Roles of manganese in photosystem II dynamics to irradiations and temperatures

Abstract

The most amazing chemistry is the light-driven water splitting reaction occurred in the oxygen-evolving complex of phototsystem II in higher plants, green algae, and cyanobacteria. Mn, in the form of Mn₄CaO₅ cluster in photosystem II, is responsible for the catalytic water splitting reaction as well as plays roles in photosystem II dynamics to irradiation and temperatures. Manganese hypothesis of UV-initiated photoinhibition as a direct target is established, and thermal inactivation of photosystem II involves the valence and structural changes of manganese. Recent progresses in understanding the roles of manganese in photoinhibition especially under UV light and in thermal inactivation including elevated temperatures using synthetic models and native PS II complexes are summarized and evaluated. Potential problems and possible solutions are discussed and presented.

Keywords

photosynthesis / manganese / photosystem II / irradiation / temperature / stress

Introduction

Photosynthesis, which harvests, transfers, converts and stores the solar energy in the form of chemical bonding energy and supports all the living things on earth (Blankenship, 2002), is one of the most important chemical reactions in science. In photosynthetic process, the most amazing chemistry is water splitting reaction, which occurs in the phototsystem II (PS II) protein complex embedded in the thylakoid membranes of higher plants, green algae, and cyanobacteria (Rutherford and Boussac, 2004; Brudvig, 2008). However the molecular basis of photosynthetic water oxidation has remained one of the major mysteries in bioenergetics research.

PS II functions as a water-plastoquinone oxidareductase and is able to catalyze the light-driven transfer of electron and proton from water at the luminal side to a pool of plastoquione molecules at the stromal side of the thylakoid membranes (Diner and Rappaport, 2002). The kinetics of the electron transfer steps in PS II has been thoroughly investigated over the complete time scale of femtosecond to many seconds (van Grondelle et al., 1994; Rappaport et al., 2002; Govindjee and Seibert, 2010). The early process occurring in PS II revealed by ultrafast spectroscopy can be divided into several steps: (1) absorption of light quanta by antenna to form excited states of pigments; (2) trapping of excitation energy by the primary electron donor P₆₈₀ in the reaction center on the picosecond time scale; (3) primary charge separation from the singlet excited state of P₆₈₀ to the primary acceptor pheophytin (Pheo) in about 3-20 ps; (4) stabilization of the separated charges from the radical pair {{\mathrm{P}}_{\mathrm{680}}}^{+}Pheo^- on the acceptor side by electron transfer to Q_A in about 200 ps and to Q_B on the hundreds of millisecond time scale; and (5) on the donor side, an electron is supplied to reduce{{\mathrm{P}}_{\mathrm{680}}}^{+} from a tyrosine residue (Y_Z) on the nanosecond time scale to microsecond time scale.

In contrast to the knowledge of the kinetics, that of the thermodynamics of electron transfer step in PS II is relatively limited (van Gorkom, 1985; Delosme et al., 1994; Delosme, 2003; Hou and Mauzerall, 2011). The free energy of the electron transfer process is obtained from midpoint redox potentials of the respective components or from the analysis of kinetic data (van Gorkom, 1985; Sakuragi et al., 2002). Using photoacoustics, quantum yield, volume changes, and reaction enthalpy of electron transfer from P₆₈₀ to Q_A in PS II of Synechocystis 6803 are determined (Hou et al., 2001a). The apparent entropy change of the reaction in PS II is negative, which is different from large positive entropy of PS I of Synechocystis 6803 and purple bacteria of Rb. Sphaeroides (Edens et al., 2000; Hou et al., 2001b; Hou and Mauzerall, 2006; Mauzerall, 2006; Hou et al., 2009). The negative entropy may be due to a mixture of electron transfer from anionic tyrosine and fast proton transfer to a polar region in PS II (Hou et al., 2001a; Hou and Mauzerall, 2011). The preliminary data using photothermal beam deflection sensor (Krivanek et al., 2008) and an air microphone photoacoustic detector (Mauzerall, 2010) suggests that the S-state cycle in PS II oxygen-evolving complex is likely entropy-driven as are steps in PS I (Mauzerall, 2006).

