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W2058209257 abstract "The catalytic center (CC) of water oxidation in photosystem II passes through four stepwise increased oxidized states (S0–S4) before O2 evolution takes place from 2H2O in the S4 → S0 transition. The pattern of the release of the four protons from the CC cannot be followed directly in the medium, because proton release from unknown amino acid residues also takes place. However, pH-independent net charge oscillations of 0:0:1:1 in S0:S1:S2:S3 have been considered as an intrinsic indicator for the H+ release from the CC. The net charges have been proposed to be created as the charge difference between electron abstraction and H+release from the CC. Then the H+ release from the CC is 1:0:1:2 for the S0 → S1 → S2 → S3 → S0 transition. Strong support for this conclusion is given in this work with the analysis of the pH-dependent pattern of H+ release in the medium measured directly by a glass electrode between pH 5.5 and 7.2. Improved and crystallizable photosystem II core complexes from the cyanobacterium Synechococcus elongatus were used as material. The pattern can be explained by protons released from the CC with a stoichiometry of 1:0:1:2 and protons from an amino acid group (pK ≈ 5.7) that is deprotonated and reprotonated through electrostatic interaction with the oscillating net charges 0:0:1:1 in S0:S1:S2:S3. Possible water derivatives that circulate through the S states have been named. The catalytic center (CC) of water oxidation in photosystem II passes through four stepwise increased oxidized states (S0–S4) before O2 evolution takes place from 2H2O in the S4 → S0 transition. The pattern of the release of the four protons from the CC cannot be followed directly in the medium, because proton release from unknown amino acid residues also takes place. However, pH-independent net charge oscillations of 0:0:1:1 in S0:S1:S2:S3 have been considered as an intrinsic indicator for the H+ release from the CC. The net charges have been proposed to be created as the charge difference between electron abstraction and H+release from the CC. Then the H+ release from the CC is 1:0:1:2 for the S0 → S1 → S2 → S3 → S0 transition. Strong support for this conclusion is given in this work with the analysis of the pH-dependent pattern of H+ release in the medium measured directly by a glass electrode between pH 5.5 and 7.2. Improved and crystallizable photosystem II core complexes from the cyanobacterium Synechococcus elongatus were used as material. The pattern can be explained by protons released from the CC with a stoichiometry of 1:0:1:2 and protons from an amino acid group (pK ≈ 5.7) that is deprotonated and reprotonated through electrostatic interaction with the oscillating net charges 0:0:1:1 in S0:S1:S2:S3. Possible water derivatives that circulate through the S states have been named. photosystem catalytic center 4-morpholineethanesulfonic acid 4-morpholinepropanesulfonic acid In photosystem (PS)1 II of oxygenic photosynthesis, the primary act starts with an electron transfer from the excited primary donor, chlorophyll a P680 (1Döring R. Renger G. Vater J. Witt H.T. Z. Naturforsch. 1969; 24b: 132-139Google Scholar), located at the inside of the thylakoid membrane, via a pheophytin (2Klimov V.V. Klevanik A.V. Shuvalov V.A. Krasnowsky A.A. FEBS Lett. 1977; 82: 183-186Crossref PubMed Scopus (317) Google Scholar) to the plastoquinone, QA, at the membrane outside (3Stiehl H.H. Witt H.T. Z. Naturforsch. 1968; 23b: 1588-1598Google Scholar). The extremely high positive redox potential of P680+/P680 (≥+1.1 eV) is the driving force for water oxidation. P680+oxidizes tyrosine 161, YZ, located on subunit D1 of PS II (4Debus R.J. Barry B.A. Babcock G.T. McIntosh C. Proc. Natl. Acad. Sci. U. S. A. 1987; 85: 427-430Crossref Scopus (353) Google Scholar). YZ is the immediate electron donor to P680+ (5Gerken S. Brettel K. Schlodder E. Witt H.T. FEBS Lett. 1988; 237: 69-75Crossref Scopus (87) Google Scholar). YZox, in turn, extracts an electron from the water oxidizing complex and catalytic center (CC), respectively (6Blankenship R.E. Babcock G.T. Warden J.T. Sauer K. FEBS Lett. 1975; 51: 287-293Crossref PubMed Scopus (119) Google Scholar). For the oxidation of 2H2O, the CC passes four oxidation states, S0 → S4(7Kok B. Forbush B. McGloin M. Photochem. Photobiol. 1970; 11: 47-475Crossref Scopus (1810) Google Scholar, 8Joliot P. Barbieri G. Chabaud R. Photochem. Photobiol. 