Dynamics of Proton Transfer to Internal Water during the Photosynthetic Oxygen-Evolving Cycle

Brahmachari, Udita; Barry, Bridgette A.

doi:10.1021/acs.jpcb.6b10164

Cited by 10 publications

(31 citation statements)

References 64 publications

(240 reference statements)

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“…In bacteriorhodopin, transient infrared spectroscopy has been used to detect catalytically important protonation of internal water . We recently used infrared spectroscopy and acquired evidence that an internal small cluster of water can be protonated during the S 1 to S 2 transition in PSII. − The S state cycle provides a unique opportunity for infrared studies. The OEC can be advanced by excitation with short laser flashes (532 nm, green arrows, Figure A).…”

Section: Methods and Resultsmentioning

confidence: 99%

“…Due to its low frequency, high intensity, D 2 O effect, and large apparent 18 O isotope shift at 263 K, this band was assigned to a stretching vibration of a cationic water cluster, formed during the S 1 to S 2 transition. These observations are not consistent with assignment of all intensity in this band to a proton polarizability band or a hydrogen-bonded water molecule (see ref and Table S1 in the Supporting Information). Hydronium ion bands in this region may be coupled with NH modes from amino acid side chains (Table S1).…”

Section: Methods and Resultsmentioning

confidence: 99%

“…RIFT-IR spectroscopy and laser flash advancement were used to flash through the S state cycle and to record the infrared spectrum of the S 3 to S 0 transition (pH 7.5, 263 K). A band at 3074 cm –1 (Figure E, black) was observed and assigned to a protonated water cluster based on D 2 O and H 2 18 O (Figure F, blue) solvent exchange . The band was also reduced in amplitude by the removal of calcium at pH 7.5.…”

Section: Methods and Resultsmentioning

confidence: 99%

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Tracking Reactive Water and Hydrogen-Bonding Networks in Photosynthetic Oxygen Evolution

2017

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In oxygenic photosynthesis, photosystem II (PSII) converts water to molecular oxygen through four photodriven oxidation events at a MnCaO cluster. A tyrosine, YZ (Y161 in the D1 polypeptide), transfers oxidizing equivalents from an oxidized, primary chlorophyll donor to the metal center. Calcium or its analogue, strontium, is required for activity. The MnCaO cluster and YZ are predicted to be hydrogen bonded in a water-containing network, which involves amide carbonyl groups, amino acid side chains, and water. This hydrogen-bonded network includes amino acid residues in intrinsic and extrinsic subunits. One of the extrinsic subunits, PsbO, is intrinsically disordered. This extensive (35 Å) network may be essential in facilitating proton release from substrate water. While it is known that some proteins employ internal water molecules to catalyze reactions, there are relatively few methods that can be used to study the role of water. In this Account, we review spectroscopic evidence from our group supporting the conclusion that the PSII hydrogen-bonding network is dynamic and that water in the network plays a direct role in catalysis. Two approaches, transient electron paramagnetic resonance (EPR) and reaction-induced FT-IR (RIFT-IR) spectroscopies, were used. The EPR experiments focused on the decay kinetics of YZ• via recombination at 190 K and the solvent isotope, pH, and calcium dependence of these kinetics. The RIFT-IR experiments focused on shifts in amide carbonyl frequencies, induced by photo-oxidation of the metal cluster, and on the isotope-based assignment of bands to internal, small protonated water clusters at 190, 263, and 283 K. To conduct these experiments, PSII was prepared in selected steps along the catalytic pathway, the S state cycle (n = 0-4). This cycle ultimately generates oxygen. In the EPR studies, S-state dependent changes were observed in the YZ• lifetime and in its solvent isotope effect. The YZ• lifetime depended on the presence of calcium at pH 7.5, but not at pH 6.0, suggesting a two-donor model for PCET. At pH 6.0 or 7.5, barium and ammonia both slowed the rate of YZ• recombination, consistent with disruption of the hydrogen-bonding network. In the RIFT-IR studies of the S state transitions, infrared bands associated with the transient protonation and deprotonation of internal waters were identified by DO and HO labeling. The infrared bands of these protonated water clusters, W (or nHO(HO), n = 5-6), exhibited flash dependence and were produced during the S to S and S to S transitions. Calcium dependence was observed at pH 7.5, but not at pH 6.0. S-state induced shifts were observed in amide C═O frequencies during the S to S transition and attributed to alterations in hydrogen bonding, based on ammonia sensitivity. In addition, isotope editing of the extrinsic subunit, PsbO, established that amide vibrational bands of this lumenal subunit respond to the S state transitions and that PsbO is a structural template for the reaction center. Taken together, these spectroscopic results su...