PS II is very sensitive to changes in environment. Under unfavorable or stressful environmental conditions, such as strong light, high concentration of salt, and low and high temperatures, the activity of PS II declines more rapidly (Pearcy et al., 1977; Aro et al., 1993; Niyogi, 1999; Barbara Demmig-Adams and Autar, 2007; Murata et al., 2007; Takahashi and Murata, 2008). The effects of environmental stress on damage and repair were explored and multiple hypothetical models were proposed.

In this review, we will summarize the recent advances in literature associated with the roles of manganese in photoinhibition and thermal inactivation. Other aspects of manganese structure and function in photosystem II were briefly discussed to provide a background of manganese in photosynthesis. The focus is placed on the response mechanisms of Mn₄CaO₅ cluster in PS II to strong light and elevated temperature. We also discuss the potential problems and possible solutions.

Mn₄CaO₅ cluster in PS II

Mn₄CaO₅ cluster in PS II plays a vital role in oxygenic photosynthesis and is responsible for the catalytic water splitting chemistry (Diner and Babcock, 1996; Diner and Rappaport, 2002; Vrettos and Brudvig, 2002). In PS II, which is integral membrane protein complex of more than 20 subunits with a molecular mass of about 350 kD, Mn₄CaO₅ cluster is the site of water oxidation to oxygen (Brudvig, 2008). When four electrons and four protons are extracted from two molecules of water, one molecule of dioxygen is produced. The mechanism of photosynthetic water oxidation in PS II is believed to occur through four distinct oxidation step as the S-state cycle by Kok et al. (1970) and Joliot et al. (1969).

The structure of PS II has been determined at resolution of 2.9–3.8 Å from Thermosynechococcus elongates and Thermsynechocccus vulcanus (Kamiya and Shen, 2003; Ferreira et al., 2004; Loll et al., 2005). However due to the sensitivity of Mn cluster to X-ray exposure and relative low resolution crystallographic data, the structure of Mn cluster and substrate water molecules in PS II are revealed. A recent study reported the high-resolution structure of PS II from Thermosynechococcus vulcanus at a resolution of 1.9 Å (Umena et al., 2011). The complete geometry arrangement of the Mn cluster including its oxo bridges and ligands were determined. Three manganese, one calcium and four oxygen atoms form a cubane-like structure. The fourth manganese is located outside the cubane. In addition, five water molecules are also identified in the structure of PS II. These molecular details reveal important function for the mechanism of water splitting and O-O bond formation.

Mn in photoinhibition of PS II

PS II plays an important role in response to the environmental conditions such as excess light, which is known as photoinhibition and is observed either under high intensity light conditions when the repair mechanisms have reached maximum capacity or at lower light intensities when an additional external factor inhibits the repair of PS II (Kok et al., 1966; Powles, 1984). The molecular mechanisms of photoinhibition were extensively investigated with great progress made during last decades (Ohad et al., 1990; Aro et al., 1993; Chow, 1994; Stewart and Brudvig, 1998; Niyogi, 1999; Tracewell et al., 2001; Adir et al., 2003; Allakhverdiev and Murata, 2004; Frank and Brudvig, 2004; Carpentier, 2005; Nishiyama et al., 2005; Szabó et al., 2005; Telfer, 2005; Nishiyama et al., 2006; Zsiros et al., 2006; Murata et al., 2007; Tyystjarvi, 2008; Kramer, 2010; Sarvikas et al., 2010a; Sarvikas et al., 2010b). Light-induced damage is targeted mainly to PS II (Powles, 1984; Barber and Andersson, 1992). The action spectra of photoinhibition of spinach chloroplast revealed that ultraviolet light is highly photoinhibitory to PS II (Jones and Kok, 1966). It was proposed that plants have a recovery mechanism that continuously repairs the photoinhibitory damages. The visible light part of the action spectra was found to have a peak in the red region, suggesting that chlorophylls act as photoreceptors of photoinhibition. Photoinhibition is accompanied by selective loss of the D1 protein in the PS II reaction center (Kyle et al., 1984). The environmental stress factors, such as salt, cold, and moderate heat, do not affect photodamage of PS II but inhibit the repair of PS II. In this way, environmental stress enhances the extent of photoinhibition (Allakhverdiev and Murata, 2004, 2008; Takahashi and Murata, 2008).

