the birnessite type comprising 50-100 Mn ions per PSII. Having shown that even today’s photosystem-II can form birnessite-type oxide particles efficiently, we propose an evolutionary scenario, which involves Mn-oxide production by ancestral photosystems, later followed by down-sizing of protein-bound Mn-oxide nanoparticles to finally yield today’s Mn4CaO5 cluster of photosynthetic water oxidation.

scholarly journals Light-driven formation of manganese oxide by today’s photosystem II supports evolutionarily ancient manganese-oxidizing photosynthesis

2020 ◽  
Vol 11 (1) ◽  
Author(s):  
Petko Chernev ◽  
Sophie Fischer ◽  
Jutta Hoffmann ◽  
Nicholas Oliver ◽  
Ricardo Assunção ◽  
...  
Keyword(s):  
Photosystem Ii ◽  
Manganese Oxide ◽  
Water Oxidation ◽  
Manganese Oxides ◽  
Early Stage ◽  
Oxygenic Photosynthesis ◽  
Oxide Nanoparticles ◽  
Manganese Ions ◽  
Oxide Particles ◽  
Photosynthetic Water Oxidation

AbstractWater 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.

scholarly journals Early Archean origin of Photosystem II

2017 ◽  
Author(s):  
Tanai Cardona ◽  
Patricia Sánchez-Baracaldo ◽  
A. William Rutherford ◽  
Anthony W. D. Larkum
Keyword(s):  
Photosystem Ii ◽  
Reaction Center ◽  
Water Oxidation ◽  
Photochemical Reaction ◽  
Early Stage ◽  
Oxygenic Photosynthesis ◽  
Recent Common Ancestor ◽  
Molecular Clocks ◽  
Most Recent Common Ancestor ◽  
History Of

AbstractPhotosystem II is a photochemical reaction center that catalyzes the light-driven oxidation of water to molecular oxygen. Water oxidation is the distinctive photochemical reaction that permitted the evolution of oxygenic photosynthesis and the eventual rise of Eukaryotes. At what point during the history of life an ancestral photosystem evolved the capacity to oxidize water still remains unknown. Here we study the evolution of the core reaction center proteins of Photosystem II using sequence and structural comparisons in combination with Bayesian relaxed molecular clocks. Our results indicate that a homodimeric photosystem with sufficient oxidizing power to split water had already appeared in the early Archean about a billion years before the most recent common ancestor of all described Cyanobacteria capable of oxygenic photosynthesis, and well before the diversification of some of the known groups of anoxygenic photosynthetic bacteria. Based on a structural and functional rationale we hypothesize that this early Archean photosystem was capable of water oxidation and had already evolved some level of protection against the formation of reactive oxygen species, which would place primordial forms of oxygenic photosynthesis at a very early stage in the evolutionary history of life.

scholarly journals Untangling the sequence of events during the S2→ S3transition in photosystem II and implications for the water oxidation mechanism

2020 ◽  
Vol 117 (23) ◽  
pp. 12624-12635 ◽  
Author(s):  
Mohamed Ibrahim ◽  
Thomas Fransson ◽  
Ruchira Chatterjee ◽  
Mun Hon Cheah ◽  
Rana Hussein ◽  
...  
Keyword(s):  
Photosystem Ii ◽  
Water Oxidation ◽  
Donor Site ◽  
Oxidation Mechanism ◽  
Oxygenic Photosynthesis ◽  
Acceptor Site ◽  
Oxygen Evolving Complex ◽  
Ps Ii ◽  
Sequence Of Events ◽  
Large Channel

In oxygenic photosynthesis, light-driven oxidation of water to molecular oxygen is carried out by the oxygen-evolving complex (OEC) in photosystem II (PS II). Recently, we reported the room-temperature structures of PS II in the four (semi)stable S-states, S1, S2, S3, and S0, showing that a water molecule is inserted during the S2→ S3transition, as a new bridging O(H)-ligand between Mn1 and Ca. To understand the sequence of events leading to the formation of this last stable intermediate state before O2formation, we recorded diffraction and Mn X-ray emission spectroscopy (XES) data at several time points during the S2→ S3transition. At the electron acceptor site, changes due to the two-electron redox chemistry at the quinones, QAand QB, are observed. At the donor site, tyrosine YZand His190 H-bonded to it move by 50 µs after the second flash, and Glu189 moves away from Ca. This is followed by Mn1 and Mn4 moving apart, and the insertion of OX(H) at the open coordination site of Mn1. This water, possibly a ligand of Ca, could be supplied via a “water wheel”-like arrangement of five waters next to the OEC that is connected by a large channel to the bulk solvent. XES spectra show that Mn oxidation (τ of ∼350 µs) during the S2→ S3transition mirrors the appearance of OXelectron density. This indicates that the oxidation state change and the insertion of water as a bridging atom between Mn1 and Ca are highly correlated.

scholarly journals Mediator-assisted water oxidation by the ruthenium “blue dimer” cis,cis-[(bpy)2(H2O)RuORu(OH2)(bpy)2]4+