1969; 10: 398-429Crossref Scopus (521) Google Scholar) through four turnovers of P680 QA → P680+ QA−. O2evolution takes place in the S4 → S0transition. With regard to the four H+ released from the two H2O in the CC, a pattern of 1:0:1:2 for the S0 → S1 → S2 → S3→ (S4) → S0 transitions has been accepted for many years (9Fowler C.F. Biochim. Biophys. Acta. 1977; 462: 414-421Crossref PubMed Scopus (88) Google Scholar, 10Saphon S. Crofts A. Z. Naturforsch. 1977; 32c: 617Crossref Scopus (96) Google Scholar, 11Förster V. Junge W. Photochem. Photobiol. 1985; 41: 183-190Crossref Scopus (114) Google Scholar). Subsequently, it was shown, however, that the stoichiometry of the protons released into the medium is generally noninteger and depends strongly on the pH, the material, and its preparation (12Rappaport F. Lavergne J. Biochemistry. 1991; 30: 10004-10012Crossref PubMed Scopus (100) Google Scholar, 13Haumann M. Junge W. Biochemistry. 1994; 33: 864-872Crossref PubMed Scopus (116) Google Scholar). It was suggested that this H+ release is a composition of protons released from the CC and protons dissociated from unknown amino acid residues by pK shifts because of electrostatic interaction with the charges of the CC. Therefore, no direct conclusions regarding the pattern of the H+ release from the CC can be drawn from pH measurements in the medium. Junge and co-workers (13Haumann M. Junge W. Biochemistry. 1994; 33: 864-872Crossref PubMed Scopus (116) Google Scholar, 14Bögershausen O. Junge W. Biochim. Biophys. Acta. 1995; 1230: 177-185Crossref Scopus (38) Google Scholar) have shown that in most if not in all S state transitions H+ release into the medium occurs very rapidly from amino acid residues located at the periphery of PS II possibly because of the electrostatic interaction with the charge of the transiently oxidized YZ. 2Oxidized tyrosine is a neutral radical (15Tommos C. Babcock G.T. Biochim. Biophys. Acta. 1999; Google Scholar) but acts as a positive charge by the released phenolic proton, which is reversibly bonded to His190 in its vicinity,i.e. YZox stands for YZ· … H+His190.2Oxidized tyrosine is a neutral radical (15Tommos C. Babcock G.T. Biochim. Biophys. Acta. 1999; Google Scholar) but acts as a positive charge by the released phenolic proton, which is reversibly bonded to His190 in its vicinity,i.e. YZox stands for YZ· … H+His190. It was supposed that in thylakoids 3–5 unknown bases are thereby created. Water oxidation with the release of 4 H+ from 2H2O should occur in the terminal S4 → S0 transition; the protons should be trapped by the bases produced in the S0 → S4 transitions (13Haumann M. Junge W. Biochemistry. 1994; 33: 864-872Crossref PubMed Scopus (116) Google Scholar, 16Haumann M. Junge W. Ort D.R. Yocum C.F. Oxygenic Photosynthesis. Kluwer Academic Publishers, Dordrecht1996: 165-192Google Scholar). On the basis of an extensive biochemical consideration, Babcock and coworkers proposed a mechanism in which the tyrosyl radical abstracts a hydrogen atom from the bound water in each S state transition (see e.g. Ref. 17Hoganson C.W. Babcock G.T. Science. 1997; 277: 1953-1956Crossref PubMed Scopus (519) Google Scholar). The preceding oxidation of YZ through P680+ should be accompanied by one H+ release into the medium. This would correspond to a H+stoichiometry of 1:1:1:1. A different model has been developed since 1984 based on an observed period of four oscillation of net charges in the CC (18Saygin Ö. Witt H.T. FEBS Lett. 1984; 176: 83-87Crossref Scopus (38) Google Scholar, 19Saygin Ö. Witt H.T. FEBS Lett. 1985; 187: 224-226Crossref Scopus (54) Google Scholar, 20Brettel K. Schlodder E. Witt H.T. Biochim. Biophys. Acta. 1984; 766: 403-415Crossref Scopus (197) Google Scholar, 21Kretschmann H. Schlodder E. Witt H.T. Biochim. Biophys. Acta. 1996; 1274: 1-8Crossref Scopus (29) Google Scholar). The latter was concluded from two independent experiments: (i) In the S state cycle of water oxidation, a local stable electric field was observed by electrochromic band shifts (18Saygin Ö. Witt H.T. FEBS Lett. 1984; 176: 83-87Crossref Scopus (38) Google Scholar, 19Saygin Ö. Witt H.T. FEBS Lett. 1985; 187: 224-226Crossref Scopus (54) Google Scholar). It was attributed to a positive net charge of the CC in S2 and S3 relative to S0 and S1. (ii) The net charge was also monitored by the strongly retarded reduction kinetics of the oxidized primary electron donor, P680+, in the S states S2 and S3 (20Brettel K. Schlodder E. Witt H.T. Biochim. Biophys. Acta. 1984; 766: 403-415Crossref Scopus (197) Google Scholar). It was shown that the net charge oscillation 0:0:1:1 in S0:S1:S2:S3 is pH-independent between pH 5.5 and 7 (21Kretschmann H. Schlodder E. Witt H.T. Biochim. Biophys. Acta. 1996; 1274: 1-8Crossref Scopus (29) Google Scholar). This pH independence was measured also for the oxidation of the CC followed at 365 nm and attributed to manganese oxidation (21Kretschmann H. Schlodder E. Witt H.T. Biochim. Biophys. Acta. 1996; 1274: 1-8Crossref Scopus (29) Google Scholar) as well as for the O2 evolution (22Meyer B. Schlodder E. Dekker J.P. Witt H.T. Biochim. Biophys. Acta. 1989; 974: 36-43Crossref Scopus (84) Google Scholar). It was proposed that the net charge is created as the charge difference between electron abstraction and intrinsic proton release from the CC. From this it follows that the pH-independent H+ release from the CC is 1:0:1:2 coupled with the S0 → S1 → S2 → S3 → (S4) → S0 transitions (18Saygin Ö. Witt H.T. FEBS Lett. 1984; 176: 83-87Crossref Scopus (38) Google Scholar, 19Saygin Ö. Witt H.T. FEBS Lett. 1985; 187: 224-226Crossref Scopus (54) Google Scholar, 20Brettel K. Schlodder E. Witt H.T. Biochim. Biophys. Acta. 1984; 766: 403-415Crossref Scopus (197) Google Scholar, 21Kretschmann H. Schlodder E. Witt H.T. Biochim. Biophys. Acta. 1996; 1274: 1-8Crossref Scopus (29) Google Scholar). This stoichiometry differs from the measurements and conclusions outlined in Ref. 12Rappaport F. Lavergne J. Biochemistry. 1991; 30: 10004-10012Crossref PubMed Scopus (100) Google Scholar, 13Haumann M. Junge W. Biochemistry. 1994; 33: 864-872Crossref PubMed Scopus (116) Google Scholar, 14Bögershausen O. Junge W. Biochim. Biophys. Acta. 1995; 1230: 177-185Crossref Scopus (38) Google Scholar (see above). This may be due to the varying features of the materials investigated. In Ref. 16Haumann M. Junge W. Ort D.R. Yocum C.F. Oxygenic Photosynthesis. Kluwer Academic Publishers, Dordrecht1996: 165-192Google Scholar, it was reported on thylakoids, PS II-enriched membrane fragments, and PS II core particles from plant material. We used PS II core complexes from cyanobacteria. Our material, provided to Junge's laboratory, was analyzed with the pH-indicating dye technique. The observed pattern of the H+ release in the medium (listed in Ref. 21Kretschmann H. Schlodder E. Witt H.T. Biochim. Biophys. Acta. 1996; 1274: 1-8Crossref Scopus (29) Google Scholar with the author's kind permission) showed between pH 5 and 7 principal differences compared with that which they measured with their PS II core complexes (14Bögershausen O. Junge W. Biochim. Biophys. Acta. 1995; 1230: 177-185Crossref Scopus (38) Google Scholar) and thylakoids from pea (13Haumann M. Junge W. Biochemistry. 1994; 33: 864-872Crossref PubMed Scopus (116) Google Scholar). We have explained in Ref. 21Kretschmann H. Schlodder E. Witt H.T. Biochim. Biophys. Acta. 1996; 1274: 1-8Crossref Scopus (29) Google Scholar that the H+ pattern of our material would be in moderate agreement with the 1:0:1:2 proton release from the CC and protons from an acid group (pK ≈ 6), which is deprotonated and reprotonated by electrostatic interaction with the oscillating net charge 0:0:1:1 of the CC. In this work, we give evidence for this prediction. (i) The H+ release into the medium was directly followed by pH measurements with a sensitive glass electrode. This technique was used to prevent problems coupled with the use of pH-indicating dyes in biological systems (see Experimental Procedure). (ii) We used improved purified PS II core complexes from cyanobacteriaSynechococcus elongatus which are highly active in O2 evolution and crystallizable (23Zouni A. Lüneberg C. Fromme P. Schubert W.D. Saenger W. Witt H.T. Garab G. Photosynthesis: Mechanism and Effects. Kluwer Academic Publishers, Dordrecht1998: 925-928Google Scholar). (iii) The discrepancy between the results obtained with the PS II material of cyanobacteria and the results measured in different materials from plants are discussed. (iv) Possible water derivatives that circulate through the S states have been named. Oxygen-evolving PS II core complexes were prepared from the cyanobacterium S. elongatus according to Refs. 23Zouni A. Lüneberg C. Fromme P. Schubert W.D. Saenger W. Witt H.T. Garab G. Photosynthesis: Mechanism and Effects. Kluwer Academic Publishers, Dordrecht1998: 925-928Google Scholar and 24Dekker J.P. Boekema E.J. Witt H.T. Rögner M. Biochim. Biophys. Acta. 1988; 936: 307-318Crossref Scopus (84) Google Scholar. The PS II complexes were characterized by about 55 Chl/QAand 66 Chl/¼ O2 estimated from the amount of photo-reducible QA and O2 per flash and chlorophyll. Flash-induced changes in pH because of proton release were measured with a light-insensitive glass electrode of the flat membrane type (SA 9218/2.N from Schott). The reference electrode (B 2830 from Schott) was separated