Photoinactivation of the PS II reaction center is hypothesized to occur by two independent mechanisms associated with the acceptor and donor sides of PS II, respectively, were published in the several comprehensive reviews (Barber and Andersson, 1992; Aro et al., 1993; Tyystjarvi, 2008). As summarized by Hakala et al. (Hakala et al., 2005), both models result in the inhibition of electron transfer in PS II and the subsequent degradation of the D1 protein (Fig. 1). The acceptor side inhibition occurs under high light conditions when the plastoquinone pool is fully reduced, and consequently there is a lack of oxidized plastoquinone to bind to the Q_B site on the D1 protein (Fig. 1C). In this case, Q_A will become doubly reduced on a second turnover of the reaction center to form {\mathrm{Q}}_{\mathrm{A}}^{2-}, because {\mathrm{Q}}_{\mathrm{A}}^{-} cannot transfer an electron to Q_B. {\mathrm{Q}}_{\mathrm{A}}^{2-} then becomes protonated to form Q_AH₂ and is released from the {\mathrm{Q}}_{\mathrm{A}}^{-} binding site on the D1 protein. It is noted that the accumulation of double reduced Q_A in photoinhibition may not occur in aerobic conditions (Setlik et al., 1990; Vass et al., 1993). With the Q_A site unoccupied, the excitation of {{\mathrm{P}}_{\mathrm{680}}}^{+} will result in the formation of the radical pair-{{\mathrm{P}}_{\mathrm{680}}}^{+}Pheo^-. Recombination of charge separation will generate a triplet state of {{\mathrm{P}}_{\mathrm{680}}}^{+}, which will react with oxygen to form singlet oxygen. The singlet oxygen as one of the reactive oxygen species (ROS) is highly toxic to proteins and cofactors and can react with the D1 protein, triggering the degradation of the D1 protein (Shipton and Barber, 1991, 1994).

The donor-side photoinhibition of PS II occurs as a result of the formation of the highly reactive {\mathrm{P}}_{\mathrm{680}}^{+} species under light (Fig. 1B). {\mathrm{P}}_{\mathrm{680}}^{+} is capable of oxidizing neighboring proteins and chromophores. Oxidation of accessory chlorophylls and β-carotene and degradation of D1 have been found to occur under conditions of {\mathrm{P}}_{\mathrm{680}}^{+} formation using the isolated PS II reaction center D1/D2/cyt b₅₅₉ complex (Telfer et al., 1990; Peng et al., 1999). Loss of donor-side electron transport and consequent photodamage to the D1 protein have been linked to the generation of high H⁺ electrochemical potential across the thylakoid membrane and the possible associated release of Ca²⁺ from the water-oxidizing complex (Ohad et al., 1994). It was also found that the process does not require the presence of oxygen (Jegerschöld and Styring, 1991; Shipton and Barber, 1992) and is not accompanied by singlet oxygen production in Tris-pretreated thylakoids (Hideg et al., 1994).

The first study on UV-B effect on photoinhibition of PS II showed that UV-B primarily attacks the water oxidizing complex in 1989 (Renger et al., 1989). Recently, a Mn-targeted hypothesis for the mechanism of UV photoinhibition of PS II was proposed (Hakala et al., 2005; Ohnishi et al., 2005), as shown in Fig. 1A. The photoinactivation of the thylakoid membranes from Thermodynechococcus elongatus by UV and blue light was suggested to be the first step of photoinhibition (Ohnishi et al., 2005). The experimental evidence seems to support that the earliest step in photoinhibition is the release of a manganese ion from PS II (Hakala et al., 2005). A photon absorbed by the manganese ions of the oxygen-evolving complex triggers inactivation of the oxygen-evolving complex, which is supported by measuring the action spectra of photoinhibition. The inhibition occurs like in the donor-side model. Furthermore, it is reported that not only the Mn ions in PS II oxygen-evolving complex (OEC) (Hakala et al., 2005), but also the PS II protein subunits, 33 kD, 24 kD and 18 kD, are released form the spinach PS II membranes under photoinhibitory illumination. The released proteins, 33 kD and 24 kD, were photodamaged and lost the ability to rebind to PS II. In addition, Mn catalase and Mn superoxide dismutase are also photosensitive to both visible and UV light (Hakala et al., 2006). The oxidation state of the water-splitting complex seems play an role in PS II sensitivity by UV-B radiation (Szilárd et al., 2007). The photodamage of the Mn₄CaO₅ complex in single crystals of PS II was also reported by exposure to X-rays during crystallographic data collection (Yano et al., 2005). Their X-ray absorption spectra show that the damage site is the reduction of high-valent manganese ions and associated with structure change.

