TY - JOUR
AU - Rutherford, A. William
AB - Abstract The Mn4Ca complex that is involved in water oxidation in PSII is affected by near-infrared (NIR) light in certain redox states and these phenomena can be monitored by electron paramagnetic resonance (EPR) at low temperature. Here we report the action spectra of the NIR effects in the S2 and S3 states in PSII from plants and the thermophilic cyanobacterium Thermosynechococcus elongatus. The action spectra obtained are very similar in both S states, indicating the presence of the same photoactive form of the Mn4Ca complex in both states. Since the chemical nature of the photoactive species is not known, an unequivocal interpretation of this result cannot be made; however, it appears to be more easily reconciled with the view that the redox state of the Mn4Ca cluster does not change from the S2 to the S3 transition, at least in those centers sensitive to NIR light. The temperature dependence of the NIR effect and the action spectra for S2 indicate the presence of structural heterogeneity in the Mn4Ca cluster. Introduction The evolution of oxygen as a result of light-driven water oxidation in photosystem II (PSII) is catalyzed by an Mn4Ca cluster that acts both as a device for accumulating oxidizing equivalents and as the active site. During the enzyme cycle, the oxidizing side of PSII goes through five different redox states that are denoted Sn, n varying from 0 to 4. Oxygen is released during the S3 to S0 transition in which S4 is a transient state (Goussias et al. 2002, Rutherford and Boussac 2004). A crystallographic structure of PSII including the Mn4Ca cluster and its amino acid ligands has been reported (Ferreira et al. 2004). The identification of the redox changes on each state of the S state cycle and the redox state of the Mn4Ca cluster are both central to any mechanistic model and yet they remain questions of debate. A key aspect of this debate is whether the S2 to S3 transition represents metal-centered or ligand-based oxidation (Goussias et al. 2002, Sauer and Yachandra 2004). In the S2 state of plant PSII, the Mn4Ca cluster gives rise to several electron paramagnetic resonance (EPR) signals: a so-called multiline signal and signals from at least two different high-spin (ground) states. The multiline signal is centered at g ≈ 2, is spread over roughly 1,800 gauss and is made up of at least 18 lines, each separated by approximately 80 gauss. The multiline signal arises from a magnetic tetramer very probably constituted by three MnIV and one MnIII in which the spin value is spin 1/2 ground state (see Charlot et al. 2005, and references therein). The better known high-spin state from S2 is that giving rise to a signal at around g ≈ 4, and such signals are seen under two different classes of experimental conditions. First, the g ≈ 4 signal can be generated by illumination at room temperature or at 200 K (Zimmermann and Rutherford 1986). The fraction of centers giving rise to this g ≈ 4 signal is dependent on the pre-treatment of the enzyme, being markedly increased by (i) having sucrose present in the medium; (ii) certain treatments that remove chloride from the medium or its replacement by F–, I–, amines or NO3; and (iii) replacing Ca2+ with Sr2+ (reviewed in Boussac et al. 2000). Secondly, the g ≈ 4 signal can also be generated by illumination at 140 K (Casey and Sauer 1984), but this proved to be due to two processes, the formation of the multiline signal due to chlorophyll-based photochemistry followed by the conversion of the multiline state to the g4 state (i.e. the state giving rise to the g ≈ 4 EPR signal) by NIR light (Boussac et al. 1996). This represents an IR-induced spin-state transition in the Mn4Ca cluster, from spin 1/2 to spin ≥5/2 (Boussac et al. 1996, Boussac et al. 1998). Above 170 K, the IR-induced spin 5/2 S2 state converts back into the spin 1/2 S2 multiline state. The g ≈ 4 signals produced under the different conditions (by 200 K illumination of the S1 state vs. NIR illumination of the S2 state) described above have quite different stability in terms of temperature (Boussac and Rutherford 2000). A third type of signal from the S2 state was reported. Signals between g ≈ 5 and g = 10 were found when the spin 1/2 multiline state was illuminated with NIR light below 77 K (Boussac et al. 1998). The new g > 5 signals were attributed to a spin ≥5/2 state (called g10 state in the following) representing a state of the Mn4Ca cluster similar to that giving rise to the g4 state but in a slightly different (unrelaxed) environment. In PSII from Thermosynechococcus elongatus, NIR illumination has similar effects, with the S2 multiline being replaced by EPR features between g = 5 and g = 9, but in this species the g4 state is not formed (Boussac et al. 2000). The S3 state is also affected by NIR light (Ioannidis and Petrouleas 2000). In PSII from plants (Ioannidis and Petrouleas 2000) and T. elongatus (Boussac et al. 2000), NIR illumination at 4 K results in the appearance of signals at g ≈ 5, attributed to a spin 7/2 state (Sanakis et al. 2001) and to a metalloradical signal reminiscent of those observed in Ca2+- or Cl–-depleted PSII (Boussac 1996) or after illumination by visible light at ≈ 10 K in the S1 and S0 states (Nugent et al. 2002, Koulougliotis et al. 2003, Zhang and Styring 2003). The metalloradical signal is usually attributed to TyrZ· interacting magnetically with the Mn4Ca cluster (Peloquin and Britt 2001, see also Mino and Itoh 2005). The action spectra for the spin state changes should reflect the chemical nature of the NIR active species in the Mn cluster. We have previously reported that the conversion of the multiline state into the g4 state showed an absorption maximum at around 820 nm (Boussac et al. 1996). Here, the action spectra and temperature dependence of the NIR effects have been reinvestigated in PSII from both plant and T. elongatus. The action spectrum of the NIR effect in S3 has also been measured and compared with those for S2. Results Fig. 1 shows the EPR spectrum recorded in the S2 state of plant PSII induced by illumination at 200 K (spectrum a). The multiline signal is detected between ≈2,400 and 4,300 gauss. The following features are also present: (i) signals at around 2,230 gauss attributed to the gz resonances of low-spin cytochrome b559 oxidized in a fraction of centers; (ii) signals between 800 and 1,600 gauss from contaminant high-spin Fe3+; (iii) and a signal at around 4,600 gauss (i.e. g = 1.9 and superimposed on the multiline signal) arising from QA–Fe2+. Spectra b and c are the difference spectra recorded after illumination at 120 K with 813 nm light for 1 and 24 min, respectively. Spectra b and c show the effect of the length of 813 nm illumination on the conversion of the multiline signal into either the g10 state (characterized by signals from g = 10 to g ≈ 5) or the g ≈ 4 signal. Fig. 2A shows the kinetics of formation of the g10 (a, squares) and g4 (b, triangles) states when spinach PSII was illuminated with 813 nm light at 120 K together with the fraction of the multiline state that disappeared (c, circles). The amplitude of the g ≈ 4 signal over that of the g = 10 signal is not a constant ratio during the time course of the experiment. These data suggest that the g10 and g4 states formed at 120 K corresponded to two different populations in the starting S2 state that are not in equilibrium at this temperature. Taking this into account, the lines through the points in Fig. 2A were drawn based on the model described in what follows. Because there is no absolute quantification in terms of numbers of spins for the g10 and g4 states, the following procedure was used to plot the data. The maximum amplitude of the multiline that disappeared upon NIR illumination for 24 min was normalized to 1. Then the amplitudes of the g = 10 signal, [g10]t, and g ≈ 4 signal, [g4]t, were each normalized to 1 when t = 24 min. Then, before plotting the data, the three data sets were fitted globally using the following equations (with [g4]t = 24 min = 1, [g10]t = 24 min = 1, [ml]t = 0 min = 1 and α = 1 – β):   \[\ {\alpha}{\times}{[}g_{4}{]}_{t}\ {=}\ (1\ {\mbox{--}}\ exp({\mbox{--}}k_{g4}{\times}t))\ \] (1)   \[\ {\beta}{\times}{[}g10{]}_{t}\ {=}\ (1\ {\mbox{--}}\ exp({\mbox{--}}\ k_{g10}{\times}t))\ \] (2)   \[\ {[}ml{]}_{t}\ {=}\ 1\ {\mbox{--}}\ ({\alpha}{\times}{[}g_{4}{]}_{t}\ {+}\ {\beta}{\times}{[}g_{10}{]}_{t})\ \] (3) The terms [g4]t and [g10]t are the proportions of the amplitude of the g ≈ 4 and g = 10 signals, respectively, formed upon the various periods of illumination; kg4 = 0.25 min–1 and kg10 = 1.10 min–1 are the rate constants for the formation of the g ≈ 4 and g = 10 signals, respectively; α = 0.42 and β = 0.58 are the proportions of centers in which the photoactive multiline state was converted either into the g4 or g10 states, respectively. In Fig. 2B, the relative proportions of the g10 (a, squares) and g4 (b, triangles) states induced as a result of 813 nm illumination and the amount of the S2 multiline signal that disappeared (c, circles) were determined between 30 and 130 K. The maximum decrease in the S2 multiline state occurred at 110 K, [ml]110K. Thus, the ratio [ml]T/[ml]110K corresponds to the efficiency of the 813 nm illumination vs. the temperature. The maximum amount of the g4 state was formed at 130 K and the maximum of the g10 state was formed between 50 and 90 K. Again, because we had no absolute quantification of the number of spins for the g ≈ 4 and g = 10 signals, we used the following expression to plot the data:   \[\ {[}ml{]}_{T}/{[}ml{]}_{110{\ }K}\ {=}\ {\gamma}{\times}({[}g_{4}{]}_{T}/{[}g_{4}{]}_{130{\ }K})\ {+}\ {\varepsilon}{\times}({[}g_{10}{]}_{T}/{[}g_{10}{]}_{70{\ }K})\ \] (4) where the terms [g4]130 K and [g10]70 K are the amplitudes of the maximum amount of the g ≈ 4 and g = 10 signals which could be formed at 130 and 70 K respectively, and [g4]T and [g10]T are the amplitude of the g ≈ 4 and g = 10 signals formed at the temperature T, and γ and ε are scaling factors. The fitted curve for [ml]T/[ml]110 K vs. the temperature (crosses) was obtained with γ = 0.38 and ε = 0.76. Fig. 3 shows the action spectrum for the formation of the g10 state (a, squares) and for the formation of the g4 state (b, triangles) together with that for the disappearance of the multiline state (c, open circles). This was obtained at 120 K, a temperature where both the g4 and g10 states are NIR induced (see Fig. 2). Arbitrarily, the time chosen for the NIR illumination was that required to induce half of the effect on the multiline signal at 120 K and at 820 nm (with interference filters). As expected, spectrum c can be reproduced by combining spectra a and b with appropriate scaling factors (full circles). Spectra a and b are similar but not identical. At 120 K, the action spectrum for the formation of the g10 state shows a maximum at ≈ 800 nm and is broader than that for the formation of the g4 state which has a maximum at ≈ 760 nm. In Fig. 4, the effect of temperature on the action spectrum for the formation of the g10 state was investigated. This transition was chosen because (i) it occurs from 30 to 120 K; and (ii) the results from plant PSII can be compared with those from T. elongatus PSII in which the g4 state is not induced by NIR illumination (only the g9 state analogous to the g10 state in plant PSII is induced by NIR light). Fig. 4A shows the action spectrum for the formation of the g10 state measured in PSII from spinach at 120 K (open squares) and at 45 K (filled squares). Fig. 4B shows the equivalent data for T. elongatus at 120 K (open diamonds) and at 45 K (filled diamond). In both species, increasing the temperature increased the width of the spectra. This results in a shift of the maximum from 760 nm at 45 K to ≈ 790 nm at 120 K. In Ca2+-depleted, EGTA-treated PSII from plants, NIR illumination resulted only in a g4 state (Boussac et al. 1996), and the corresponding action spectrum showed a relatively narrow peak at 760 nm (Fig. 5). The EPR spectrum of the NIR-induced state in the S3 state of PSII from T. elongatus (Boussac et al. 2000) is similar to that originally observed in PSII from plants (Ioannidis and Petrouleas 2000) (Fig. 6). Quantification of the field swept electron spin echo spectrum