from the reaction medium by an electrolyte bridge filled with the reaction medium. A pH meter (model 645 from Knick) was used to read out the pH-dependent voltage. After compensation of the steady-state level by a constant offset voltage, the output signals were further amplified, filtered by a low pass filter (Dual Hi/Lo Filter model 452 from Wavetek Rockland) and digitized by a storage oscilloscope (Nicolet 1090A). The reaction medium contained 0.5 mm buffer (at pH 5.5 and 6.0, MES and at pH 7.2 and 7.0, MOPS), 100 mm KCl, 10 mmMgCl2, 10 mm CaCl2, 0.02%n-dodecyl-β,d-maltoside, 100 μm2,5 dichloro-p-benzoquinone, 1 mmK3[Fe(CN)6], and PS II complexes equivalent to 20–30 μm chlorophyll a. For measurements 3 ml of the reaction medium were filled into the reaction vessel (diameter, 3 cm) and stirred at 17 °C. The dark-adapted samples were illuminated through the vessel bottom with saturating xenon flashes (pulse duration, 15 μs) filtered by a colored glass (RG610 from Schott). The dark time between flashes in each series of flashes was 1 s. For each flash series with a different number of flashes we used a fresh sample. The difference between the proton release after i and i + 1 flashes was calculated to obtain the proton release induced by the ith flash. Calibration of the proton release was achieved by addition of 5 μl of 1 mm HCl to the medium. The use of a sensitive pH glass electrode to measure pH changes offers the following advantages compared with pH-indicating dye techniques: (i) Excitation of the sample by measuring light that is necessary to follow pH-indicating absorption changes is excluded by glass electrode measurements performed in the dark. (ii) The interpretation of pH-indicating absorption changes is complicated in a suspension of biological particles. The response may depend on the partition of the dye in the different phases (aqueous and hydrophobic regions and their interfaces). The meaning of a multiphasic response has led to controversial conclusions (25Jahns P. Lavergne J. Rappaport F. Junge W. Biochim. Biophys. Acta. 1991; 1057: 313-319Crossref Scopus (37) Google Scholar). The proton release measured in dependence on the flash number is not correlated directly to the individual S state transitions. Therefore the experimental pattern of proton release was deconvoluted with the Kok parameters (So/S1 ratio of dark-adapted samples, misses and double hits) to obtain the amount of protons released on every S state transition. Fig. 1 shows the time course of pH changes measured with a glass electrode after excitation of dark-adapted PS II core complexes from Synechococcus at pH 6 with one, two, three, and four flashes. The kinetics of the proton release were determined by the instrumental response time of ∼10 s. Dichloro-p-benzoquinone (100 μm) and K3[Fe(CN)6] (1 mm) were used as electron acceptors (see “Experimental Procedures”). Measurements without ferricyanide show the uptake of about 1 proton/flash and PS II in addition to the proton release at the donor side of PS II (not shown). This result gives evidence that ferricyanide oxidizes the reduced dichloro-p-benzoquinone acceptor fast enough to prevent a proton uptake by reduced dichloro-p-benzoquinone at the acceptor side of PS II. Without any electron acceptor the pH change induced by the first flash was below the detection limit, and the signal amplitude induced by 100 flashes was less than 1% of the control. To obtain the proton release induced by the nth flash, the difference between the proton release after n andn − 1 flashes was calculated. Fig.2 shows the extent of the proton release as a function of the flash number for pH 5.5, 6.0, 7.0, and 7.2 normalized to the average proton yield of flashes 1–9. The measured patterns (see data points in Fig. 2) were fitted (seesolid lines in Fig. 2) according to the Kok parameters with 25% S0 and 75% S1 in the dark-adapted state, 10% misses, 7% double hits, as well as, with proton release stoichiometries for the S0 → S1 → S2 → S3 → S0 transitions as indicated in the legend of Fig. 2. The proton release evaluated for the four S state transitions (Fig. 2) is depicted in Fig.3 (see data points) as function of pH.Figure 2Proton release per PS II into the medium measured with a glass electrode at pH 5.5, 6.0, 7.0, and 7.2 as a function of the flash number. The curves are calculated with the Kok parameters 25% S0 and 75% S1 in the dark-adapted state, 10% misses, and 7% double hits and the following proton stoichiometries for the S0 → S1 → S2 → S3 → S0transitions 1.0:0.0:1.0:2.0 at pH 7 and 7.2, 1.0:0.2:1.0:1.8 at pH 6.0, and 1.0:0.8:1.0:1.2 at pH 