Carboxylate Shifts Steer Interquinone Electron Transfer in Photosynthesis

Chernev, Petko; Zaharieva, Ivelina; Dau, Holger; Haumann, Michael

doi:10.1074/jbc.m110.202879

Cited by 33 publications

(30 citation statements)

References 62 publications

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“…It seems reasonable to expect that both mechanisms would lower the redox potential of Q A =Q −• A . These findings are relevant to an earlier suggestion based on X-ray absorption studies that the bidentate carboxylic acid binding to the nonheme iron becomes transiently monodentate on Q −• A formation (40). That said, it also seems possible that the presence of an uncompensated anion on Q A could make binding of the HCO 3 − anion less strong without the formation of a discrete monodentate intermediate.…”

Section: Added (Triangles) (D) Effect Of Preillumination On Hco 3 − supporting

confidence: 48%

Bicarbonate-induced redox tuning in Photosystem II for regulation and protection

Brinkert

Causmaecker

Krieger‐Liszkay

et al. 2016

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

120

173

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The midpoint potential (E m ) of Q A =Q −• A , the one-electron acceptor quinone of Photosystem II (PSII), provides the thermodynamic reference for calibrating PSII bioenergetics. Uncertainty exists in the literature, with two values differing by ∼80 mV. Here, we have resolved this discrepancy by using spectroelectrochemistry on plant PSII-enriched membranes. Removal of bicarbonate (HCO 3 − ) shifts the E m from ∼−145 mV to −70 mV. The higher values reported earlier are attributed to the loss of HCO 3 − during the titrations (pH 6.5, stirred under argon gassing). P hotosystem II (PSII), the water/plastoquinone photooxidoreductase, is at the heart of the major energy cycle that powers the biosphere. Chlorophyll-based photochemistry drives charge separation followed by electron transfer reactions that result in the reduction of quinone on one side of the thylakoid membrane ( Fig. 1) and the oxidation of water on the other. The photochemistry is intrinsically a one-photon/one-electron process, but the quinone reduction and water oxidation are two-and fourelectron processes, respectively. As a result, both processes involve the accumulation of intermediates that are stabilized by the protein and by coupling to protonation reactions (1-3).The electron acceptor side of PSII contains a nonheme ferrous iron (Fe 2+ ) that is flanked by the two quinones, Q A and Q B (Fig. 1) (reviewed in refs. 3 and 4). The Fe 2+ is coordinated by four histidine residues, two from D1 and two from D2, and a bicarbonate ion (HCO 3 − ) that provides a bidentate ligand (3-5). The HCO 3 − is thought to play a role in the Q B protonation pathway (reviewed in refs. 3-5). Recent EPR (6) and computation chemistry studies (7) based on the highest-resolution X-ray crystallographic model (8) implicated HCO 3 − in the second of two protonation steps that are associated with Q B reduction. Measurements of the dissociation constant of HCO 3 − (K d = 40-80 μM), compared with estimates of the HCO 3 − concentration in the stroma (reviewed in ref. 9), led to the assumption that HCO 3 − remains bound under physiological conditions (10). Recently, however, it was reported that the HCO 3 − bound to PSII in Chlamydomonas can be displaced by acetate when present in the culture medium (11).The redox potential of Q A has been the subject of research for decades (12). The current detailed thermodynamic picture of PSII redox chemistry is based on estimates of energy differences between the electron transfer components, but these estimates A , differing by ∼150 mV, depending on the nature of the PSII (12-14). The fully active enzyme showed an E m value that was ∼150 mV lower than that in PSII lacking the Mn 4 CaO 5 cluster. This shift was, in fact, due to the binding (or absence thereof) of the Ca 2+ ion involved in water splitting, but because the Mn cluster provides the Ca binding site, the potential is indirectly determined by the presence of Mn cluster (12)(13)(14). Given the high valence state on the Mn cluster even in the lowest redox state of the water splitti...

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Section: Added (Triangles) (D) Effect Of Preillumination On Hco 3 − supporting

confidence: 48%

Bicarbonate-induced redox tuning in Photosystem II for regulation and protection

Brinkert

Causmaecker

Krieger‐Liszkay

et al. 2016

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

120

173

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“…•-states do not result in dramatic differences in the bicarbonate ligation such as those proposed by Chernev et al (37). It seems possible that the changes in the environment of the nonheme Fe 2+ reported by Chernev et al using X-ray absorption spectroscopy could have resulted from the changes in the H-bond network associated with D1-Tyr246, D2-Tyr244, and the bicarbonate (Fig.…”

Section: •-mentioning

confidence: 71%

“…Because the atomic coordinates were unavailable, we could not evaluate the specific models discussed in ref. 37, however we addressed the same question in our calculations using the most recent structure (9). We could not observe such a dramatic (∼1 Å) change of the Fe-O bicarbonate bond.…”

