Photosystem II (PSII) in plants and cyanobacteria performs light-driven water oxidation to obtain electrons necessary for CO2 fixation. In PSII, a series of electron transfer reactions take place from the Mn4CaO5 cluster, the catalytic site of water oxidation, to a plastoquinone molecule via several redox cofactors. Light-induced Fourier transform infrared (FTIR) difference spectroscopy has been extensively used to investigate the structures and reactions of the redox cofactors in PSII. Recently, FTIR spectroelectrochemistry combined with the light-induced difference technique was applied to study the mechanism of electron-transfer regulation in PSII involving the quinone electron acceptors, QA and QB, and the non-heme iron that bridges them. In this mini-review, this combined FTIR method is introduced, and obtained results about the redox reactions of the non-heme iron and QB, involving the long-range interaction of the Mn4CaO5 cluster with the electron-acceptor side, are summarized.
Photosystem II (PSII), one of the major protein complexes that work in oxygenic photosynthesis, has a unique function of light-induced water oxidation . Electrons from water are ultimately used for CO2 reduction and released protons generate a proton gradient across the thylakoid membrane to synthesize ATP. In addition, molecular oxygen, a byproduct of water oxidation, makes an oxygenic atmosphere, which is essential for sustenance of life on the earth. In photosystem II, light absorption triggers charge separation between the chlorophyll dimer (P680) and the pheophytin (Pheo) electron acceptor to produce P680+Pheo− . On the electron-acceptor side, an electron on Pheo− is transferred to the primary quionone electron acceptor (QA) and then to the secondary quinone electron acceptor (QB) [16,38,48], while on the electron donor side, the electron hole on P680+ is transferred to the redox-active tyrosine (YZ) then to the Mn4CaO5 cluster, at which water oxidation takes place via a cycle of five intermediates called states () (Fig. 1) [23,36,52]. QA and QB both consist of a plastoquinone-9 (PQ) molecule and are structurally linked by a non-heme iron though His ligands (D2-His214 and D1-His215) (Fig. 1) [18,21,63]. In spite of the same chemical species and similar molecular interactions, QA and QB have rather different functions [16,38,48]; QA performs only a single-electron reaction and relays an electron from Pheo− to QB, whereas QB can be doubly reduced to become plastoquinole (PQH2) by binding two protons and leaves the binding site of PSII.
The electron transfer reaction between QA and QB is controlled by the gap of their redox potentials (). A larger provides a driving force to promote an efficient forward electron transfer from QA to QB, whereas a smaller or negative promotes a backward electron transfer. The backward electron transfer, which seems non-productive in photosynthesis, also plays an important role in the photoprotection mechanism [10,54,66]. The value between QA and QB, however, has not been determined exactly and only indirectly predicted from kinetic and thermodynamic data [12,15,53]. The value of QA, , has been extensively estimated using chemical and electrochemical titration and determined to be approximately −100 mV in oxygen-evolving intact PSII [1,24,26,30,31,56,57]. In contrast, the of QB, , has not been directly measured mainly because of the absence of spectroscopic methods that provide specific QB signals. It has also been demonstrated that the value is shifted by about +150 mV by depletion of the Mn4CaO5 cluster from PSII [1,24,26,30,31,56,57]. This phenomena was argued in the context of a photoprotection mechanisms, in which when the Mn4CaO5 cluster is inactivated, the electron on the quinone electron acceptors is thermally relaxed by direct recombination with P680+ [10,26,32,54,65,66]. However, the effect of inactivation of the Mn4CaO5 cluster on the of QB in addition to its absolute value in intact PSII was still unknown. Therefore, the full mechanism of photoprotection by regulation of the electron transfer between QA and QB has not been established. Another important question here is how inactivation of the Mn4CaO5 cluster influences the through the long distance of about 40 Å between the Mn4CaO5 cluster and QA. A possible hypothesis for this long-range interaction is that the structural change on the electron-donor side by Mn depletion is transferred to the QB site through the transmembrane helices of the D1 subunit and then to the QA site via the molecular bridge of the non-heme iron [10,28,31]. If this were the case, the donor-side perturbation would influence the redox properties of the non-heme iron and QB as well as .
