Abstract
Photosystem II (PSII) of the photosynthetic apparatus in oxygenic organisms contains a catalytic center that performs one of the most important reactions in bioenergetics: light-dependent water oxidation to molecular oxygen. The catalytic center is a Mn4CaO5 cluster consisting of four cations of manganese and one calcium cation linked by oxygen bridges. The authors reported earlier that a structural transition occurs at pH 5.7 in the cluster resulting in changes in manganese cation(s) redox potential and elevation of the Mn‑clus-ter resistance to reducing agents. The discovered effect was examined in a series of investigations that are reviewed in this work. It was found that, at pH 5.7, Fe(II) cations replace not two manganese cations as it happens at pH 6.5 but only one cation; as a result, a chimeric Mn3Fe1 cluster is produced. In the presence of exogenous calcium ions, membrane preparations of PSII with such a chimeric cluster are capable of evolving oxygen in the light (at a rate of approximately 25% of the rate in native PSII). It was found that photoinhibition that greatly depends on the processes of oxidation or reduction at pH 5.7 slows down as compared with pH 6.5. PSII preparations were also more resistant to thermal inactivation at pH 5.7 than at pH 6.5. However, in PSII preparations lacking manganese cations in the oxygen-evolving complex, the rates of photoinhibition at pH 6.5 and 5.7 did not differ. In thylakoid membranes, protonophores that abolish the proton gradient and increase pH in the lumen (where the manganese cluster is located) from 5.7 to 7.0 considerably elevated the rate of PSII photoinhibition. It is assumed that the structural transition in the Mn-cluster at pH 5.7 is involved in the mechanisms of PSII defense against photoinhibition.
Avoid common mistakes on your manuscript.
INTRODUCTION
A major basic process called photosynthesis occurs in oxygenic organisms (higher plants, algae, and cyanobacteria) in the photosynthetic apparatus whose main components are photosystem II (PSII) and photosystem I (PSI). PSII contains a unique catalytic center responsible for light-dependent oxidation of two water molecules and formation of a linkage between two remaining atoms of oxygen. This is associated with the liberation of electrons and protons necessary for photosynthesis. Produced molecular oxygen is released to the atmosphere as a by-product. This reaction is essentially the sole source of oxygen on our planet.
The catalytic center that oxidizes water consists of four cations of manganese and one calcium cation linked by oxygen bridges (Mn4CaO5). In 2011, Umena et al. determined the structure of the catalytic center at a resolution of 1.9 Å by means of X-ray structure analysis [1]. This structure is shown in Fig. 1. It is an irregular cube formed by one calcium cation, three manganese cations, and four oxygen atoms. The fourth cation of manganese is located at a distance from the cube but is connected to it. The detached cation of manganese and the cation of calcium have two molecules of water each as ligands. At present, it is not known whether these molecules are substrate water or not. A certain drawback of this work was the risk of manganese cations’ reduction by X-rays in the course of the experiment, which could disturb the accuracy of measuring distances between the components of a cluster. This problem was later solved by means of a laser generating femtosecond X-ray pulses [2]. However, in spite of the fact that the structure of the catalytic center is currently known, the mechanism of molecular oxygen synthesis by this center remains obscure.
Functional activity and characteristics of the manganese-calcium catalytic center considerably depend on surrounding pH, which may be associated with the process of protonation or deprotonation of not only amino acid residues but also of oxygen bridges, some of which (for instance, O5 bridge) may directly participate in the formation of molecular oxygen [3]. In this review, we are going to present the results of our investigation into the effect of protonation or deprotonation on the properties of the catalytic center responsible for water oxidation in PSII. We have shown that, at pH 5.7, the redox potential of one of the manganese ions belonging to the oxygen-evolving complex (OEC) of PSII considerably decreased. This process results in improvement of resistance of this manganese cation to endogenous and exogenous reducing agents. Using the discovered effect, we have worked out a method of producing PSII membrane preparations with a chimeric catalytic center in OEC consisting of three cations of manganese and one cation of iron and capable of evolving molecular oxygen as a result of water oxidation at the efficiency of 25% of native PSII preparation [4]. The obtained results may be useful for development of water photolysis artificial systems as generators of molecular oxygen and hydrogen. In the course of investigating the mechanism of photoinhibition, we revealed a relationship between pH-dependent structural transition in OEC at pH 5.7 and resistance to photoinhibition. This relationship is a novel and earlier unknown mechanism of photosynthetic apparatus self-defense against photoinhibition in oxygenic organisms. As photoinhibition strongly influences the gross yield of photosynthesis, we expect that further investigation of this effect will be of great practical and theoretical importance.
рН DEPENDENCE OF PSII FUNCTIONAL ACTIVITY
The rate of molecular oxygen generation by PSII OEC in oxygenic photosynthesizing organisms greatly depends on surrounding pH. Oxygen-evolving activity of PSII membrane preparations is described by a bell-shaped curve with a peak at pH 6.2–6.8 and descending legs corresponding to 50% inhibition at pH 4.8−5.7 and pH 7.3−7.5 [5–11]. The mechanism of pH-dependent inactivation of PSII is still poorly understood. Inhibition of OEC in the alkaline region is at least partially accounted for by the extraction of Сl– anion therefrom [8]. In the acidic pH region, inactivation of OEC largely depends on dissociation of extrinsic proteins. PsbP, PsbQ, and PsbO extrinsic proteins have pKs (50% dissociation) of 5.0, 4.1, and 3.6, respectively [12]. pH-dependent extraction of PsbP and PsbQ proteins is accompanied by loss of Са2+ from OEC, which results in inhibition of water oxidation [13]. A rise in proton concentration in the medium also exerts an influence on the manganese cluster of OEC, including S-transitions in the catalytic cycle. Bernát et al. and Suzuki et al. showed essentially identical results with PSII preparations isolated from spinach [14] and thermophilic cyanobacteria Thermosynechoccocus elongatus [15]. The conducted experiments showed that, in spinach OEC, S1 → S2 transition does not depend on pH in the range of 4.1−8.4, whereas S2 → S3, S3 → [S4] → S0, and S0 → S1 transitions have pKs of 4.0, 4.5, and 4.7, respectively [14].
