Azide as a Probe of Proton Transfer Reactions in Photosynthetic Oxygen Evolution

Cooper, Ian B.; Barry, Bridgette A.

doi:10.1529/biophysj.108.136879

Cited by 9 publications

(11 citation statements)

References 73 publications

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“…Accompanying dramatic decreases in intensity in the mid-infrared region were also observed (compare Figure S5C,D, green). Compared to the previous mid-infrared report in the literature, 26,40,72 the intensity change in the mid-infrared region in Figure S5 is more extensive, consistent with more effective chloride depletion in this type of preparation and with this method.…”

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confidence: 82%

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Chloride Maintains a Protonated Internal Water Network in the Photosynthetic Oxygen Evolving Complex

et al. 2017

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In photosystem II (PSII), water oxidation occurs at a MnCaO cluster and results in production of molecular oxygen. The MnCaO cluster cycles among five oxidation states, called S states. As a result, protons are released at the metal cluster and transferred through a 35 Å hydrogen-bonding network to the lumen. At 283 K, an infrared band at 2830 cm is assigned to an internal solvated hydronium ion via HO solvent exchange. This result is similar to a previous report at 263 K. Computations on an oxygen evolving complex model predict that chloride can stabilize a hydronium ion on a network of nine water molecules. In this model, a HO stretching mode at 2738 cm is predicted to shift to higher frequency with bromide and to lower frequency with nitrate substitution. The calculated frequencies were compared to S-minus-S reaction-induced Fourier transform infrared spectra acquired from chloride-, bromide-, or nitrate-containing PSII samples, which were active in oxygen evolution. As predicted, the frequency of the 2830 cm band shifted to higher energy with bromide and to lower energy with nitrate substitution. These results support the conclusion that an internal hydronium ion and chloride play a direct role in an internal proton transfer event during the S-to-S transition.

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confidence: 82%

“…Note that the literature contains reports of anion replacement and depletion in "salt washed" PSII and BBY membranes. 26,40,72 However, the 2800 cm −1 region was not reported in those previous studies.…”

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confidence: 67%

Chloride Maintains a Protonated Internal Water Network in the Photosynthetic Oxygen Evolving Complex

et al. 2017

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“…Reactioninduced FTIR difference spectroscopy was performed as described (18,20,41,51) at 263 or 283 K and at pH 7.5. Briefly, a calcium-depleted sample was thawed and pelleted.…”

Section: Methodsmentioning

confidence: 99%

Detection of an intermediary, protonated water cluster in photosynthetic oxygen evolution

Polander

Barry

2013

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

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In photosynthesis, photosystem II evolves oxygen from water by the accumulation of photooxidizing equivalents at the oxygenevolving complex (OEC). The OEC is a Mn 4 CaO 5 cluster, and its sequentially oxidized states are termed the S n states. The darkstable state is S 1 , and oxygen is released during the transition from S 3 to S 0 . In this study, a laser flash induces the S 1 to S 2 transition, which corresponds to the oxidation of Mn(III) to Mn(IV). A broad infrared band, at 2,880 cm, is produced during this transition. Experiments using ammonia and 2 H 2 O assign this band to a cationic cluster of internal water molecules, termed "W 5 + ." Observation of the W 5 + band is dependent on the presence of calcium, and flash dependence is observed. These data provide evidence that manganese oxidation during the S 1 to S 2 transition results in a coupled proton transfer to a substrate-containing, internal water cluster in the OEC hydrogen-bonded network. Internal proton transfer reactions play important catalytic roles in many integral membrane proteins. In these enzymes, including bacteriorhodopsin, light-driven or redox-coupled proton-transfer reactions lead to the production of a transmembrane, electrochemical gradient. Amino acid side chains often participate in the acid/base chemistry that occurs in proton-transfer pathways. However, internal bound water clusters can also play essential roles as proton donors or acceptors (reviewed in ref. 1).In photosystem II (PSII), proton transfer contributes to the generation of a transmembrane potential, and chemical protons are released from the substrate, water, during the light-driven reactions that produce molecular oxygen (2). PSII is a complex membrane protein consisting of both integral, membrane-spanning subunits and extrinsic subunits (3). A monomeric unit of PSII consists of at least 20 distinct protein subunits, which are composed of 17 integral subunits and 3 extrinsic polypeptides (4, 5). The primary subunits that make up the reaction center and bind most of the redox-active cofactors are D1, D2, CP43, and CP47. The light-induced electron transfer pathway in the reaction center involves the dimeric chlorophyll (chl) donor, P 680 , and accessory chl molecules. One light-induced charge separation oxidizes the primary donor, P 680 , and reduces a bound plastoquinone acceptor, Q A . P 680 + oxidizes a tyrosine residue, YZ, Y161 of the D1 polypeptide, which is a powerful oxidant. YZ• oxidizes the oxygen-evolving complex (OEC) on each photoinduced charge separation (reviewed in ref. 6).The OEC is a Mn 4 CaO 5 cluster ( Fig. 1 A, Inset) (5). Oxygen release from the OEC fluctuates with period four (7). The OEC cycles through five sequentially oxidized states, called the S n states. A single flash given to a dark-adapted sample (S 1 state) generates the S 2 state (Fig. 1A), which corresponds to the oxidation of Mn(III) to Mn(IV) (8). Subsequent flashes advance the remaining manganese ions to higher oxidation states, with an accompanying deprotonation of two bound wat...

