Monitoring Proton Release during Photosynthetic Water Oxidation in Photosystem II by Means of Isotope-Edited Infrared Spectroscopy

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.

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FTIR detection of water reactions in the oxygen-evolving centre of photosystem II

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2007.2214 ◽

2007 ◽

Vol 363 (1494) ◽

pp. 1189-1195 ◽

Cited By ~ 107

Author(s):

Takumi Noguchi

Keyword(s):

Photosystem Ii ◽

Water Oxidation ◽

State Transitions ◽

Proton Release ◽

Difference Spectra ◽

Band Shift ◽

Bonding Structure ◽

Ph Dependency ◽

Ftir Difference Spectroscopy ◽

Oxygen Evolving

Flash-induced Fourier transform infrared (FTIR) difference spectroscopy has been used to study the water-oxidizing reactions in the oxygen-evolving centre of photosystem II. Reactions of water molecules were directly monitored by detecting the OH stretching bands of weakly H-bonded OH of water in the 3700–3500 cm −1 region in FTIR difference spectra during S-state cycling. In the S 1 →S 2 transition, a band shift from 3588 to 3617 cm −1 was observed, indicative of a weakened H-bond. Decoupling experiments using D 2 O : H 2 O (1 : 1) showed that this OH arose from a water molecule with an asymmetric H-bonding structure and this asymmetry became more significant upon S 2 formation. In the S 2 →S 3 , S 3 →S 0 and S 0 →S 1 transitions, negative bands were observed at 3634, 3621 and 3612 cm −1 , respectively, representing formation of a strong H-bond or a proton release reaction. In addition, using complex spectral features in the carboxylate stretching region (1600–1300 cm −1 ) as ‘fingerprints’ of individual S-state transitions, pH dependency of the transition efficiencies and the effect of dehydration were examined to obtain the information of proton release and water insertion steps in the S-state cycle. Low-pH inhibition of the S 2 →S 3 , S 3 →S 0 and S 0 →S 1 transitions was consistent with a view that protons are released in the three transitions other than S 1 →S 2 , while relatively high susceptibility to dehydration in the S 2 →S 3 and S 3 →S 0 transitions suggested the insertion of substrate water into the system during these transitions. Thus, a possible mechanism of water oxidation to explain the FTIR data is proposed.

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1P257 Proton-coupled electron transfer mechanism of photosynthetic water oxidation as revealed by time-resolved infrared spectroscopy(18B. Photobiology:Photosynthesis,Poster,The 52nd Annual Meeting of the Biophysical Society of Japan(BSJ2014))

Seibutsu Butsuri ◽

10.2142/biophys.54.s183_5 ◽

2014 ◽

Vol 54 (supplement1-2) ◽

pp. S183

Author(s):

Hiroki Sakamoto ◽

Ryo Nagao ◽

Takumi Noguchi

Keyword(s):

Electron Transfer ◽

Infrared Spectroscopy ◽

Annual Meeting ◽

Water Oxidation ◽

Time Resolved ◽

Electron Transfer Mechanism ◽

Proton Coupled Electron Transfer ◽

Biophysical Society ◽

Time Resolved Infrared Spectroscopy ◽

Photosynthetic Water Oxidation

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

10.1101/2021.09.30.462629 ◽

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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