рН DEPENDENCE OF RESISTANCE OF MANGANESE CATIONS IN OEC TO EXOGENOUS REDUCTANTS
It is known that exogenous reductants with a small molecule, such as hydroxylamine (NH2OH), hydrazine (NH2NH2), and hydrogen peroxide (Н2О2), can reduce manganese cations in OEC of intact PSII [16]. Reducing agents with bigger molecules, such as hydroquinone and benzidine, can also reduce manganese cations but only in PSII preparations where the Mn4CaO5 cluster is not protected by extrinsic proteins PsbP and PsbQ [16]. The latter type of PSII preparation (PSII(-Са)) is produced by means of PSII treatment with a concentrated NaCl solution (2 М); as a result, PSII loses not only two extrinsic proteins PsbP and PsbQ but also a calcium cation from OEC [17]. Manganese cations (Mn(II)) reduced by exogenous agents leave binding sites. This reaction is often used for extraction of manganese cations from PSII OEC (for instance, for extraction of manganese with hydroxylamine or Tris at alkaline pH). It is interesting that hydroxylamine treatment does not remove the extrinsic manganese-stabilizing protein PsbO from PSII, whereas extraction of manganese with Tris eliminates all three extrinsic proteins [18–21].
Peculiarities of Reduction of Manganese Cations with Exogenous Reducing Agents
The effect of reductants on manganese cations within OEC shows some peculiarities. The efficiency of manganese cations’ reduction depends on the nature of the agent. For instance, hydroxylamine extracts all four cations at pH 6.5 (most favorable for evolution of oxygen [11]), whereas hydroquinone extracts only three manganese cations out of four [11], and iron cations extract two manganese cations [22]. We also looked into the efficiency of manganese cations’ extraction from OEC at other pH whose value corresponded to pK (≈5.7) of descending portion of the curve describing oxygen evolution in acidic pH region [11]. These experiments have shown that the efficiency of extraction depends on pH. For instance, Fe(II) cations extract two Mn(II) cations at pH 6.5 and only one manganese cation at pH 5.7. At the same pH values, hydroquinone and Н2О2 extract three and two cations, respectively (Table 1).
Thus, pH-dependent resistance to the effect of exogenous reductants is probably characteristic of only one manganese cation belonging to the OEC manganese cluster. When extraction of manganese cations from OEC of calcium-depleted PSII particles with Fe(II) cations was investigated, it was shown that one of the extracted manganese cations is associated with the high-affinity Mn-binding site [22] and its resistance to the effect of reductant is regulated by the calcium cation [23]. In PSII particles, the high-affinity Mn-binding site is a unique spot since, after extraction of the Mn/Ca cluster, it is the only Mn-binding site to bind Mn(II) cation subsequently oxidized by the secondary electron donor YZ [24]. It is interesting that the dissociation constant for the manganese cation bound to this site strongly depended on рН in the region of 5.0–7.0 [24]; it decreased when pH rose, i.e., the strength of Mn(II) cation binding with the high-affinity spot decreased at lower pH. This suggests that a labile manganese cation (the cation replaced by iron cation at pH 5.7 and regulated by calcium cation) is bound to the high-affinity Mn-binding site. However, pH may also affect the binding affinity of not only the Mn(II) cation but also of the manganese cation with a greater valence, which may modify another parameter: the redox potential of bound manganese cations. Since manganese cations are extracted as a result of their reduction, this may point to an important role of the ratio between redox potentials of the reductant and manganese cations in this process [25]. Thereupon, one may assume that elevation of resistance to the effect of reductants of one of the manganese cations in the cluster depends on a decrease in its redox potential at a lower pH. On the other hand, the Mn4CaO5 cluster also contains a manganese cation very much resistant to reductants at pH 6.5, which is not extracted by hydroquinone or Н2О2 (Table 1), and this cation is not associated with the high-affinity site [22]. Not long ago, Zabret et al. [26] discovered one unidentified positively charged ion (probably, manganese cation) occupying a high-affinity position within native PSII in the crystallographic structure of PSII undergoing the process of assembly (still without Mn cluster and OEC proteins). Taking into consideration this fact and the feasibility of extraction of manganese cation from the high-affinity site with reducing agents, we can assume that this ion is not the manganese cation resistant to reductants.