of the metalloradical signal generated by NIR illumination indicated that this involved ≈20% of the centers (not shown). Fig. 7 shows the action spectrum of this NIR effect in PSII from T. elongatus at 45 K (open diamonds). For comparison, the action spectrum for the formation of the g9 signal in S2 at 45 K is also re-plotted (filled diamonds). Discussion The action spectra for the NIR effect in S2 and S3 are remarkably similar. This seems to imply that the same photoactive state of the Mn4Ca cluster is present in both S states. If the Mn4Ca cluster is tetrameric in terms of its electronic structure, a situation supported by spectroscopic and crystallographic evidence, then the Mn tetramer itself would constitute the NIR-sensitive state. If so, the current data would appear to indicate that the Mn4Ca cluster does not undergo a valence change on the S2 to S3 transition, at least in the fraction of centers that are photoactive. For recent papers in this on-going debate, see Dau et al. (2001), Sauer and Yachandra (2004), Haumann et al. (2005) and, for a review, see Goussias et al. (2002). If, on the other hand, the cluster can be considered as having electronically distinct elements, it may be possible that the valence of the Mn cluster could change without necessarily changing the action spectrum of the photoactive species. The current structural and magnetic model for the Mn cluster is a ‘3+1’ structure (Peloquin and Britt 2001, Ferreira et al. 2004, Sauer and Yachandra 2004). Recently, a Y-shaped 4J-coupling scheme has been proposed to reproduce the spin densities of the MnIIIMn3IVCa cluster in the multiline state. All the required criteria such as a spin 1/2 ground state with a low lying excited spin state (30 cm–1) and an easy conversion to a spin ≥ 5/2 system responsible for the g = 4.1 EPR signals were shown to be satisfied with four antiferromagnetic interactions (Charlot et al. 2005). In such a model, IR light would affect the position of the MnIII in the Y-shaped structure. Other suggestions for the chemical origin of the NIR effects include: (i) excitation of an MnaIII and MnbIV intervalence band resulting in MnaIV and MnbIII with possibly a change in the sign of one coupling between two of the four Mn ions (Peloquin and Britt 2001); (ii) excitation of a dd transition in an MnIII ion (dz2→dx2–y2) (Baxter et al. 1999, Smith et al. 2002); and (iii) conversion of the high spin state (S = 2) of MnIII into its low spin state (S = 1), with a double exchange mechanism between the spin 3/2 MnIV and the spin 1 MnIII. If any of these explanations is correct and if the valence of the Mn4Ca cluster in S2 is MnIIIMn3IV, as suggested from several lines of evidence (see for example Charlot et al. 2005, Kulik et al. 2005, Peloquin and Britt 2001, Sauer and Yachandra 2004, see however Carrell et al. 2002), then this would imply that MnIII is present in both S2 and S3. Then this would be a further argument against Mn oxidation on the S2 to S3 transition in the fraction of centers that are photoactive in the IR range. The NIR effects in S2 show additional complexity compared with the previous model (Boussac et al. 1998) where the g10 state represented a high energy state separated from the lower energy g4 state by an activation barrier. The present data indicate that while this occurs in some centers, in other centers the g4 state is formed without a stable g10 intermediate. This indicates the presence of two subpopulations of the Mn4Ca cluster, both susceptible to NIR light and both giving a multiline signal, reflecting some kind of frozen-in structural equilibrium. The action spectra for the NIR effect in S2 is slightly different from that reported earlier. Part of this difference is due to their temperature dependence, broadening and shifting to longer wavelength at higher temperatures. This could indicate a structural distribution in the photoactive species so that the longer wavelength absorption results in reversible photochemistry unless a process involving thermal energy occurs allowing the stable product to be formed. Materials and Methods