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Section: Methods and Resultsmentioning

confidence: 99%

Section: Methods and Resultsmentioning

confidence: 99%

Section: Methods and Resultsmentioning

confidence: 99%

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Tracking Reactive Water and Hydrogen-Bonding Networks in Photosynthetic Oxygen Evolution

2017

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“…3C). In one stage of the oxygen-generating cycle, a hydrogen-bonded cluster of water molecules at this site acts as a catalytic proton acceptor, storage site, and donor (63)(64)(65): an example of bound water serving as a reactive chemical substrate.…”

Section: How Hydration Water Assists Protein Functionmentioning

confidence: 99%

Water is an active matrix of life for cell and molecular biology

Ball

2017

Proc. Natl. Acad. Sci. U.S.A.

338

290

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Szent-Gy} orgi called water the "matrix of life" and claimed that there was no life without it. This statement is true, as far as we know, on our planet, but it is not clear whether it must hold throughout the cosmos. To evaluate that question requires a close consideration of the many varied and subtle roles that water plays in living cells-a consideration that must be free of both an assumed essentialism that gives water an almost mystical life-giving agency and a traditional tendency to see it as a merely passive solvent. Water is a participant in the "life of the cell," and here I describe some of the features of that active agency. Water's value for molecular biology comes from both the structural and dynamic characteristics of its status as a complex, structured liquid as well as its nature as a polar, protic, and amphoteric reagent. Any discussion of water as life's matrix must, however, begin with an acknowledgment that our understanding of it as both a liquid and a solvent is still incomplete.water | hydration | hydrophobic effect | protein chemistry | solvation chemistry

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“…Conventional steady-state S-state difference spectra collected hundreds of milliseconds after the laser flash could reflect the changes directly coupled to the stable light-induced oxidation state changes of manganese ions, as often assumed so far 15,16 (but see also ref. 17 ). Then, the steady-state difference spectrum should correspond to the DAS of the tO2 (= 2.5 ms) component, as indeed visible in Fig.…”

Section: Pivotal Proton Vacancy By Sidechain Deprotonationmentioning

confidence: 99%

The electron-proton bottleneck of photosynthetic oxygen evolution

Dau

Greife

Schönborn

et al. 2022

Preprint

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Photosynthesis fuels life on Earth by storing solar energy in chemical form, inspiring technological schemes for sustainable fuel production. Today’s oxygen-rich atmosphere results from photosynthetic O2-production during water-splitting at the protein-bound manganese cluster of photosystem II. Formation of the O2 molecule starts from a state with four accumulated electron holes, the S4-state, postulated half a century ago1 and remaining enigmatic ever since. Here we resolve this missing key element in photosynthetic O2-formation and its crucial mechanistic role. We tracked 230,000 excitation cycles of dark-adapted photosystems with microsecond infrared spectroscopy. Combing these results with computational chemistry reveals that in S4 not only are four electron holes accumulated by metal ion and protein sidechain oxidation, but also a crucial proton vacancy is created through gated sidechain deprotonation. Subsequently, a reactive oxygen radical is formed in an astonishing single-electron multi-proton transfer event. This is the slowest step in photosynthetic O2-formation – despite its low energetic barrier – due to entropic slowdown. In conjunction with previous breakthroughs in experimental and computational investigations, a compelling atomistic picture of photosynthetic O2-formation emerges. Our results provide insight into a biological process that has probably operated in the same unique way for three billion years and are expected to support the knowledge-based design of artificial water-splitting systems.

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Dynamics of Proton Transfer to Internal Water during the Photosynthetic Oxygen-Evolving Cycle

Cited by 10 publications

References 64 publications

Tracking Reactive Water and Hydrogen-Bonding Networks in Photosynthetic Oxygen Evolution

Tracking Reactive Water and Hydrogen-Bonding Networks in Photosynthetic Oxygen Evolution

Water is an active matrix of life for cell and molecular biology

The electron-proton bottleneck of photosynthetic oxygen evolution

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