Effect of Са2+ on Reduction of Manganese Cations by Hydroquinone and Iron Cations
Oxidation of two water molecules coupled with the formation of molecular oxygen is performed by the catalytic center comprising one cation of calcium in addition to four manganese cations. The calcium cation is linked to Mn cations 1, 2, 3, and 4 via oxygen bridges О1, О2, and О5 (Fig. 1). Details of the mechanism of Ca2+ participation in water photolysis are still unknown. According to one of the hypotheses, the calcium cation binds a molecule of substrate water. Actually, X-ray structure analysis has shown that Ca2+ binds two molecules of water (W3 and W4). Experimental data indicate that oxygen of one of them (W3) probably participates in the formation of the molecular oxygen [27]. A new hypothesis based on model experiments has been proposed recently. Tsui and Agapie [28] revealed a linear relationship between the redox potential of the heterometallic manganese-oxido cluster and the Lewis acidity of the redox-inactive metal cation. The researchers assumed that this correlation points to the participation of the calcium cation in the modulation of the redox potential of manganese cluster. Thus, the calcium cation within OEC may affect the redox potential of one or several manganese cations and, therefore, regulate the efficiency in the reduction of manganese cations by exogenous redox agents. In this relation, we examined the effect of Ca2+ on the efficiency of extraction of manganese cations by hydroquinone and Fe(II) cations. The obtained results shown in Table 2 suggest that Ca2+ affects the reduction of manganese cations in OEC. Incubation of the PSII(-Ca) preparation with Ca2+ and hydroquinone prevents the extraction of the manganese cation at pH 6.5 but does not influence the process of extraction at pH 5.7 (Table 2). As to another reductant, namely Fe(II) cation, Cа2+ inhibits the extraction of additional the Mn cation both at pH 5.7 and pH 6.5 (Table 2). The inhibitory effect of Ca2+ on the extraction of manganese cations from OEC by hydroquinone and iron cations corroborates a possible effect of Ca2+ within OEC on the redox potential of one or several manganese cations. In addition to Ca2+, we also investigated the effect of other metal cations on the extraction of manganese cations from OEC by Fe(II) ions and hydroquinone. Out of all the tested cations (La3+, Cd2+, Ni2+, Mg2+, Sr2+ [23] and Co2+, Cd2+ Mg2+, Sr2+ [11]), only Sr2+ affected extraction, and this effect was similar to the influence of calcium cations. It is worth noting that, out of all the metal cations examined in literature reports, only strontium cations may biosynthetically replace Ca2+ cations in OEC in vivo [29–31] and restore oxygen-evolving activity (up to 40–50%) in PSII preparations without Ca2+ in OEC [32, 33]. In the aggregate, these results suggest that the mechanism of calcium influence on redox properties of manganese cation(s) in OEC depends on the participation of calcium in water photolysis. The fact that calcium cation affects the number of extracted cations of manganese indicates that the modification of preparation alters its properties, which should be taken into consideration when the experiments are designed and the obtained results interpreted.
Structural Transition in Manganese Cluster of OEC at pH 5.7
The results mentioned above suggest that, at pH 5.7 and below, there occurs a protonation of oxygen bridge(s) or one or several amino-acid residues belonging to the manganese cluster or its immediate surroundings. This process apparently reduces the redox potential of one of the manganese cations and it becomes inaccessible to the reductant [11]. It is possible that the pH dependence of reductant affects the process of protonation or deprotonation of the reductant itself as in the case of hydroquinone; however, the effect of iron cations indicates that pH dependence is mainly controlled by protonation or deprotonation of OEC. It is interesting that accurately measured (at an interval of рН 0.1) pH dependence of oxygen-evolving activity of membrane preparations of spinach and cyanobacteria has a small bend at pH 5.7 [8]. Terentyev et al. [9] also observed a short bend on the plot describing pH dependence of oxygen evolution rate. A more pronounced bend is observed on the curve of pH dependence of PSII functional activity at pH 5.3 in Synechocystis sp. PCC 6803 mutants D1-S169A and D2-K317A with substituted amino acids that apparently participate in the operation of proton channels and interact via hydrogen bonds with the manganese cluster [34]. Operation of these channels that remove protons from OEC may play a very important role in the mechanism of water oxidation since it ensures a balance in OEC between charges necessary for efficient synthesis of molecular oxygen. In other words, the rate of oxygen production may be limited by the rate of proton liberation. This assumption is corroborated by the following facts: (1) in Chlamydomonas mutant lacking a carbonic anhydrase associated with the PSII donor side, oxygen evolution is suppressed in the absence of \({\text{HCO}}_{3}^{ - }\) [35]; (2) carbonic anhydrase activity may maintain photosynthetic activity of PSII under certain conditions [9].
pH-Dependent structural transition may also be related to the effect on the PSII protein component. Extrinsic proteins of PSII are known to dissociate from the core of PSII upon acidification of the medium [12]. Protein PsbP is the first to leave the binding site; its 50% dissociation is observed at pH 5.0 [12]. For PSII particles without Са2+, this fact is of no importance since these preparations already lack this protein. However, in the case of native preparations (for instance, in thylakoid membranes), such an effect should be taken into account (see below). In the case of profound destruction of OEC, some conformational effects associated with protein СР43 [36] may arise, but they occur upon a destruction of the manganese cluster.