Light-induced Fourier transform infrared (FTIR) difference spectroscopy has been extensively used to investigate the structures and reactions of the redox cofactors in PSII [5,11,13,14,39–43]. In this method, photoreactions are initiated by illumination of continuous-wave light or flashes from a pulse laser, and the structural changes of the cofactors and surrounding protein moieties are studied by detecting small infrared absorption changes. On the other hand, an FTIR spectroelectrochemical method has been used to investigate redox reactions of biomolecules and proteins [3,6,7,20,34,35,37]. In these studies, the redox reactions were triggered by changing the electrode potential and FTIR difference spectra were measured. Spectroelectrochemistry utilizing UV-Vis and fluorescence spectroscopies has been used to determine the values of redox cofactors [17,29,56–58]. The merit of FTIR spectroelectrochemistry over such conventional methods is that it provides additional information of structural changes coupled to the redox reactions. In this mini-review, we introduce our recent approaches using FTIR spectroelectrochemistry combined with light-induced FTIR difference technique to investigate the redox and structural properties of the non-heme iron and [27,28]. In particular, the of QB was directly measured for the first time using FTIR signals specific to . The results provided a clear view on the regulation mechanism of electron transfer in PSII upon inactivation of the Mn4CaO5 cluster and an insight into the long-range interaction between the electron donor and acceptor sides of the PSII protein complex.
2.Instrumental setup of FTIR spectroelectrochemistry combined with light-induced FTIR difference spectroscopy
Figure 2A shows a schematic view of an optically transparent thin-layer electrode (OTTLE) cell used in our FTIR spectroelectrochemical measurements. This cell is similar to the ones previously reported [7,37]. Because strong infrared absorption of water interferes with the bands of proteins, a very thin-layer metal mesh, for example 6 µm in thickness, is used as a working electrode. When an Au working electrode is used, the surface of the electrode is modified with thiols to prevent irreversible adsorption and denaturation of proteins . A commercially obtained Ag/AgCl/3 M KCl reference electrode (Cypress Systems Inc., 66-EE009; +208 mV vs. SHE) with a diameter of 2 mm and a Pt black wire as a counter electrode are arranged in the Teflon body (Fig. 2A).
Because redox cofactors located inside a protein are difficult to interact with an electrode directly, redox mediators are necessary for electrochemical measurements. Several mediators are used to cover the potential regions of target cofactors. For example, for the measurement of the non-heme iron in PSII, Ru(NH3)6Cl2 (), K3Fe(CN)6 (), and ferreocenylmethyl trimetyl ammonium () were used , while for QB, 1-methoxy-5-methylphanazinium methosulfate (methoxy-PMS; ), N,N,N′,N′-tetramethyl-p-phenylenediamine (TMPD; ), and K3Fe(CN)6 () were used . A sample containing the mediators is sandwiched between a pair of CaF2 plates together with an Au mesh. The interspace between the CaF2 plates and the Teflon body is filled with a buffer solution containing mediators to achieve an electric contact between the working electrode and the counter and reference electrodes.
For photosensitive proteins like PSII, there is a merit to combine the spectroelectrochemistry and a light-induced difference technique for studies of redox cofactors. The values for the redox reactions of cofactors in PSII are very small, usually in the level of 10−5–10−4 [5,11,13,14,39–43], and hence electrochemically-induced FTIR difference spectra of the redox cofactors are not easy to measure with a high quality due to baseline changes during the period in which a redox equilibrium is reached (sometimes tens of minutes). In contrast, high-quality difference spectra can be obtained by utilizing the light-induced difference method for a sample that is equilibrated at a certain redox potential controlled by a potentiostat. Using this combined FTIR method of spectroelectrochemistry and light-induced difference spectroscopy, the redox properties like values and the structural changes upon redox reactions are obtained simultaneously.
For light-induced FTIR difference measurements of electrochemically controlled samples, the OTTLE cell wired with a potentiostat is set in the sample room of FTIR spectrophotometer (Fig. 2B), and light illumination is performed, for example by flashes from a Q-switched Nd:YAG laser (532 nm; ∼7 ns width), which are synchronized to FTIR scans by triggers from the spectrophotometer . The temperature of the OTTLE cell is controlled by circulating cold water in a copper holder. Details of the methodology of light-induced FTIR difference spectroscopy and application to PSII have been described in previous review articles [5,11,13,14,39–43].