5.5.View Large Image Figure ViewerDownload Hi-res image Download (PPT)Figure 3Proton release per PS II into the medium at the indicated S state transitions as a function of pH. Thethree curves are calculated ones assuming the presence of a deprotonable acid group AH with pK ≈ 5.7 and a pH-independent 1:0:1:2 proton release from the CC as predicted from the net charge oscillation 0:0:1:1 (18Saygin Ö. Witt H.T. FEBS Lett. 1984; 176: 83-87Crossref Scopus (38) Google Scholar, 19Saygin Ö. Witt H.T. FEBS Lett. 1985; 187: 224-226Crossref Scopus (54) Google Scholar, 20Brettel K. Schlodder E. Witt H.T. Biochim. Biophys. Acta. 1984; 766: 403-415Crossref Scopus (197) Google Scholar). The data points are based on the measurements shown in Fig. 2.View Large Image Figure ViewerDownload Hi-res image Download (PPT) In Ref. 21Kretschmann H. Schlodder E. Witt H.T. Biochim. Biophys. Acta. 1996; 1274: 1-8Crossref Scopus (29) Google Scholar and in the introduction it was outlined that the pH-independent H+ release 1:0:1:2 from the CC concluded from the net charge oscillation 0:0:1:1 is modified by protons dissociated from amino acid groups to a pH-dependent H+ release into the medium. The electrostatic interaction between the net charge in S2 and an amino acid residue, AH, might result in a stable base, A−, and a proton release into the medium. If one AH exists per PS II, then m in mAH indicates the fraction of AH that is in the protonated state in S0(Scheme FS1). The base, mA−, is reprotonated when the net charge disappears in S3 → (S4) → S0 through the release of two H+ from the CC. Therefore, the H+ release in S3 → (S4) → S0 is (2 − m), and in the S0 → S1 → S2 → S3 → (S4) → S0 transitions 1:m:1:(2 − m) (for nBH in Scheme FS1; see legend). In cyanobacteria and PS II-enriched membrane fragments from spinach an amino acid residue with a pK between 5.3 and 6.0 has been discussed (22Meyer B. Schlodder E. Dekker J.P. Witt H.T. Biochim. Biophys. Acta. 1989; 974: 36-43Crossref Scopus (84) Google Scholar, 26Vaas I. Styring S. Biochemistry. 1991; 30: 830-839Crossref PubMed Scopus (271) Google Scholar). For an optimal fit of the data in Fig. 3, we have to assume in the following a reactive acid group, AH, with an apparent pK ≈ 5.7 and a positive net charge in S2 inducing a pK shift that would release all mH+ from mAH in the considered pH 5.5–7.2 range. This is the case if a ΔpK ≥ 2 is induced. Neglecting secondary effects, ΔpK ≥ 2 is consistent with the result of a simple calculation in which the reasonable values of ε ≈ 10 and d ≈ 12 Å are assumed for the unknown dielectric constant ε and distance d between the net charge and the acid. For a weak acid it is log (1 − m)/m = pH − pK. With this relation and a pH-independent 1:0:1:2 proton release from the CC as concluded from the net charge oscillation 0:0:1:1, it results a stoichiometry of the H+ being released into the medium between pH 5 and pH 7 as shown by the three curves in Fig.3. This calculation fairly agrees with the glass electrode measurements in the medium (data points in Fig. 3). This agreement supports the assumption made in the calculation, especially the prediction that the pH-independent H+ release from the CC is 1:0:1:2. The stoichiometry of the proton release into the medium at pH 7.0 and 7.2 is identical to the predicted H+ release from the CC, because at this pH the acid mAH is practically deprotonated and cannot contribute to the proton release into the medium. The possible pathways of the protons released from the CC and mAH are depicted in Scheme FS1. The evaluated stoichiometry of the proton release from the CC may be a basis for obtaining information about the possible water derivatives in the different S states. In this regard, we have to take into account that the light-induced S0 → S4 state cycling can be turned backwards in the dark with reducing agents such as hydroxylamine NH2OH (27Bouges B. Biochim. Biophys. Acta. 1971; 234: 103-112Crossref PubMed Scopus (85) Google Scholar). We have shown that with NH2OH S0 can be reversibly overreduced by one electron into a state S−1 identified by a corresponding overreduced manganese state (28Saygin Ö. Witt H.T. Photobiochem. Photobiophys. 1985; 10: 71-82Google Scholar). In addition, we observed a local electrochromic absorption change and net charge, respectively, in state S−1 (28Saygin Ö. Witt H.T. Photobiochem. Photobiophys. 