PRODUCTION OF Mn3Fe1 CHIMERIC CLUSTER IN OEC OF PSII AT pH 5.7
The interaction of iron cations as reductants with manganese cations within OEC has certain peculiarities. First, interaction is only possible in PSII preparations without extrinsic PsbQ and PsbP proteins that shield the manganese cluster in OEC and make it inaccessible to Fe(II) cations. Second, Fe(III) cations with a high specificity and efficiency combine with Mn-binding sites of OEC, including the high-affinity Mn-binding site [37–39]. This property of oxidized iron cations accounts for the fact that, upon reduction of manganese cation by the Fe(II) cation, Mn(II) cations are liberated from the binding site, and the vacant Mn-binding site highly efficiently binds the Fe(III) cation. This process was investigated when Fe(II) cations interacted with the manganese cluster of OEC at pH 6.5 [22]; it was shown that iron cations replace two manganese cations out of which one is associated with the high-affinity Mn-binding site. In the light, the chimeric cluster oxidizes water molecules at a lower efficiency than native PSII preparations but produces Н2О2 instead of molecular oxygen. As was shown above (Table 2), iron cations extract one manganese cation instead of two from OEC at pH 5.7. Extraction is apparently also accompanied by the replacement of a manganese cation with an iron cation; as a result, the Mn3Fe1 cluster arises in OEC. This hypothesis is corroborated by the fact that hydroquinone does not extract manganese cations from the Mn3Fe1 chimeric cluster but extracts three manganese cations from the native Mn4 cluster lacking iron cations [4]; i.e., manganese cations in the chimeric cluster are more resistant to the effect of reductant. This indirectly suggests that the cluster contains an iron cation that elevates the resistance of manganese cations. This conclusion is corroborated by the fact that the effect was the same when we compared the chimeric cluster Mn2Fe2 with Mn2 cluster [4]. Investigation into the functional activity of PSII with the chimeric cluster Mn3Fe1 resulted in an interesting discovery. In contrast to PSII with chimeric cluster Mn2Fe2, PSII with cluster Mn3Fe1 evolves oxygen in the light in the presence of exogenous calcium. The efficiency of the oxygen-evolving reaction comes to 27% of the rate observed in native PSII. The feasibility of water oxidation by the chimeric cluster with evolution of oxygen is promising for investigating the mechanism of photosynthetic oxidation of water (identification of manganese cations playing a key role in water photolysis, etc.) and for elaboration of artificial systems of water photolysis as generators of molecular oxygen and hydrogen.
рН DEPENDENCE OF PHOTOINHIBITION AND THERMAL INACTIVATION
It is known that PSII is destroyed under the effect of light and the rate of this process increases with light intensity. This effect is called photoinhibition and there are numerous reports indicating that the first stage of this process is the destruction of manganese cluster Mn4CaO5 in OEC [40–42]. The manganese cluster may be destroyed by reductants, for instance, by some reactive oxygen species (\({\text{O}}_{2}^{{ - \,\bullet }}\) and Н2О2) generated on the donor and acceptor sides of PSII [43]. Thus, an elevated resistance of manganese cluster to the effect of reductants (hydroquinone, Н2О2, and Fe(II) cations) at pH 5.7 we discovered [4, 11] may also improve PSII resistance to photoinhibition at this pH. We compared kinetics of photoinhibition in PSII membrane preparations from spinach at pH 5.7 and 6.5 [44]. The efficiency of photoinhibition was evaluated from the rate of oxygen evolution and reduction of 2,6-dichlorophenolindophenol (DCPIP) after illumination of a certain duration (Fig. 2). It was found that photoinhibition of electron transport in PSII is more efficient at pH 6.5 than at pH 5.7. The time necessary for 50% inhibition is 7.8 ± 0.4 and 18.0 ± 0.6 min at pH 6.5 and 5.7, respectively. Thus, we observed a stronger defense against photoinhibition at pH 5.7 and, judging from pH dependence of this effect, it was most pronounced exactly at this pH value.
Extraction of calcium cation from OEC does not influence pH effect and the rate of photoinhibition. However, PSII preparations with a removed Mn4CaO5 cluster, together with extrinsic proteins (PSII(-Mn)), showed quite different kinetics of photoinhibition (Fig. 3).
The obtained results show that the rate of photoinhibition in PSII(-Mn) preparations is much greater than in native PSII preparations (t1/2 = 0.18 ± 0.01 min at pH 6.5 vs. t1/2 = 7.8 ± 0.4 min in native preparations). A rise in the rate of photoinhibition of PSII lacking manganese was reported earlier [45]. An increased light sensitivity is accounted for by oxidative injury of the reaction center, whereas life span of primary oxidized donors Р680+ and \({\text{Y}}_{{\text{Z}}}^{ + }\) becomes much longer in the absence of electrons arriving from the manganese cluster or water. However, it is important to mention another fact: pH does not affect the rate of photoinactivation of PSII depleted of manganese in the region of structural transition in OEC (pH 5.7); kinetics of photoinactivation at pH 5.7 and 6.5 is the same (Fig. 3) in contrast to time courses of photoinactivation of native PSII preparations or PSII preparations lacking calcium but possessing a manganese cluster. This result distinctly shows that pH dependence of photoinactivation is controlled by a pH-dependent process in PSII OEC (without OEC, there is no pH dependence of photoinhibition; in other words, there is no elevation of resistance to light at pH 5.7).