2008 ◽  
Vol 105 (46) ◽  
pp. 17632-17635 ◽  
Author(s):  
Javier J. Concepcion ◽  
Jonah W. Jurss ◽  
Joseph L. Templeton ◽  
Thomas J. Meyer
Keyword(s):  
Carbon Dioxide ◽  
Electron Transfer ◽  
Renewable Energy ◽  
Photosystem Ii ◽  
Water Splitting ◽  
Water Oxidation ◽  
Oxygenic Photosynthesis ◽  
Reduced Water ◽  
Insight Into ◽  
Recent Insight

Light-driven water oxidation occurs in oxygenic photosynthesis in photosystem II and provides redox equivalents directed to photosystem I, in which carbon dioxide is reduced. Water oxidation is also essential in artificial photosynthesis and solar fuel-forming reactions, such as water splitting into hydrogen and oxygen (2 H2O + 4 hν → O2 + 2 H2) or water reduction of CO2 to methanol (2 H2O + CO2 + 6 hν → CH3OH + 3/2 O2), or hydrocarbons, which could provide clean, renewable energy. The “blue ruthenium dimer,” cis,cis-[(bpy)2(H2O)RuIIIORuIII(OH2)(bpy)2]4+, was the first well characterized molecule to catalyze water oxidation. On the basis of recent insight into the mechanism, we have devised a strategy for enhancing catalytic rates by using kinetically facile electron-transfer mediators. Rate enhancements by factors of up to ≈30 have been obtained, and preliminary electrochemical experiments have demonstrated that mediator-assisted electrocatalytic water oxidation is also attainable.

scholarly journals Electron, proton and hydrogen–atom transfers in photosynthetic water oxidation

2002 ◽  
Vol 357 (1426) ◽  
pp. 1383-1394 ◽  
Author(s):  
Cecilia Tommos
Keyword(s):  
Photosystem Ii ◽  
Proton Transfer ◽  
Water Oxidation ◽  
Oxidation Mechanism ◽  
Bulk Solution ◽  
Hydrogen Atoms ◽  
Redox Active ◽  
Hydrogen Atom Transfers ◽  
Reduce Carbon Dioxide ◽  
Photosynthetic Water Oxidation

When photosynthetic organisms developed so that they could use water as an electron source to reduce carbon dioxide, the stage was set for efficient proliferation. Algae and plants spread globally and provided the foundation for our atmosphere and for O 2 –based chemistry in biological systems. Light–driven water oxidation is catalysed by photosystem II, the active site of which contains a redox–active tyrosine denoted Y Z , a tetramanganese cluster, calcium and chloride. In 1995, Gerald Babcock and co–workers presented the hypothesis that photosynthetic water oxidation occurs as a metallo–radical catalysed process. In this model, the oxidized tyrosine radical is generated by coupled proton/electron transfer and re–reduced by abstracting hydrogen atoms from substrate water or hydroxide–ligated to the manganese cluster. The proposed function of Y Z requires proton transfer from the tyrosine site upon oxidation. The oxidation mechanism of Y Z in an inhibited and O 2 –evolving photosystem II is discussed. Domino–deprotonation from Y Z to the bulk solution is shown to be consistent with a variety of data obtained on metal–depleted samples. Experimental data that suggest that the oxidation of Y Z in O 2 –evolving samples is coupled to proton transfer in a hydrogen–bonding network are described. Finally, a dielectric–dependent model for the proton release that is associated with the catalytic cycle of photosystem II is discussed.

scholarly journals Fast enzymatic HCO3- dehydration supports photosynthetic water oxidation in Photosystem II from pea

2021 ◽  
Author(s):  
Alexandr V. Shitov ◽  
Vasily V. Terentyev ◽  
Govindjee Govindjee
Keyword(s):  
Photosystem Ii ◽  
Pisum Sativum ◽  
Water Oxidation ◽  
Photochemical Reactions ◽  
O2 Evolution ◽  
Donor Side ◽  
Psii Photochemistry ◽  
Similar Dependence ◽  
Enzymatic Nature ◽  
Photosynthetic Water Oxidation

Carbonic anhydrase (CA) activity, associated with Photosystem II (PSII) from Pisum sativum, has been shown to enhance water oxidation. But, the nature of the CA activity, its origin and role in photochemistry has been under debate, since the rates of CA reactions, measured earlier, were less than the rates of photochemical reactions. Here, we demonstrate high CA activity in PSII from Pisum sativum, measured by HCO3- dehydration at pH 6.5 (i.e. under optimal condition for PSII photochemistry), with kinetic parameters Km of 2.7 mM; Vmax of 2.74·10-2 mM·sec-1; kcat of 1.16·103 sec-1 and kcat/Km of 4.1·105 M-1 sec-1, showing the enzymatic nature of this activity, which kcat exceeds by ~13 times the rate of PSII, as measured by O2 evolution. The similar dependence of HCO3- dehydration, of the maximal quantum yield of photochemical reactions and of O2 evolution on the ratio of chlorophyll/photochemical reaction center II demonstrate the interconnection of these processes on the electron donor side of PSII. Since the removal of protons is critical for fast water oxidation, and since HCO3- dehydration consumes a proton, we suggest that CA activity, catalyzing very fast removal of protons, supports efficient water oxidation in PSII and, thus, photosynthesis in general.

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