3.FTIR spectroelectrochemical study on the non-heme iron
The non-heme iron connects QA and QB by a molecular bridge, QA-His214(D2)-Fe-His215(D1)-QB (Fig. 1) [18,21,63]. In addition to these His ligands, other two His residues, D1-His272 and D2-His268, and a bicarbonate ion function as ligands to the non-heme iron [18,21,63]. Under physiological conditions, the non-heme iron is not involved in the electron transfer reaction from QA to QB [16,38,48], because of its high value of about +400 mV at pH 7.0 with a pH dependence of −60 mV/pH [8,25,44,49]. However, under oxidative conditions, e.g., in the presence of ferricyanide, the non-heme iron is oxidized to Fe3+ and serves as an endogenous electron acceptor, and hence Fe3+ is re-reduced to Fe2+ by light illumination. This photoreaction allows the measurement of a light-induced FTIR difference spectrum of the non-heme iron to investigate the structures of the nearby protein moieties involving the QB binding site [4,22,44,60,61]. Utilizing the light-induced Fe2+/Fe3+ measurement in combination with the spectroelectrochemical method, we recently studied the effects of the depletion of the Mn4CaO5 cluster on the redox and structural properties of the non-heme iron .
Figure 3 shows flash-induced FTIR difference spectra of the O2-evolving (a, black line) and Mn-depleted (c, red line) PSII membranes of spinach at pH 6.5 measured in an electrolytic solution at +600 mV (vs. SHE) . Bands at 1339, 1258, 1229, 1109, and 1101 cm−1, which were observed in both spectra, are typical of the Fe2+/Fe3+ difference signals [4,22,44,60,61]. The 1339(+)/1229(−) cm−1 bands were attributed to the symmetric CO stretching vibrations of the bicarbonate ligand , while the positive band at 1258 cm−1 and a part of the 1229 cm−1 negative band were assigned to the CO stretching vibration of a Tyr side chain (either D1-Tyr246 or D2-Tyr244) structurally coupled to the non-heme iron using [4-13C]Tyr labeling . In addition, the 1109(+)/1101(−) peaks were assigned to the CN stretching vibrations of the imidazole ring of the His ligands . In the difference spectrum of intact PSII, signals were also observed at 1439, 1419, 1404 and 1365 cm−1, which arise from the transition from the dark-stable state to the state in the Mn4CaO5 cluster [11,13,14,39–43]. Indeed, a spectrum of intact PSII measured at pH 5.5 at +430 mV, which reflects a pure difference without the contribution of the electron-acceptor side in PSII (Fig. 3a, green line), showed the same signals. These bands were assigned to the symmetric stretching vibrations of carboxylate groups surrounding the Mn4CaO5 cluster [45,46]. Because there are some minor peaks in the difference spectrum overlapping the non-heme iron signals (e.g., bands at 1260/1244 and 1113 cm−1), the spectrum (Fig. 3a, green line) was subtracted from the difference spectrum (Fig. 3a, black line) to estimate the pure contribution of Fe2+/Fe3+ signals in intact PSII (Fig. 3b).
From the intensities of the major signals around 1240 cm−1 in the thus-obtained Fe2+/Fe3+ spectra at a series of electrode potentials between +350 and +600 mV (Fig. 4A), the molar ratios of Fe3+ and Fe2+ were estimated and analyzed in a semilogarithmic Nernst plot (Fig. 4B) . A linear relationship with slopes of 65 and 62 mV was obtained for the intact and Mn-depleted PSII samples, respectively; These slopes are similar to the theoretical value of 56 mV at 10°C (measuring temperature). The data from both PSII samples well followed the theoretical one-electron Nernstian curves (Fig. 4C), and the values were determined to be +468 ± 3 and +486 ± 4 mV for intact and Mn-depleted PSII samples, respectively . Thus, the FTIR spectroelectrochemical measurements revealed that Mn depletion induces a relatively small shift of by +18 mV . This value is about ∼8 times smaller than the shift of ( [1,24,26,30,31,56,57]).
The Fe2+/Fe3+ difference spectra also showed some changes in the COOH and His CN regions upon Mn depletion (Fig. 5). A negative peak at 1750 cm−1 was observed in the region of the C=O stretching vibration of COOH in intact PSII, whereas this band was not detected in Mn-depleted PSII (Fig. 5A). It was suggested that the of a COOH group near the non-heme iron is upshifted upon Mn depletion . One of several Glu residues (D1-Glu226, D1-Glu242, D1-Glu243, D1-Glu244, D2-Glu241, and D2-Glu242) located on the stromal side will be responsible for this band; The best candidate is D1-Glu244 that is coupled to the non-heme iron through bicarbonate (Fig. 1). In the His CN region, two negative peaks were observed at 1102 and 1093 cm−1 in intact PSII, whereas the lower-frequency peak diminished upon Mn depletion (Fig. 5B). This peak has been assigned to the deprotonated anion form of His, most probably D1-His215 interacting QB [4,22]. Thus, it was suggested that the of D1-His215 increased upon Mn depletion. These changes of the Glu and His residues as well as a small shift of by Mn depletion should results from the long-range interaction between the electron-donor and acceptor sides of PSII.