рН-Dependence of PSII Photoinhibition in Thylakoid Membranes. Structural Transition in OEC at pH 5.7 as a Mechanism of Defense against Photoinhibition
Our analysis of pH dependence of PSII photoinactivation has shown that the greatest resistance to light is observed at pH 5.7. This value is very interesting since pH 5.7 corresponds to the acidity of intrathylakoid space (lumen) upon illumination [46–48]. It is known that electron transport in PSII generated by light ensures transmembrane proton gradient (ΔрН) used by ATP-synthase for ATP production. Generation of ΔрН is accompanied by a decrease in the lumen pH from 7.0 (in the dark) to pH 5.7–5.8 [49, 50]. When pH in the lumen is above 7.0, OEC in some PSII preparations is irreversibly inhibited [9]. It is known that the proton gradient on thylakoid membranes may vary depending on light intensity, ATP-synthase activity, etc. Moreover, there may exist great lateral pH heterogeneity between granal and stromal compartments of thylakoids [51, 52]. Taking into consideration these results, we investigated photoinhibition of PSII and the effect of uncouplers NH4Cl and nigericin on this process. Photoinactivation was monitored by recording the rate of oxygen evolution using an acceptor of electrons 2,6-dichloro-p-benzoquinone (0.2 mM). Thylakoid membranes were suspended in tricine buffer at pH 7.6 (20 µg Chl/mL), illuminated (1300 µE/(m2 s)) at 25°С, and the rate of oxygen evolution was measured. The results are shown in Table 3. According to the obtained data, the rate of photoinactivation of thylakoid membranes was somewhat lower than in PSII preparations (Fig. 2, Table 3). However, uncouplers considerably accelerated this process (Table 3). Since uncouplers abolish the proton gradient [53] raising pH in the lumen (where OEC is located), this result may be considered as an additional indication that pH 5.7 ensures the strongest defense of PSII against photoinhibition.
Elevation of PSII Thermostability at pH 5.7
Improvement of resistance of manganese cations in OEC to exogenous reductants with a maximum at pH 5.7 may also play an important role in plant defense against heat injury since thermal inactivation apparently involves reactive oxygen species [54], some of which are efficient reductants [43]. We discovered that membrane preparations of PSII suspended in a buffer with pH 5.7 are less sensitive to heat stress (50°C) than identical samples at pH 6.5. After a thermal treatment, the residual rate of electron transport to artificial acceptor DCPIP at pH 6.5 was close to zero, whereas it amounted to 20–25% of the initial level at pH 5.7 [55]. We assume that elevation of OEC resistance to heat stress at pH 5.7 is accounted for by pH-dependent changes in redox potential Em of one or several manganese cations in OEC [11]. In turn, changes in Em elevate the resistance of manganese cations to reductants, for instance, to some forms of reactive oxygen species. Taking into consideration an identical effect of pH in photoinhibition [44], we suppose that structural transition within the manganese cluster at pH 5.7 may play an important role in defensive response of PSII to destructive environmental impacts.
CONCLUSIONS
Agreement of acidity at which protection of PSII from photoinhibition is elevated (pH 5.7) with pH value arising in the lumen upon generation of transmembrane pH gradient implies that pH-dependent structural transition at pH 5.7 may play the role of a novel (earlier unknown) pH-dependent mechanism ensuring self-defense of photosynthetic apparatus against photoinactivation. A diagram of such a mechanism shown in Fig. 4 envisages the following: in thylakoid membranes, illumination of PSII is accompanied by generation of ΔpH on the thylakoid membrane and a decrease in pH in the lumen to the value of ≈5.7 [49, 50], i.e., to pH ensuring the strongest defense against photoinhibition. Thus, the effect we discovered accounts for an additional mechanism of PSII defense against photoinhibition in the light.
REFERENCES
Umena, Y., Kawakami, K., Shen, J.-R., and Kamiya, N., Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å, Nature, 2011, vol. 473, p. 55. https://doi.org/10.1038/nature09913
Suga, M., Akita, F., Hirata, K., Ueno, G., Murakami, H., Nakajima, Y., Shimizu, T., Yamashita, K., Yamamoto, M., Ago, H., and Shen, J.-R., Native structure of photosystem II at 1.95 Å resolution viewed by femtosecond X‑ray pulses, Nature, 2015, vol. 517, p. 99. https://doi.org/10.1038/nature13991
Shen, J.-R., The structure of photosystem II and the mechanism of water oxidation in photosynthesis, Annu. Rev. Plant Biol., 2015, vol. 66, p. 23. https://doi.org/10.1146/annurev-arplant-050312-120129
Semin, B.K., Davletshina, L.N., Seibert, M., and Rubin, A.B., Creation of a 3Mn/1Fe cluster in the oxygen-evolving complex of photosystem II and investigation of its functional activity, J. Photochem. Photobiol. B., 2018, vol. 178, p. 192. https://doi.org/10.1016/j.jphotobiol.2017.11.016