The mixed-valence Mn(III/IV)-oxo dimer compound, [Mn(III)(O)₂Mn(IV)(H₂O)₂(Terpy)₂](NO₃)₃, is the first functional model oxygen-evolution complex of PS II (Limburg et al., 1999). The structure of the Mn-oxo mix-valence dimer is shown in Fig. 2. The Mn-oxo mix-valence dimer is able to catalyze oxygen evolution in the presence of several chemical oxidants such as hypochlorite (Limburg et al., 1999; Cady and Brudvig, 2008), Ce⁴⁺ ion (Tagore et al., 2007a) and oxone (Chen et al., 2007). The mechanism of its catalytic reaction in water oxidation was well studied (Limburg et al., 2001; Tagore et al., 2007b; Usov et al., 2007; Cady and Brudvig, 2008).

When the Mn-oxo dimer was exposed to strong illumination, photodamage of the compound was confirmed by the changes in the UV-visible spectra shown in Fig. 3. The UV illumination at 254 nm and 312 nm caused the appearance of two novel absorption peaks at 440 nm and 400 nm (Wei et al., 2011). The increased absorption at 400-450 nm is a characteristic of formation of a Mn(IV/IV)-oxo species (Limburg et al., 2001; Wei et al., 2011). In contrast, the exposure to light at 365, 453, 555, and 655 nm had no such effects. As the energy of UV light is higher than that of visible light, the formation of a Mn(IV/IV) species during the photoreaction is likely the consequence yield by UV radiation.

In addition, fluorescence spectrometric data on the synthetic Mn-oxo dimer compound showed that the a novel fluorescence peak at 514 nm was observed under UV illumination (Wei et al., 2011). The UV-induced formation of the Mn(IV/IV) species is correlated with the formation of a species that exhibits a fluorescence emission in aqueous solution. This is the first observation of a fluorescent high-valent Mn-oxo complex in the literature. The observed fluorescence peak at 514 nm is most likely emitted by the Terpy (2,2':6',6''-terpyridine) ligand and not by the central manganese ions. It was reported that 2,2'-bipyridine and 1, 10-phenanthroline are emissive depending the pH values of the solutions (Henry and Hoffman, 1979). The fluorescent Mn species might involve the hydration or protonation of the Terpy ligand.

Figure 4 is the absorption action spectrum, oxygen-evolution action spectrum of photodamage of the Mn(III/IV) dimer, and oxygen-evolution action spectrum of PS complexes from spinach. The action spectra of the synthetic manganese compound and PS II complexes are similar throughout the UV and visible wavelength range, suggesting that the mechanism of the photodamage reaction in the Mn model compound might be share the similar model with PS II. The UV light may cause a valence change of the Mn ion in the OEC of PS II in photoinhibition and that visible light cannot produce the same effect. This observation support that the high energy UV light is directly absorbed by the Mn ions in the PS II OEC and cause a valence change of Mn. The high-valent Mn(IV) species may oxidize another redox component such the protein or cofactors in PS II. Similar conclusion was reached by use of a tetra nuclear oxo-Mn(IV) complex, [Mn₄O₆(bpea)₄]₄Br₄ (Antal et al., 2009). The light-induced changes of the Mn (IV) tetramer are consistent with a one-electron reduction in the compound. The possible photoxidation of bromide by the Mn(IV) tetramer is possible and implies that the oxidation of chloride is involved in photoinhibition (Antal et al., 2009). This Mn-initiated photoinhibition is different from those in visible light-induced photodamage, which involves the photodamage of chlorophylls and carotenoid molecules.

