Calculated coupling of electron and proton transfer in the photosynthetic reaction center of Rhodopseudomonas viridis

Lancaster, C. Roy D.; Michel, Hartmut; Honig, Barry; Gunner, M. R.

doi:10.1016/s0006-3495(96)79820-x

Cited by 190 publications

(237 citation statements)

References 79 publications

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“…5, a triggering mechanism implies that coupling between (19,39) and (ii) proton binding by amino acids near Q B in response to Q A reduction (32,40,41). Electrostatic calculations also suggest coupling between the Q A and Q B binding sites (42,43).…”

Section: Discussionmentioning

confidence: 99%

Conformational gating of the electron transfer reaction Q _A ⁻ ^⋅ Q _B → Q _A Q _B ⁻ ^⋅ in bacterial reaction centers of Rhodobacter sphaeroides determined by a driving force assay

Graige

Fehér

Okamura

1998

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

209

235

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The mechanism of the electron transfer reaction, Q A ؊ ⅐ Q B 3 Q A Q B ؊ ⅐ , was studied in isolated reaction centers from the photosynthetic bacterium Rhodobacter sphaeroides by replacing the native Q 10 in the Q A binding site with quinones having different redox potentials. These substitutions are expected to change the intrinsic electron transfer rate by changing the redox free energy (i.e., driving force) for electron transfer without affecting other events that may be associated with the electron transfer (e.g., protein dynamics or protonation). The electron transfer from Q A ؊ ⅐ to Q B was measured by three independent methods: a functional assay involving cytochrome c 2 to measure the rate of Q A ؊ ⅐ oxidation, optical kinetic spectroscopy to measure changes in semiquinone absorption, and kinetic near-IR spectroscopy to measure electrochromic shifts that occur in response to electron transfer. The results show that the rate of the observed electron transfer from Q A ؊ ⅐ to Q B does not change as the redox free energy for electron transfer is varied over a range of 150 meV. The strong temperature dependence of the observed rate rules out the possibility that the reaction is activationless. We conclude, therefore, that the independence of the observed rate on the driving force for electron transfer is due to conformational gating, that is, the rate limiting step is a conformational change required before electron transfer. This change is proposed to be the movement, controlled kinetically either by protein dynamics or intermolecular interactions, of Q B by Ϸ5 Å as observed in the x-ray studies of Stowell et al.

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Section: Discussionmentioning

confidence: 99%

Conformational gating of the electron transfer reaction Q _A ⁻ ^⋅ Q _B → Q _A Q _B ⁻ ^⋅ in bacterial reaction centers of Rhodobacter sphaeroides determined by a driving force assay

Graige

Fehér

Okamura

1998

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

209

235

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“…However, the reactions need not be full deprotonation reactions of each site, but might consist of partial deprotonation reactions of interacting residues (see Ref. 52, for an example).…”

Section: Discussionmentioning

confidence: 99%

Deprotonation of the 33-kDa, Extrinsic, Manganese-stabilizing Subunit Accompanies Photooxidation of Manganese in Photosystem II

Hutchison¹,

Steenhuis²,

Yocum³

et al. 1999

Journal of Biological Chemistry

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Photosystem II catalyzes photosynthetic water oxidation. The oxidation of water to molecular oxygen requires four sequential oxidations; the sequentially oxidized forms of the catalytic site are called the S states. An extrinsic subunit, the manganese-stabilizing protein (MSP), promotes the efficient turnover of the S states. MSP can be removed and rebound to the reaction center; removal and reconstitution is associated with a decrease in and then a restoration of enzymatic activity. We have isotopically edited MSP by uniform 13 C labeling of the Escherichia coli-expressed protein and have obtained the Fourier transform infrared spectrum associated with the S 1 to S 2 transition in the presence either of reconstituted 12 C or 13 C MSP. 13 C labeling of MSP is shown to cause 30 -60 cm ؊1 shifts in a subset of vibrational lines. The derived, isotope-edited vibrational spectrum is consistent with a deprotonation of glutamic/ aspartic acid residues on MSP during the S 1 to S 2 transition; the base, which accepts this proton(s), is not located on MSP. This finding suggests that this subunit plays a role as a stabilizer of a charged transition state and, perhaps, as a general acid/base catalyst of oxygen evolution. These results provide a molecular explanation for known MSP effects on oxygen evolution.In oxygenic photosynthesis, the multi-subunit protein complex, photosystem II (PSII), 1 uses light energy to oxidize water and to form molecular oxygen. Hydrophobic subunits, such as the D1 and D2 proteins, bind most of the prosthetic groups involved in charge separation. Water oxidation occurs at a catalytic site containing four manganese atoms. The catalytic site accumulates the four oxidizing equivalents required for water oxidation. The five sequentially oxidized states of the catalytic site are called the S states. Each oxidation of the catalytic site is associated with the reduction of quinone acceptor molecules, Q A , a single electron acceptor, and then Q B , a two-electron, two-proton acceptor (reviewed in Ref. 1).The 33-kDa, manganese-stabilizing protein (MSP) of PSII plays an important role in water oxidation (reviewed in Ref. 2). As an extrinsic subunit, MSP can be removed from the plant reaction center by several different types of biochemical treatments (3-6). MSP has also been removed by mutagenesis in the cyanobacterium, Synechocystis sp. PCC 6803 (7), and in a green algae, Chlamydomonas reinhardtii (8). In the presence of low concentrations of calcium and chloride, plant MSP was found to be required for photosynthetic oxygen evolution and for maintaining the stability of the manganese cluster (9, 10). In the presence of high concentrations of calcium and chloride, oxygen evolution occurs, but the steady state rate of enzymatic activity is impaired upon removal of MSP (7,9,(11)(12)(13)(14). In addition, removal of MSP and replacement with calcium and chloride result in kinetic inhibition of the S state transitions (12,(15)(16)(17)(18)(19). MSP can be rebound to PSII (20), and this reconstitution reverses ...