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“…Reaction-induced FT-IR difference spectroscopy was performed at 263 K and pH 7.5, and in the presence of 7 mM potassium ferricyanide, as previously described (17,(46)(47)(48). The resuspended sample, described above, was thawed and pelleted.…”

Section: Methodsmentioning

confidence: 99%

A hydrogen-bonding network plays a catalytic role in photosynthetic oxygen evolution

Polander

Barry

2012

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

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In photosystem II, oxygen evolution occurs by the accumulation of photo-induced oxidizing equivalents at the oxygen-evolving complex (OEC). The sequentially oxidized states are called the S 0 -S 4 states, and the dark stable state is S 1 . Hydrogen bonds to water form a network around the OEC; this network is predicted to involve multiple peptide carbonyl groups. In this work, we tested the idea that a network of hydrogen bonded water molecules plays a catalytic role in water oxidation. As probes, we used OEC peptide carbonyl frequencies, the substrate-based inhibitor, ammonia, and the sugar, trehalose. Reaction-induced FT-IR spectroscopy was used to describe the protein dynamics associated with the S 1 to S 2 transition. A shift in an amide CO vibrational frequency (1664 (S 1 ) to 1653 (S 2 ) cm −1 ) was observed, consistent with an increase in hydrogen bond strength when the OEC is oxidized. Treatment with ammonia/ammonium altered these CO vibrational frequencies. The ammonia-induced spectral changes are attributed to alterations in hydrogen bonding, when ammonia/ammonium is incorporated into the OEC hydrogen bond network. The ammonia-induced changes in CO frequency were reversed or blocked when trehalose was substituted for sucrose. This trehalose effect is attributed to a displacement of ammonia molecules from the hydrogen bond network. These results imply that ammonia, and by extension water, participate in a catalytically essential hydrogen bond network, which involves OEC peptide CO groups. Comparison to the ammonia transporter, AmtB, reveals structural similarities with the bound water network in the OEC.amide carbonyl frequency | Amt B transporter | photosystem II | vibrational spectroscopy | water oxidation I n oxygenic photosynthesis, photosystem II (PSII) catalyzes the oxidation of water and reduction of plastoquinone (1). Each reaction center includes the transmembrane subunits D1, D2, CP43, and CP47, which bind the redox-active cofactors. After photoexcitation, a charge separation is generated between the dimeric chl donor, P 680 , and a bound plastoquinone, Q A . Q A − reduces a second quinone, Q B , and P 680 þ oxidizes a tyrosine residue, YZ, Y161 in the D1 polypeptide. The radical, YZ•, is a powerful oxidant (2). Under physiological conditions, YZ• oxidizes the Mn 4 CaO 5 cluster, where water oxidation occurs (3). Four sequential photooxidations lead to the release of molecular oxygen (4). The oxygen yield fluctuates with period four. The sequentially oxidized states of the Mn cluster are called the Sn states, where n refers to the number of oxidizing equivalents stored at the OEC. S 1 is the dark stable state of the OEC. A single flash given to a dark-adapted sample of PSII generates the S 2 state, which corresponds to the oxidation of Mn(III) to Mn (IV) (5). The water oxidation chemistry in the S state cycle occurs on the microsecond to millisecond time scale, and oxygen is released during the S 3 to S 0 transition (4, 6).The structure of PSII has been reported at a resolution of 1.9 Å (3). T...

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Azide as a Probe of Proton Transfer Reactions in Photosynthetic Oxygen Evolution

Cited by 9 publications

References 73 publications

Chloride Maintains a Protonated Internal Water Network in the Photosynthetic Oxygen Evolving Complex

Chloride Maintains a Protonated Internal Water Network in the Photosynthetic Oxygen Evolving Complex

Detection of an intermediary, protonated water cluster in photosynthetic oxygen evolution

A hydrogen-bonding network plays a catalytic role in photosynthetic oxygen evolution

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