O2-evolving PSII samples from spinach and T. elongatus were prepared as previously described (Boussac et al. 1996, Boussac et al. 2000). After dark adaptation for 1 h at 0°C for PSII from spinach and at room temperature for PSII from T. elongatus, 1 mM phenyl-p-benzoquinone dissolved in ethanol (95%) was added to the sample as an electron acceptor. Then, formation of the S2 state was achieved by illumination at 200 K as previously described (Boussac et al. 1996, Horner et al. 1998). Formation of the S3 state in PSII samples from T. elongatus was done using laser flashes at room temperature as previously described (Boussac et al. 2000). The temperature was controlled with an RhFe probe (Oxford Instruments). NIR illumination was provided either by a laser diode emitting at 813 nm (Coherent, diode S-81-1000C) (Fig. 1, 2) or by a 1,000 W tungsten lamp filtered through band-pass filters (bandwith ≈ 3 nm, Pomfret Research Optics Inc.) (Fig. 3–6). NIR illumination of the samples was done between 130 and 30 K in the EPR cavity. Light intensity, for experiments reported in Figures 1 and 2, was adjusted so that the kinetics could be resolved. In Fig. 3–6, the light intensity was adjusted for each filter so that the same energy was received by the samples at all wavelengths. This adjustment from filter to filter corresponded to <10% of the average energy measured for all filters and agreed with values obtained from the transmittance of the filters measured independently. EPR spectra at 9.42 GHz were recorded at 8 K with a Bruker ESP300 X-band spectrometer equipped with an Oxford Instruments cryostat with a microwave power of 20 mW, a modulation amplitude of 25 gauss and a modulation frequency of 100 kHz. View largeDownload slide Fig. 1 EPR spectrum (a) recorded in the S2 state of spinach PSII induced by a 200 K illumination. Spectra (b) and (c) correspond to the difference spectra after minus before 813 nm illumination for either 1 or 24 min at 120 K, respectively. Instrument settings: temperature, 9 K; microwave power, 20 mW; modulation amplitude, 25 gauss; microwave frequency, 9.4 GHz; modulation frequency, 100 kHz. The central part of the spectra corresponding to the TyrD· region was deleted. View largeDownload slide Fig. 1 EPR spectrum (a) recorded in the S2 state of spinach PSII induced by a 200 K illumination. Spectra (b) and (c) correspond to the difference spectra after minus before 813 nm illumination for either 1 or 24 min at 120 K, respectively. Instrument settings: temperature, 9 K; microwave power, 20 mW; modulation amplitude, 25 gauss; microwave frequency, 9.4 GHz; modulation frequency, 100 kHz. The central part of the spectra corresponding to the TyrD· region was deleted. View largeDownload slide Fig. 2 Yield of formation of the g10 state (a, open square) and g4 state (b, open triangle) together with the proportion of the multiline state which disappeared (c, open circle) in PSII from spinach vs. the time of illumination at 813 nm at 120 K (A). Yield of formation of the g10 state (a, open square) and g4 state (b, open triangle) together with the proportion of the multiline state which disappeared (c, open circle) in PSII from spinach vs. the temperature at which the sample was illuminated after 813 nm illumination for 24 min (B). Data were plotted as described in the text and the curves through the points result from the fitting procedures by using Equations 1 to 4. View largeDownload slide Fig. 2 Yield of formation of the g10 state (a, open square) and g4 state (b, open triangle) together with the proportion of the multiline state which disappeared (c, open circle) in PSII from spinach vs. the time of illumination at 813 nm at 120 K (A). Yield of formation of the g10 state (a, open square) and g4 state (b, open triangle) together with the proportion of the multiline state which disappeared (c, open circle) in PSII from spinach vs. the temperature at which the sample was illuminated after 813 nm illumination for 24 min (B). Data were plotted as described in the text and the curves through the points result from the fitting procedures by using Equations 