Section: •-mentioning

confidence: 99%

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Mechanism of proton-coupled quinone reduction in Photosystem II

Saito

Rutherford

Ishikita

2012

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

136

161

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Photosystem II uses light to drive water oxidation and plastoquinone (PQ) reduction. PQ reduction involves two PQ cofactors, Q A and Q B , working in series. Q A is a one-electron carrier, whereas Q B undergoes sequential reduction and protonation to form Q B H 2 . Q B H 2 exchanges with PQ from the pool in the membrane. Based on the atomic coordinates of the Photosystem II crystal structure, we analyzed the proton transfer (PT) energetics adopting a quantum mechanical/molecular mechanical approach. The potential-energy profile suggests that the initial PT to Q B•-occurs from the protonated, D1-His252 to Q B •-via D1-Ser264. The second PT is likely to occur from D1-His215 to Q B H − via an H-bond with an energy profile with a single well, resulting in the formation of Q B H 2 and the D1-His215 anion. The pathway for reprotonation of D1-His215-may involve bicarbonate, D1-Tyr246 and water in the Q B site. Formate ligation to Fe 2+ did not significantly affect the protonation of reduced Q B , suggesting that formate inhibits Q B H 2 release rather than its formation. The presence of carbonate rather than bicarbonate seems unlikely because the calculations showed that this greatly perturbed the potential of the nonheme iron, stabilizing the Fe 3+ state in the presence of Q B•-, a situation not encountered experimentally. H-bonding from D1-Tyr246 and D2-Tyr244 to the bicarbonate ligand of the nonheme iron contributes to the stability of the semiquinones. A detailed mechanistic model for Q B reduction is presented.electron transfer gating | purple bacterial reaction center | low-barrier hydrogen bond | photoinhibition | tyrosine peroxide T he core of the Photosystem II (PSII) reaction center is composed of D1/D2, a heterodimer of protein subunits containing the cofactors involved in photochemical charge separation, quinone reduction, and water oxidation. These reactions are driven by light absorption by pigments absorbing around 680 nm (P680). P680 is composed of four chlorophyll a (Chla) molecules, P D1 /P D2 , Chl D1 /Chl D2 , and two pheophytin a molecules (Pheo D1 /Pheo D2 ). Excitation of P680 initially leads to the formation of a range of charge separated states, with the Chl D1•+ Pheo D1•− state dominating. After a short time the secondary radical pair, [P D1 /P D2 ], is formed in nearly all centers. This state is stabilized by electron transfer to the first quinone, Q A , and by electron donation from a tyrosine residue, D1-Tyr160 (TyrZ), to P D1• then oxidizes the Mn 4 CaO 5 cluster, which catalyzes the subsequent water splitting reaction. Q A /Q A •− acts as a one-electron redox couple, accepting electrons from Pheo D1•− and donating to the second quinone, Q B , without undergoing protonation itself. In contrast, Q B reduction involves two consecutive one-electron reduction reactions with a series of associated proton uptake reactions (reviewed in 1-6).Q B is located near the nonheme Fe 2+ and the ligand to the Fe 2+ , D1-His215, donates an H-bond to the Q B carbonyl O atom that is nearer to the Fe complex (...

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“…Density Functional Theory Calculations (DFT)-Spin-unrestricted geometry optimizations and calculations of electronic parameters of structural models of the metal sites were performed using the ORCA program package (79) as described previously (30,80). Geometry optimizations involved the BP86 exchange-correlation functional (81) with a triple-valence (TZVP) basis set (82).…”

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confidence: 99%

Rapid X-ray Photoreduction of Dimetal-Oxygen Cofactors in Ribonucleotide Reductase

Sigfridsson

Chernev

Leidel

et al. 2013

Journal of Biological Chemistry

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Background: Typical FeFe and MnFe cofactors bind to numerous enzymes such as ribonucleotide reductases. Crystallographic data suggest x-ray photoreduction (XPR) effects. Results: Rapid XPR-induced cofactor changes were monitored using time-resolved x-ray absorption spectroscopy. Conclusion: The XPR-induced cofactor states differ significantly from the native configurations, but comply with crystallographic structures. Significance: Structure determination for high-valent dimetal-oxygen cofactors requires free electron-laser protein crystallography combined with x-ray spectroscopy.

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Carboxylate Shifts Steer Interquinone Electron Transfer in Photosynthesis

Cited by 33 publications

References 62 publications

Bicarbonate-induced redox tuning in Photosystem II for regulation and protection

Bicarbonate-induced redox tuning in Photosystem II for regulation and protection

Mechanism of proton-coupled quinone reduction in Photosystem II

Rapid X-ray Photoreduction of Dimetal-Oxygen Cofactors in Ribonucleotide Reductase

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