1985; 10: 71-82Google Scholar) (Table I). These results were supported in Ref. 29Kretschmann H. Pauly S. Witt H.T. Biochim. Biophys. Acta. 1991; 1059: 208-214Crossref Scopus (18) Google Scholar and extended in Ref. 30Kretschmann H. Witt H.T. Biochim. Biophys. Acta. 1993; 1144: 331-345Crossref Scopus (26) Google Scholar. In the light-induced forward S−1 → S0 transition, the net charge disappears. This is only possible when in S−1 → S0, together with the electron abstraction, two H+ are released from the CC. Then in toto four H+ are released between S−1 and S3. With the assumption that reversibly bound water within the CC is the source of these protons, this is possible if S−1 contains 2H2O. With this “calibration” the possible water derivatives in the native S states should be those depicted in Table I and Scheme FS1. Because S3 does not contain any more water protons, the S3 → S4transition is not accompanied by a proton release from the CC. Therefore, in this transition a second net charge is created in state S4. From the conclusion that 2OH− is the substrate in state S0 it follows that in the S4→ S0 transition 2H2O (not 2OH−) are taken up with the subsequent release of two protons.Table IPossible derivatives of water in the S−1 to S4states‖S−1⊕‖2H2O‖→−e−2H+‖S0‖2OH−‖→−e−H+‖S1‖OH−/O=‖→−e‖‖S2⊕‖OH−/O=‖→−e−H+S3⊕‖2O=‖→−e|‖S4⊕⊕‖2O=‖→+2H2O−02,−2H+‖S0‖2OH− Open table in a new tab Because manganese oxidation probably takes place in each S state up to state S3 (see below) and YZox is proposed to be the fourth oxidized state in S4 (see below), it follows that water is oxidized only in the S4 → S0 transition. The complete proton depletion from water prior to the S4 → S0 transition (Table I and Scheme FS1) is in line with an energetic consideration, showing that deprotonated water is possibly the most favorable state for oxidation (31Brudvig G.W. de Paula J.C. Progress in Photosynthesis Research. 1987; I (Biggins, J., ed.) I.5.491, Martinus Nijhoff Publishers, Dordrecht: 491-498Google Scholar). In Ref. 32Messinger J. Bader M. Wydrzynski T. Proc. Natl. Acad. Sci. U. S. A. 1995; 92: 3209-3213Crossref PubMed Scopus (223) Google Scholar, a slow and a fast exchanging water derivative was measured in the S3state, a result that may exclude symmetric water ligands in S3, e.g. as predicted in Schemes FS1 and FS2. But, if YZox represents the fourth oxidizing equivalent (see below), YZ is possibly in the vicinity of only one of the two active Mn4+ = O couples. Because the other ligands of the two manganeses may be also different, this could account for different exchange rates. Different limiting water channels between the two manganese sites and the solvent phase could also be responsible for the biphasic behavior (33Hillier W. Mesinger J. Wydrzynski T. Garab G. Photosynthesis: Mechanism and Effects. Kluwer Academic Publishers, Dordrecht1998: 1307-1310Google Scholar).Figure FS2Model of the period four oscillation of manganese oxidation, net charge formation, and water deprotonation. The S state cycle S0 → S4 is driven by quaternary, light-induced transmembrane electron transfers from P680 to QA. P680+oxidizes step by step via tyrosine YZ, a manganese dimer up to S3. The oxidized YZ has been hypothesized in Ref. 35Saygin Ö. Witt H.T. Biochim. Biophys. Acta. 1987; 893: 452-469Crossref Scopus (64) Google Scholar to be the fourth oxidizing equivalent in S4 that triggers the electron transfer from the two oxo-atoms to the four oxidizing equivalents by its electric field. For clarity the charges of the water derivatives (Scheme FS1) have been omitted.View Large Image Figure ViewerDownload Hi-res image Download (PPT) With regard to the oxidized equivalents in the different S states, these have been analyzed by UV absorption changes attributed to oxidation of manganeses (34Dekker J.P. van Gorkom H. Wensink J. Ouwehand L. Biochim. Biophys. Acta. 1984; 767: 1-9Crossref Scopus (144) Google Scholar). Manganese oxidation states derived from our measurements in the UV are depicted in Scheme FS2. These were obtained inter alia under improved conditions in which the S state sequences from S0 up to S3 were before the opposite reaction S3 → S0 (35Saygin Ö. Witt H.T. Biochim. Biophys. Acta. 1987; 893: 452-469Crossref Scopus (64) Google Scholar, 36Kretschmann H. Dekker J.P. Saygin Ö. Witt H.T. Biochim. Biophys. Acta. 1988; 932: 358-361Crossref Scopus (22) Google Scholar). Only a manganese dimer was considered to be functional. The mixed valence states in S0 and S2 (spin = ½) are in agreement with an EPR multiline signal in S0 (41Messinger J. Robblee J, Yu, W.O. Sauer K. Yachandra V.K. Klein M.P. J. Am. Chem. Soc. 1997; 119: 11349-11350Crossref PubMed Scopus (150) Google Scholar,42Ahrling K.A. Peterson S. Styring S. Biochemistry. 1997; 36: 13148-13152Crossref PubMed Scopus (152) Google Scholar) and S2 (43Dismukes G.C. Photochem. Photobiol. 