1 to 4. View largeDownload slide Fig. 3 Action spectra of the formation of the g10 state (a, open square) and g4 state (b, open triangle) and of disappearance of the multiline state (c, open circle) in PSII from spinach upon illumination at 813 nm at 120 K. The maximum amplitude of spectrum c was normalized to 1. Filled circles result from the fitting procedure described in the text by using Equation 4. View largeDownload slide Fig. 3 Action spectra of the formation of the g10 state (a, open square) and g4 state (b, open triangle) and of disappearance of the multiline state (c, open circle) in PSII from spinach upon illumination at 813 nm at 120 K. The maximum amplitude of spectrum c was normalized to 1. Filled circles result from the fitting procedure described in the text by using Equation 4. View largeDownload slide Fig. 4 Action spectrum of the formation of the g10 state in PSII from spinach (A) or of the formation of the g9 state in PSII from T. elongatus (B) measured either at 45 K (filled symbols) or at 120 K (open symbols).The maximum amplitude of the spectra was arbitrarily normalized to 1. View largeDownload slide Fig. 4 Action spectrum of the formation of the g10 state in PSII from spinach (A) or of the formation of the g9 state in PSII from T. elongatus (B) measured either at 45 K (filled symbols) or at 120 K (open symbols).The maximum amplitude of the spectra was arbitrarily normalized to 1. View largeDownload slide Fig. 5 Action spectrum of the formation of the g4 state at 90 K in Ca2+-depleted, EGTA-treated PSII from spinach. The maximum amplitude of the spectra was arbitrarily normalized to 1. View largeDownload slide Fig. 5 Action spectrum of the formation of the g4 state at 90 K in Ca2+-depleted, EGTA-treated PSII from spinach. The maximum amplitude of the spectra was arbitrarily normalized to 1. View largeDownload slide Fig. 6 EPR spectrum recorded in the S3 state of PSII from T. elongatus (a, thin line). Spectrum (b) (thick line) was recorded after an additional illumination at 813 nm at 50 K in the EPR cavity for 2 min. Instrument settings: temperature, 4.2 K; microwave power, 20 mW; modulation amplitude, 12.5 gauss; microwave frequency, 9.4 GHz; modulation frequency, 100 kHz. The central part of the spectra corresponding to the TyrD• region was deleted. View largeDownload slide Fig. 6 EPR spectrum recorded in the S3 state of PSII from T. elongatus (a, thin line). Spectrum (b) (thick line) was recorded after an additional illumination at 813 nm at 50 K in the EPR cavity for 2 min. Instrument settings: temperature, 4.2 K; microwave power, 20 mW; modulation amplitude, 12.5 gauss; microwave frequency, 9.4 GHz; modulation frequency, 100 kHz. The central part of the spectra corresponding to the TyrD• region was deleted. View largeDownload slide Fig. 7 Action spectra at 45 K in PSII from T. elongatus of the formation of the g9 state in the S2 state (filled diamonds) and of the formation of the split signal in the S3 state (open diamonds).The maximum amplitude of the spectra was normalized to 1. View largeDownload slide Fig. 7 Action spectra at 45 K in PSII from T. elongatus of the formation of the g9 state in the S2 state (filled diamonds) and of the formation of the split signal in the S3 state (open diamonds).The maximum amplitude of the spectra was normalized to 1. Abbreviations EPR electron paramagnetic resonance IR infrared NIR near-infrared PPBQ phenyl-p-benzoquinone TyrZ the tyrosine acting as the electron donor to P680+ References Baxter, R., Krausz, E., Wydrzynski, T. and Pace, R.J. ( 1999) Identification of the near-infrared absorption band from the Mn cluster of photosystem II. J. Amer. Chem. 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TI - Near-infrared-induced Transitions in the Manganese Cluster of Photosystem II: Action Spectra for the S2 and S3 Redox States
JO - Plant and Cell Physiology
DO - 10.1093/pcp/pci088
DA - 2005-06-01
UR - https://www.deepdyve.com/lp/oxford-university-press/near-infrared-induced-transitions-in-the-manganese-cluster-of-DwmeNFCkZp
SP - 837
EP - 842
VL - 46
IS - 6
DP - DeepDyve
ER -