Damoder, R. and Dismukes, G.C., pH dependence of the multiline, manganese EPR signal for the 'S2' state in PS II particles. Absence of proton release during the S1→S2 electron transfer step of the oxygen evolving system, FEBS Lett., 1984, vol. 174, p. 157. https://doi.org/10.1016/0014-5793(84)81096-0
Vass, I. and Styring, S., pH-dependent charge equilibria between tyrosine-D and the S states in photosystem II. Estimation of relative midpoint redox potentials, Biochem., 1991, vol. 30, p. 830. https://doi.org/10.1021/bi00217a037
Haddy, A., Hatchell, J.A., Kimel, R.A., and Thomas, R., Azide as a competitor of chloride in oxygen evolution by photosystem II, Biochem., 1999, vol. 38, p. 6104. https://doi.org/10.1021/bi983075c
Schiller, H. and Dau, H., Preparation protocols for high-activity photosystem II membrane particles of green algae and higher plants, pH dependence of oxygen evolution and comparison of the S2-state multiline signal by X-band EPR spectroscopy, J. Photochem. Photobiol. B, 2000, vol. 55, p. 138. https://doi.org/10.1016/S1011-1344(00)00036-1
Terentyev, V.V., Shukshina, A.K., and Shitov, A.V., Carbonic anhydrase CAH3 supports the activity of photosystem II under increased pH, Biochim. Biophys. Acta Bioenerg., 2019, vol. 1860, no. 7, p. 582. https://doi.org/10.1016/j.bbabio.2019.06.003
Semin, B.K., Davletschina, L.N., Aleksandrov, A.Yu., Lanchinskaya, V.Yu., Novakova, A.A., and Ivanov, I.I., pH dependence of iron binding to the donor side of photosystem II, Biochem. (Mosc.), 2004, vol. 69, p. 410. https://doi.org/10.1023/B:BIRY.0000022066.38297.8a
Semin, B.K., Davletshina, L.N., and Rubin, A.B., Correlation between pH dependence of O2 evolution and sensitivity of Mn cations in the oxygen-evolving complex to exogenous reductants, Photosynth. Res., 2015, vol. 125, p. 95. https://doi.org/10.1007/s11120-015-0155-4
Shen, J.-R. and Inoue, Y., Low pH-induced dissociation of three extrinsic proteins from O2-evolving photosystem II, Plant Cell Physiol., 1991, vol. 32(3), p. 453. https://doi.org/10.1093/oxfordjournals.pcp.a078101
Ono, T. and Inoue, Y., Discrete extraction of the Ca atom functional for O2 evolution in higher plant photosystem II by a simple low pH treatment, FEBS Lett., 1988, vol. 227, p. 147. https://doi.org/10.1016/0014-5793(88)80886-X
Bernát, G., Morvaridi, F., Feyziyev, Y., and Styring, S., pH dependence of the four individual transitions in the catalytic S-cycle during photosynthetic oxygen evolution, Biochemistry, 2002, vol. 41, p. 5830. https://doi.org/10.1021/bi011691u
Suzuki, H., Sugiura, M., and Noguchi, T., pH dependence of the flash-Induced S-state transitions in the oxygen-evolving center of photosystem II from Thermosynechoccocus elongatus as revealed by Fourier transform infrared spectroscopy, Biochemistry, 2005, vol. 44, p. 1708. https://doi.org/10.1021/bi0483312
Ghanotakis, D.F., Topper, J.N., and Yocum, C.F., Exogenous reductants reduce and destroy the Mn-complex in photosystem II membranes depleted of the 17 and 23 kDa polypeptides, Biochim. Biophys. Acta, 1984, vol. 767, p. 524. https://doi.org/10.1016/0005-2728(84)90051-3
Ono, T. and Inoue, Y., Abnormal redox reactions in photosynthetic O2-evolving centers in NaCl/EDTA-washed PS II. A dark-stable EPR multiline signal and an unknown positive charge accumulator, Biochim. Biophys. Acta, 1990, vol. 1020, p. 269. https://doi.org/10.1016/0005-2728(90)90157-Y
Klimov, V.V., Allakhverdiev, S.I., Shuvalov, V.A., and Krasnovsky, A.A., Effect of extraction and re-addition of manganese on light reactions of photosystem-II preparations, FEBS Lett., 1982, vol. 148, p. 307. https://doi.org/10.1016/0014-5793(82)80830-2
Ghirardi, M.L., Lutton, T.W., and Seibert, M., Interactions between diphenylcarbazide, zinc, cobalt, and manganese on the oxidizing side of photosystem II, Biochem., 1996, vol. 35, p. 1820. https://doi.org/10.1021/bi951657d
Allakhverdiev, S.I., Yruela, I., Picorel, R., and Klimov, V.V., Bicarbonate is an essential constituent of the water-oxidizing complex of photosystem II, Proc. Natl. Acad. Sci. U.S.A., 1997, vol. 94, p. 5050. https://doi.org/10.1073/pnas.94.10.5050
Nagata, T., Zharmukhamedov, S.K., Khorobrykh, A.A., Klimov, V.V., and Allakhverdiev, S.I., Reconstitution of the water-oxidizing complex in manganese-depleted photosystem II preparations using synthetic Mn-complexes: a fluorine-19 NMR study of the reconstitution process, Photosynth. Res., 2008, vol. 98, p. 277. https://doi.org/10.1007/s11120-008-9319-9
Semin, B.K. and Seibert, M., Substituting Fe for two of the four Mn ions in photosystem II—effects on water-oxidation, J. Bioenerg. Biomembr., 2016, vol. 48, p. 227. https://doi.org/10.1007/s10863-016-9651-2