1986; 43: 99-115Crossref Scopus (252) Google Scholar). Valence states of the manganeses have also been derived from x-ray absorption shifts at the manganese-K-edge (37Klein M.P. Sauer K. Yachandra V.K. Photosynth. Res. 1993; 38: 265-277Crossref PubMed Scopus (46) Google Scholar, 38Kusunoki M. Ono T. Noguchi T. Inoue Y. Oyanagi H. Photosynth. Res. 1993; 38: 331-339Crossref PubMed Scopus (22) Google Scholar, 39Iuzzolino L. Dittmer J. Dörner W. Meyer-Klaucke W. Dau H. Biochemistry. 1998; 37: 17112-17119Crossref PubMed Scopus (175) Google Scholar, 40Dau H. Iuzzolino L. Dittmer J. Dörner W. Meyer-Klaucke W. Garab G. Photosynthesis: Mechanism and Effects. Kluwer Academic Publishers, Dordrecht1998Google Scholar) indicating manganese oxidations up to S3. In Ref.37Klein M.P. Sauer K. Yachandra V.K. Photosynth. Res. 1993; 38: 265-277Crossref PubMed Scopus (46) Google Scholar a manganese oxidation has, however, not been observed in the S2 → S3 transition. With respect to the S3 → S4 transition, a signal indicating the creation of a fourth oxidizing equivalent has not been found by any of the methods. We have proposed in Ref. 35Saygin Ö. Witt H.T. Biochim. Biophys. Acta. 1987; 893: 452-469Crossref Scopus (64) Google Scholar that the immediate electron donor to P680+, i.e. oxidized tyrosine YZox itself, represents the fourth oxidizing equivalent, i.e. S4 ≡ YZox · S3. The oxidation of YZ in S3 → S4 was shown to take place biphasically with 50 and 260 ns (20Brettel K. Schlodder E. Witt H.T. Biochim. Biophys. Acta. 1984; 766: 403-415Crossref Scopus (197) Google Scholar). From this follows that the transition S3 → S4 should take place within this time (Schemes FS1 and FS2). We have outlined that in S4 the electrostatic field of YZox is the actual promoter giving rise to a two-electron transfer from the two oxo-atoms O2− to the active Mn4+ ions resulting in a peroxo-intermediate Mn3+-O-O-Mn3+. In a further two-electron oxidation, this may be followed by the O2 evolution within milliseconds, coupled with the formation of YZ and Mn2+-Mn3+, uptake of 2H2O, and the subsequent release of 2 H+ (35Saygin Ö. Witt H.T. Biochim. Biophys. Acta. 1987; 893: 452-469Crossref Scopus (64) Google Scholar). The function of YZox as electrostatical promoter in S4 has recently also been discussed in Ref. 44Ahlbrink R. Haumann M. Cherepanov D. Bögershausen O. Mulkidjanian A. Junge W. Biochemistry. 1998; 37: 1131-1142Crossref PubMed Scopus (163) Google Scholar. For the clarification of the mechanism of water cleavage, straightforward measurement of protons released from the CC into the medium is not possible because protons released from amino acid residues are superimposed. H+ release from these residues is induced by electrostatic interaction between the charges in the CC and amino acid groups. In the medium very different proton stoichiometries were observed, depending on the material (thylakoids, PS II-enriched membrane fragments, and PS II core complexes) and its isolation procedure (12Rappaport F. Lavergne J. Biochemistry. 1991; 30: 10004-10012Crossref PubMed Scopus (100) Google Scholar, 13Haumann M. Junge W. Biochemistry. 1994; 33: 864-872Crossref PubMed Scopus (116) Google Scholar, 14Bögershausen O. Junge W. Biochim. Biophys. Acta. 1995; 1230: 177-185Crossref Scopus (38) Google Scholar, 16Haumann M. Junge W. Ort D.R. Yocum C.F. Oxygenic Photosynthesis. Kluwer Academic Publishers, Dordrecht1996: 165-192Google Scholar). This indicates that at least part of such proton dissociation cannot have a function in connection with the events leading to water oxidation. The treatments during isolation and purification of the material may induce increased contact of hydrophobic protein domains with water and partial protein unfolding. This may be coupled with a decrease of pK values of otherwise “silent” acids, whereby these become deprotonatable. The H+ release relevant to the water oxidation may be masked by interference with such nonspecific protolytic reactions. These reasons may also account for the nonoscillating proton release observed with PS II core complexes from plants (14Bögershausen O. Junge W. Biochim. Biophys. Acta. 1995; 1230: 177-185Crossref Scopus (38) Google Scholar), because addition of glycerol, known as an agent inducing refolding and stabilizing the native protein structure (45Timasheff S.N. Arakwa T. Creighton T.E. Protein Structure. Oxford University Press, Oxford1990: 331-345Google Scholar), can in part restore the oscillation in these core complexes as shown in (46Haumann M. Hundelt M. Jahns P. Chroni S. Bögershausen O. Ghanotakis D. Junge W. FEBS Lett. 1997; 410: 143-248Crossref Scopus (37) Google Scholar). In this work, however, we used PS II core complexes from cyanobacteria that are crystallizable. This feature indicates that unfolded protein domains or other defects of the protein matrix are most likely negligible because otherwise with this material crystallization would not be possible. This conclusion is consistent with the observation that added glycerol has no effect on the H+ pattern of our PS II core complexes between pH 5 and 7 (not shown). Regarding the oscillating H+ release in thylakoids coupled with the S state transition (13Haumann M. Junge W. Biochemistry. 