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“…17). At neutral pH, theoretical calculations have suggested that groups in the Q B environment are the ones that respond to the formation of Q A Ϫ (18,19). This last hypothesis has not yet been confirmed by experimental data.…”

mentioning

confidence: 96%

Proton uptake by bacterial reaction centers: The protein complex responds in a similar manner to the reduction of either quinone acceptor

Mikšovská

Schiffer

Hanson

et al. 1999

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

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In bacterial photosynthetic reaction centers, the protonation events associated with the different reduction states of the two quinone molecules constitute intrinsic probes of both the electrostatic interactions and the different kinetic events occurring within the protein in response to the light-generated introduction of a charge. The kinetics and stoichiometries of proton uptake on formation of the primary semiquinone Q A ؊ and the secondary acceptor QB ؊ after the first and second flashes have been measured, at pH 7.5, in reaction centers from genetically modified strains and from the wild type. The modified strains are mutated at the L212Glu and͞or at the L213Asp sites near Q B; some of them carry additional mutations distant from the quinone sites (M231Arg 3 Leu, M43Asn 3 Asp, M5Asn 3 Asp) that compensate for the loss of L213Asp. Our data show that the mutations perturb the response of the protein system to the formation of a semiquinone, how distant compensatory mutations can restore the normal response, and the activity of a tyrosine residue (M247Ala 3 Tyr) in increasing and accelerating proton uptake. The data demonstrate a direct correlation between the kinetic events of proton uptake that are observed with the formation of either Q A ؊ or QB ؊ , suggesting that the same residues respond to the generation of either semiquinone species. Therefore, the efficiency of transferring the first proton to Q B is evident from examination of the pattern of H ؉ ͞QA ؊ proton uptake. This delocalized response of the protein complex to the introduction of a charge is coordinated by an interactive network that links the Q ؊ species, polarizable residues, and numerous water molecules that are located in this region of the reaction center structure. This could be a general property of transmembrane redox proteins that couple electron transfer to proton uptake͞release reactions.proton transfer ͉ site-specific mutagenesis ͉ membrane protein ͉ water channel R eaction centers (RCs) from photosynthetic bacteria convert light energy into chemical free energy. These transmembrane complexes are composed of three protein subunits. Two of them, L and M, are fully embedded in the photosynthetic membrane and carry all of the pigments and cofactors present in the RC. The three-dimensional structures of the RCs from two species, Rhodobacter sphaeroides and Rhodopseudomonas viridis, are known at 2.2 Å (1) and 2.0 Å (2) resolution, respectively. The initial capture of energy is achieved through a transmembrane charge separation between the primary electron donor-a bacteriochlorophyll dimer (''P''), situated near the periplasmic side of the protein, and a system of two quinones located near the cytoplasmic side. The primary quinone acceptor, Q A , is bound in a relatively hydrophobic region of the M subunit. The formation of the transient P ϩ Q A Ϫ state occurs by electron transfer from P via H A (an intermediate bacteriopheophytin electron carrier) and is followed by electron donation to Q B , the secondary quinone acceptor. Q A functi...

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Calculated coupling of electron and proton transfer in the photosynthetic reaction center of Rhodopseudomonas viridis

Cited by 190 publications

References 79 publications

Conformational gating of the electron transfer reaction Q _A ⁻ ^⋅ Q _B → Q _A Q _B ⁻ ^⋅ in bacterial reaction centers of Rhodobacter sphaeroides determined by a driving force assay

Conformational gating of the electron transfer reaction Q _A ⁻ ^⋅ Q _B → Q _A Q _B ⁻ ^⋅ in bacterial reaction centers of Rhodobacter sphaeroides determined by a driving force assay

Deprotonation of the 33-kDa, Extrinsic, Manganese-stabilizing Subunit Accompanies Photooxidation of Manganese in Photosystem II

Proton uptake by bacterial reaction centers: The protein complex responds in a similar manner to the reduction of either quinone acceptor

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Calculated coupling of electron and proton transfer in the photosynthetic reaction center of Rhodopseudomonas viridis

Cited by 190 publications

References 79 publications

Conformational gating of the electron transfer reaction Q A − ⋅ Q B → Q A Q B − ⋅ in bacterial reaction centers of Rhodobacter sphaeroides determined by a driving force assay

Conformational gating of the electron transfer reaction Q A − ⋅ Q B → Q A Q B − ⋅ in bacterial reaction centers of Rhodobacter sphaeroides determined by a driving force assay

Deprotonation of the 33-kDa, Extrinsic, Manganese-stabilizing Subunit Accompanies Photooxidation of Manganese in Photosystem II

Proton uptake by bacterial reaction centers: The protein complex responds in a similar manner to the reduction of either quinone acceptor

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Conformational gating of the electron transfer reaction Q _A ⁻ ^⋅ Q _B → Q _A Q _B ⁻ ^⋅ in bacterial reaction centers of Rhodobacter sphaeroides determined by a driving force assay

Conformational gating of the electron transfer reaction Q _A ⁻ ^⋅ Q _B → Q _A Q _B ⁻ ^⋅ in bacterial reaction centers of Rhodobacter sphaeroides determined by a driving force assay