Semin, B.K., Davletshina, L.N., Goryachev, S.N., and Seibert, M., Ca2+ effects on Fe(II) interactions with Mn-binding sites in Mn-depleted oxygen-evolving complexes of photosystem II and on Fe replacement of Mn in Mn-containing, Ca-depleted complexes, Photosynth. Res., 2021, vol. 147(2), p. 229. https://doi.org/10.1007/s11120-020-00813-z
Ono, T. and Mino, H., Unique binding site for Mn2+ ion responsible for reducing an oxidized YZ tyrosine in manganese-depleted photosystem II membranes, Biochem., 1999, vol. 38, p. 8778. https://doi.org/10.1021/bi982949s
Kuntzleman, T., McCarrick, R., Penner-Hahn, J., and Yocum, C., Probing reactive sites within the photosystem II manganese cluster: evidence for separate populations of manganese that differ in redox potential, Phys. Chem. Chem. Phys., 2004, vol. 6, p. 4897. https://doi.org/10.1039/B406601D
Zabret, J., Bohn, S., Schuller, S.K., Arnolds, O., Möller, M., Meier-Credo, J., Liauw, P., Chan, A., Tajkhorshid, E., Langer, J.D., Stoll, R., Krieger-Liszkay, A., Engel, B.D., Rudack, T., Schuller, J.M., and Nowaczyk, M.M., Structural insights into photosystem II assembly, Nat. Plants, 2021, vol. 7, p. 524. https://doi.org/10.1038/s41477-021-00895-0
Kim, C.J., and Debus, R.J., Evidence from FTIR difference spectroscopy that a substrate H2O molecule for O2 formation in photosystem II is provided by the Ca ion of the catalytic Mn4CaO5 cluster, Biochemistry, 2017, vol. 56, p. 2558. https://doi.org/10.1021/acs.biochem.6b01278
Tsui, E.Y. and Agapie, T., Reduction potentials of heterometallic manganese-oxido cubane complexes modulated by redox-inactive metals, Proc. Natl. Acad. Sci. U.S.A., 2013, vol. 110, p. 10084. https://doi.org/10.1073/pnas.1302677110
Boussac, A., Rappaport, F., Carrier, P., Verbavatz, J.M., Gobin, R., Kirilovsky, D., Rutherford, A., and Sugiura, M. Biosynthetic Ca2+/Sr2+ exchange in the photosystem II oxygen-evolving enzyme of Thermosynechococcus elongatus, J. Biol. Chem., 2004, vol. 279, p. 22809. https://doi.org/10.1074/jbc.M401677200
Kargul, J., Maghlaoui, K., Murray, J.W., Deak, Z., Boussac, A., Rutherford, A.W., Vass, I., and Barber, J. Purification, crystallization and X-ray diffraction analyses of the T. elongatus PSII core dimer with strontium replacing calcium in the oxygen-evolving complex, Biochim. Biophys. Acta Bioenerg., 2007, vol. 1767, p. 404. https://doi.org/10.1016/j.bbabio.2007.01.007
Koua, F.H.M., Structural changes in the acceptor site of photosystem II upon Ca2+/Sr2+ exchange in the Mn4CaO5 cluster site and the possible long-range interactions, Biomolecules, 2019, vol. 9, p. 371. https://doi.org/10.3390/biom9080371
Ghanotakis, D.F., Babcock, G.T., and Yocum, C.F., Calcium reconstitutes high rates of oxygen evolution in polypeptide depleted photosystem II preparations, FEBS Lett., 1984, vol. 167, p. 127. https://doi.org/10.1016/0014-5793(84)80846-7
Vrettos, J.S., Limburg, J., and Brudvig, G.W., Mechanism of photosynthetic water oxidation: combining biophysical studies of photosystem II with inorganic model chemistry, Biochim. Biophys. Acta, 2001, vol. 1503, p. 229. https://doi.org/10.1016/S0005-2728(00)00214-0
Ghosh, I., Khan, S., Banerjee, G., Dziarski, A., Vinyard, D.J., Debus, R.J., and Brudvig, G.W., Insights into proton-transfer pathways during water oxidation in photosystem II, J. Phys. Chem. B., 2019, vol. 123, p. 8195. https://doi.org/10.1021/acs.jpcb.9b06244
Shutova, T., Kenneweg, H., Buchta, J., Nikitina, J., Terentyev, V., Chernyshov, S., Andersson, B., Allakhverdiev, S., Klimov, V., Dau, H., Junge, W., and Samuelsson, G., The photosystem II-associated Cah3 in Chlamydomonas enhances the O2 evolution rate by proton removal, EMBO J., 2008, vol. 27, p. 782. https://doi.org/10.1038/emboj.2008.12
Tokano, T., Kato, Y., Sugiyama, S., Uchihashi, T., and Noguchi, T., Structural dynamics of a protein domain relevant to the water-oxidizing complex in photosystem II as visualized by high-speed atomic force microscopy, J. Phys. Chem. B, 2020, vol. 124, p. 5847. https://doi.org/10.1021/acs.jpcb.0c03892
Semin, B.K., Ivanov, I.I., Rubin, A.B., and Parak, F., High-specific binding of Fe(II) at the Mn-binding site in Mn-depleted PSII membranes from spinach, FEBS Lett., 1995, vol. 375, p. 223. https://doi.org/10.1016/0014-5793(95)01215-Z
Semin, B.K., Ghirardi, M.L., and Seibert, M., Blocking of electron donation by Mn(II) to YZ· following incubation of Mn-depleted photosystem II membranes with Fe(II) in the light, Biochemistry, 2002, vol. 41, p. 5854. https://doi.org/10.1021/bi0200054
Semin, B.K. and Seibert, M., A carboxylic residue at the high-affinity, Mn-binding site participates in the binding of iron cations that block the site, Biochim. Biophys. Acta, 2006, vol. 1757(3), p. 189. https://doi.org/10.1016/j.bbabio.2006.02.001
Virgin, I., Styring, S., and Andersson, B., Photosystem II disorganization and manganese release after photoinhibition of isolated spinach thylakoid membranes, FEBS Lett., 1998, vol. 233, p. 408. https://doi.org/10.1016/0014-5793(88)80472-1