In contrast to the chlorophyll a-containing species, a new unique strain chlorophyll d-containing cyanobacterium Acaryochloris marina is able to use chlorophyll d to store solar energy at longer wavelengths of light (690 and 750 nm) (Miyashita et al., 1996; Murakami et al., 2004; Kashiyama et al., 2008). The energetic data of electron transfer in this species has been reported (Allakhverdiev et al., 2010; Allakhverdiev et al., 2011; Tomo et al., 2011). Its energy-storage efficiency is comparable to or higher than that in typical, chlorophyll a-utilizing oxygenic species, determined by photoacoustic measurement on whole cells (Mielke et al., 2011). Acaryochloris is able to adapt to the low light environment. However under excess light illumination, it is extremely sensitive and vulnerable. HPLC analysis showed that the content of photosynthetic pigments including zeaxanthin, chlorophyll d, and a-carotene are decreased by about 80% upon strong light treatment. Interestingly, the cells of Acaryochloris marina were affected differently upon the illumination of visible light at 700 nm and UV radiation at 312 nm. The data suggested that the UV light at 312 nm targets on Mn cluster and 700 nm on chlorophyll d light-harvesting system.

In the manganese-induced photoinhibition mechanism as shown in Fig. 1, the role of manganese of PS II in photoinhibition may be summarized in Fig. 5. In high plant PS II and cyanobacterium Acaryochloris marina, the UV light targets mainly on the manganese cluster and causes subsequently damage of proteins and pigments. In contrast, the visible light aims at different sites: 1) in high plant PSII, the target is the chlorophyll a molecule in the reaction center of PS II, such as primary electron donor P₆₈₀ species; 2) in Acaryochloris marina, the objective of light is on the chlorophyll d molecules in the light harvesting system.

Mn in thermal inactivation of PS II

The thermal inactivation of the photosynthetic reaction center from Rb. Sphaeroides involves at least one intermediate degradation of subunits at elevated temperature, possibly by a reversible transformation between the native and an off-pathway intermediate and followed by a irreversible transformation to the denatured state (Hughes et al., 2006). PS II, like other membrane protein complexes, is unstable upon elevated temperature and undergoes a protein denature reaction. Molecular responses in photosynthesis has been investigated and revealed that the primary targets of thermal damage in plants are the oxygen evolving complexes in PS II (Allakhverdiev et al., 2008). Thermal denaturation of PS II complex was investigated by differential scanning calorimetry (DSC) (Thompson et al., 1986; Thompson et al., 1989). The thermal reaction may involve a reaction of the Mn complex with hydroxide ions, which are oxidized to peroxide or superoxide, and results in the reduction and release of Mn.

Heat inactivation of oxygen evolution by isolated PS II particles is enhanced by depleting chloride ion and exogenous Mn(II) ion (Nash et al., 1985). Weak red light also accelerated heat inactivation. Heat treatment released the 33, 24 and 18 kD proteins and Mn from the Photosystem II particles. Cl^- depletion and exogenous Mn²⁺ stimulated the protein release, and the Mn release was also stimulated by Cl^- depletion. A 50% loss of Mn corresponded to full inactivation of oxygen evolution, whereas no direct correlation seemed to exist between the loss of any one protein and inactivation of oxygen evolution. Removal of the 24 and 18 kD proteins from photosystem II particles only slightly decreased the heat stability of oxygen evolution.

Due to the complexity of PSII, which contains more 20 polypeptides and more than 250 cofactors, the details of thermal disassembly process in PS II is difficult and challenging. To provide novel insights into the structure and mechanisms of the water-oxidation chemistry of the functional PSII model complex, the effect of elevated temperature on the functional PSII model complex, a mixed-valence Mn(III/IV)-oxo dimer compound, [Mn(III)(O)₂Mn(IV)(H₂O)₂(Terpy)₂](NO₃)₃, was investigated over the range of 25 to 85°C by UV-visible absorption spectrometry, atomic absorption spectrometry, oxygen evolution measurements, FTIR, and EPR methodologies (Zhang et al., 2011). The UV-visible spectra of the Mn(III/IV)-oxo dimer at different temperature in the range of 25 °C to 85 °C indicated a decomposition of the compound in two transformation steps. The first step started at 65 °C. The increased absorbance at 400 nm may be attributed to the formation of Mn(IV/IV) species from Mn(III/IV) precursor. The significant increase at 300 nm is likely due to the dissociation of the Terpy ligand from the Mn-oxo dime compound.