1994; 33: 864-872Crossref PubMed Scopus (116) Google Scholar), its pH dependence strongly deviates from that of our PS II core complexes shown in Fig. 3. (Recently, stoichiometries for thylakoids were reported in Ref. 46Haumann M. Hundelt M. Jahns P. Chroni S. Bögershausen O. Ghanotakis D. Junge W. FEBS Lett. 1997; 410: 143-248Crossref Scopus (37) Google Scholar that are different from the results detailed in Ref. 13Haumann M. Junge W. Biochemistry. 1994; 33: 864-872Crossref PubMed Scopus (116) Google Scholar.) From the variable extent and kinetics of the proton release at pH 6.5 and 7.5, it was concluded in (13Haumann M. Junge W. Biochemistry. 1994; 33: 864-872Crossref PubMed Scopus (116) Google Scholar) that 3–5 bases are created by deprotonation of different amino acid residues in the transitions from So→ S4. The bases have been supposed to trap the 4 H+ suggested to be released upon oxidation of 2H2O in the terminal S4 → S0transition (13Haumann M. Junge W. Biochemistry. 1994; 33: 864-872Crossref PubMed Scopus (116) Google Scholar, 16Haumann M. Junge W. Ort D.R. Yocum C.F. Oxygenic Photosynthesis. Kluwer Academic Publishers, Dordrecht1996: 165-192Google Scholar). This concept is, however, not consistent with the two results discussed in this work: (i) Here, the proton release of PS II complexes from cyanobacteria measured in the medium with a glass electrode can be simulated satisfactorily with the assumption of only one deprotonatable acid group AH (pK ≈ 5.7) and a pH-independent 1:0:1:2 proton release from the CC (Fig. 3). (ii) The result is in agreement with the net charge oscillation of 0:0:1:1 in S0:S1:S2:S3 (18Saygin Ö. Witt H.T. FEBS Lett. 1984; 176: 83-87Crossref Scopus (38) Google Scholar, 19Saygin Ö. Witt H.T. FEBS Lett. 1985; 187: 224-226Crossref Scopus (54) Google Scholar, 20Brettel K. Schlodder E. Witt H.T. Biochim. Biophys. Acta. 1984; 766: 403-415Crossref Scopus (197) Google Scholar). This observation was explained by a H+ release from the CC with a stoichiometry of 1:0:1:2. This consistently supports the conclusion drawn from the proton measurement in the medium. We are very grateful to Prof. B. Rumberg for providing us with the sensitive electrode equipment for proton measurements and for his critical comments. We thank M. Çetin, D. DiFiore, and H. Schmidt very much for excellent biochemical assistance." @default.
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W2058209257 title "Stoichiometry of Proton Release from the Catalytic Center in Photosynthetic Water Oxidation" @default.
W2058209257 cites W1518076846 @default.
W2058209257 cites W1963482869 @default.
W2058209257 cites W1967419755 @default.
W2058209257 cites W1972259729 @default.
W2058209257 cites W1995020775 @default.
W2058209257 cites W1995475333 @default.
W2058209257 cites W1995994720 @default.
W2058209257 cites W1999096297 @default.
W2058209257 cites W2000605698 @default.
W2058209257 cites W2001131145 @default.
W2058209257 cites W2001779952 @default.
W2058209257 cites W2001873677 @default.
W2058209257 cites W2008126782 @default.
W2058209257 cites W2011333654 @default.
W2058209257 cites W2016156461 @default.
W2058209257 cites W2026940293 @default.
W2058209257 cites W2044105506 @default.
W2058209257 cites W2045622515 @default.
W2058209257 cites W2048879936 @default.
W2058209257 cites W2051638155 @default.
W2058209257 cites W2055744837 @default.
W2058209257 cites W2062808472 @default.
W2058209257 cites W2066652100 @default.
W2058209257 cites W2067783680 @default.
W2058209257 cites W2069702639 @default.
W2058209257 cites W2070766739 @default.
W2058209257 cites W2071258949 @default.
W2058209257 cites W2073305160 @default.
W2058209257 cites W2075567202 @default.
W2058209257 cites W2079632413 @default.
W2058209257 cites W2082579379 @default.
W2058209257 cites W2085602613 @default.
W2058209257 cites W2096781815 @default.
W2058209257 cites W2098472363 @default.
W2058209257 cites W2149377812 @default.
W2058209257 cites W2235196671 @default.
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