Hakala, M., Tuominen, I., Keränen, M., Tyystjärvi, T., and Tyystjärvi, E., Evidence for the role of the oxygen-evolving manganese complex in photoinhibition of photosystem II, Biochim. Biophys. Acta, 2005, vol. 1706, p. 68. https://doi.org/10.1016/j.bbabio.2004.09.001
Tyystjärvi, E., Photoinhibition of photosystem II and photodamage of the oxygen evolving manganese cluster, Coord. Chem. Rev., 2008, vol. 252, p. 361. https://doi.org/10.1016/j.ccr.2007.08.021
Pospišil, P., Molecular mechanisms of production and scavenging of reactive oxygen species by photosystem II, Biochim. Biophys. Acta, 2012, vol. 1817, p. 218. https://doi.org/10.1016/j.bbabio.2011.05.017
Davletshina, L.N. and Semin, B.K., pH dependence of photosystem II photoinhibition: relationship with structural transition of oxygen-evolving complex at the pH of thylakoid lumen, Photosynth. Res., 2020, vol. 145, p. 135. https://doi.org/10.1007/s11120-020-00769-0
Klimov, V.V., Shafiev, M.A., and Allakhverdiev, S.I., Photoinactivation of the reactivatipon capacity of photosystem II in pea subchloroplast particles after a complete removal of manganese, Photosynth. Res., 1990, vol. 23, p. 59. https://doi.org/10.1007/BF00030063
Kramer, D.M., Sacksteder, C.A., and Cruz, J.A., How acidic is the lumen?, Photosynth. Res., 1999, vol. 60, p. 151.https://doi.org/10.1023/A:1006212014787
Cruz, J.A., Sacksteder, C.A., Kanazawa, A., and Kramer, D.M., Contribution of electric field (Δψ) to steady-state transthylakoid proton motive force (pmf) in vitro and in vivo. Control of PMF parsing into Δψ and ΔpH by ionic strength, Biochem., 2001, vol. 40, p. 1226. https://doi.org/10.1021/bi0018741
Takizawa, K., Cruz, J.A., Kanazawa, A., and Kramer, D.M., The thylakoid proton motive force in vivo. Quantitative, non-invasive probes, energetics, and regulatory consequences of light-induced PMF, Biochim. Biophys. Acta, 2007, vol. 1767, p. 1233.https://doi.org/10.1016/j.bbabio.2007.07.006
Cruz, J.A., Kanazawa, A., Treff, N., and Kramer, D.M., Storage of light-driven transthylakoid proton motive force as an electric field (Δψ) under steady-state conditions in intact cells of Chlamydomonas reinhardtii, Photosynth. Res., 2005, vol. 85, p. 221. https://doi.org/10.1007/s11120-005-4731-x
Kramer, D.M., Cruz, J.A., and Kanazawa, A., Balancing the central roles of the thylakoid proton gradient, Trends Plant Sci., 2003, vol. 8, p. 27. https://doi.org/10.1016/S1360-1385(02)00010-9
Vershubskii, A.V., Trubitsin, B.V., Priklonskii, V.I., and Tikhonov, A.N., Lateral heterogeneity of the proton potential along the thylakoid membranes of chloroplasts, Biochim. Biophys. Acta Biomembr., 2017, vol. 1859, p. 388. https://doi.org/10.1016/j.bbamem.2016.11.016
Tikhonov, A.N., Photosynthetic electron and proton transport in chloroplasts: EPR Study of ΔpH generation, an overview, Cell Biochem. Biophys., 2017, vol. 75, p. 421. https://doi.org/10.1007/s12013-017-0797-2
Sen, K., Ghosh, A., Chakraborty, M., Maity, S., Ghosh, S., and DasGupta, M., Trans-thylakoid ΔpH dependent oscillation of FPSI/FPSII under continuous irradiance in isolated thylakoids, J. Bioenerg. Biomembr., 2014, vol. 46, p. 71.https://doi.org/10.1007/s10863-013-9533-9
Yamashita, A., Nijo, M., Pospišil, P., Morita, N., Takenaka, D., Aminaka, R., Yamamoto, Yo., and Yamamoto, Ya., Quality control of photosystem II. Reactive oxygen species are responsible for the damage to photosystem II under moderate heat stress, J. Biol. Chem., 2008, vol. 283, p. 28380. https://doi.org/10.1074/jbc.M710465200
Lovyagina, E. and Semin, B., Elevation of photosystem II thermal stability at pH 5.7 due to the structural transition in the oxygen-evolving complex, J. Plant Biochem. Biotechnol., 2021, vol. 31, p. 440. https://doi.org/10.1007/s13562-021-00693-x
ACKNOWLEDGMENTS
This work was performed within the framework of a state assignment given to Moscow State University, project no. 121032500058-7.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
The authors declare that they have no conflicts of interest.
Additional information
Translated by N. Balakshina
Abbreviations: Chl—chlorophyll; DCPIP—2,6-dichlorophenolindophenol; OEC—oxygen-evolving complex; PSII(-Ca)—photosystem II without calcium cation and proteins PsbP and PsbQ in the oxygen-evolving complex; PSII(-Mn)—photosystem II without oxygen-evolving complex.
Rights and permissions
Open Access. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
About this article
Cite this article
Semin, B.K., Davletshina, L.N., Loktyushkin, A.V. et al. Physiological Role of pH-Dependent Structural Transition in Oxygen-Evolving Complex of PSII. Russ J Plant Physiol 70, 1 (2023). https://doi.org/10.1134/S1021443722700017
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1134/S1021443722700017