Figure 6 shows the EPR spectra of frozen solutions of the Mn(III/IV)-oxo dimer collected over time during the heating process (Zhang et al., 2011). The native Mn compound samples in acetate buffer shows a 16-line signal in the range of 2800-4100 G, which is characteristic for the Mn mix-valence species. When the solution was heated at 75 °C, the 16-line EPR signal was decreased by a factor of 90% within 10 min. This indicates that the Mn(III/IV)-oxo dimer is converted by heating into an EPR silent species, such as Mn(IV/IV)-oxo dimer suggested by the UV-visible spectrophotometric data. The kinetics of the decomposition reaction of Mn(III/IV)-oxo dimer was fit and revealed that the half time of transformation of the Mn(III/IV) dimer was 3.5 min in the first step and 19 min in the following slow step (Fig. 7) (Zhang et al., 2011). Using the Arrhenius plots the activation energies for the two steps were determined to be 68 kJ/mol and 82 kJ/mol, respectively (Zhang et al., 2011). Although the Terpy ligand in the synthetic PS II model is far different from the natural amino acids, the Mn valence and geometry are somewhat similar to the Mn₄CaO₅ cluster in PS II OEC. It is speculated that the thermal denaturation of PS II may be couple with a Mn valence change in the Mn₄CaO₅ center.

X-ray absorption spectroscopy provides structural information on the Mn₄CaO₅ cluster in the oxygen-evolving complex (Dau et al., 2003; Pospísil et al., 2003; Yano and Yachandra, 2008). The effect of temperature on PSII revealed that the target of the temperature jump from 25°C to 47°C is the Mn₄CaO₅ cluster (Pospísil et al., 2003, 2007). One interesting intermediate formed within 10 min of hearing is binuclear Mn unit with Mn(III) ions separated by 2.7Å and connected by one d-μ-oxo bridge (Pospísil et al., 2003). The disassembly of the Mn complex of PSII by a temperature jump from 25°C to 47°C experienced three distinct phases (Fig. 8). First, the oxygen-evolution activity was lost. This phase also involved the release of Ca but the overall structure of Mn complex remained largely intact. Subsequently, two Mn(III) or Mn(IV) ions in the native complex were reduced to Mn(II) and released. The two unreleased Mn ions formed a di-μ-oxo bridged Mn(III/III) dimer complex. Finally, the tightly bound Mn(III/III) unit was slowly reduced and released. The rate constants for each step in the model were determined (Pospísil et al., 2003). These data provide insightful information on the response mechanisms of Manganese in PS II thermal inactivation.

Conclusions

Mn, in the form of Mn₄CaO₅ center, plays a central role in oxygenic photosynthesis as the inorganic core of PS II OEC. In sensing and responding the diverse environmental stress factors, Mn plays an important role in regulating and protecting of photosynthetic machineries. In particular Mn is the primary target of photoinhibition under strong UV light and elevated temperature conditions as documented in this review. The manganese hypothesis may be the dominant mechanism in photoinhibition. However the several details of the mechanism including the nature of the intermediates remain to be elucidated. The first observed fluorescent Mn(IV) species may provide novel insights into the mechanism of the UV-based photoinhibition of photosynthesis. The detailed measurements on synthetic manganese compounds, native PS II complexes, and site-directed mutants of PS II using sophisticate biophysical methodologies including X-ray absorption spectroscopy may provide strong evidence to support or disapproval of the current hypotheses and models in photo-induced and heat-initiated inactivation of PS II OEC in vivo. Such measurements may also offer novel opportunities and open new routes for understanding the mechanisms of assembly of PS II OEC and shed light on solar energy production using artificial photosynthesis.

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