4.FTIR spectroelectrochemical study on QB
In contrast to many reports of the measurement of of QA [1,24,26,30,31,56,57], there has been no report of direct measurement of of QB. The main reason for this is the difficulty in spectroscopic detection of the QB reaction. It is well known that fluorescence measurement is useful to monitor the redox states of QA because reduction of QA increases the level of fluorescence [9,33,47,48]. However, the fluorescence method is not applicable to the QB reaction. Although UV-Vis absorption and electron spin resonance have also been applied to the redox titration of QA (summarized in ), these spectroscopic methods have not been used in QB titration probably due to the similar signals of and [19,50,55,64]. On the other hand, it was shown that FTIR difference spectroscopy provided signals specific to the QA and QB reactions ; A sharp positive peak was observed at 1721 and 1745 cm−1 in the and difference spectra, respectively (Fig. 6A, B). These peaks were assigned to the 132-ester C=O vibrations of nearby Pheo molecules (PheoD1 and PheoD2 for QA and QB, respectively; Fig. 6C), which are affected by reduction of the quinone electron acceptors . The frequency of the 1721 cm−1 peak in the spectrum lower than that of the 1745 cm−1 peak in the spectrum is consistent with the presence of a hydrogen bond at the 132-ester C=O of PheoD1 with D1-Tyr126 (Fig. 6C) [18,21,63]; The corresponding residue on the D2 side is D2-Phe125, which does not form a hydrogen bond with PheoD2. These peaks at 1721 and 1745 cm−1 are thus good markers to discriminate the QA and QB reactions.
This marker peak of QB at 1745 cm−1 was used to examine the redox state of QB at a series of the electrode potentials (Fig. 7A) . Note that in this method, the QB signal is obtained as a light-induced change of QB, typically one electron reduction of QB, after reaching equilibrium of electrochemical reactions, and hence electrochemically-induced changes are not directly detected in FTIR spectra. The semilogarithmic Nernst plots of the relative intensities of this peak against the electrode potential (Fig. 7B) showed virtually linear relationships with slopes of 30 ± 2 and 39 ± 1 mV for intact and Mn-depleted PSII, respectively. These slopes are closer to 28 mV, the theoretical value of a two-electron reaction at 10°C (measurement temperature), than 56 mV, that of a one-electron reaction. The apparent redox potentials () were obtained from the intercepts of the plots to be +155 and +132 mV for intact and Mn-depleted PSII, respectively (Fig. 7B). The data closer to a two-electron reaction indicates that the redox potential of the second reduction of QB, , is higher than that of the first reduction, , and hence that QB was electrochemically doubly reduced to PQH2 without forming singly reduced as a major component. However, an ideal two-electron process with the slope value of 28 mV is realized unless is at least 180 mV more negative than  (see also SI in ). Thermodynamic simulation of the experimental Nernst plots with and as fitting parameters (Fig. 7C) yielded the following values at pH 6.5: and for intact PSII; and for Mn-depleted PSII. These are the values of QB directly measured for the first time (to our knowledge).
By determining the values of QB in intact and Mn-deleted PSII samples, the mechanism of photoprotection when the Mn4CaO5 cluster is inactivated is now clear (Fig. 8). The together with the reported (approximately −100 mV [1,24,26,30,31,56,57]) provided the between QA and QB as approximately 190 mV in intact PSII . Mn depletion induces a negative shift of by only 6 mV , which is in sharp contrast to a large positive shift () of by the same treatment [1,24,26,30,31,56,57]. Thus, for the first reduction of QB in intact PSII decreases to ∼40 mV (Fig. 8B). This large decrease in plays a significant role in photoprotection. The decrease accelerates backward electron transfer from to QA to facilitate direct charge recombination of with P680+, preventing oxidative damage by P680+ [10,54]. In addition, the large positive shift of increases between PheoD1 and QA and hence prevents charge recombination via PheoD1−, which otherwise leads to generation of harmful singlet oxygen via a chlorophyll triplet state [10,26,32,54,65,66].
The combined method of thin-layer electrochemistry and light-induced FTIR difference spectroscopy was applied to study the redox properties of the non-heme iron and the terminal quinone QB on the electron-acceptor side of PSII. In particular, the FTIR signal specific to QB reduction enabled the first direct measurement of the of QB , which has not been achieved by other spectroscopic methods. This success demonstrated that this combined FTIR method is a very powerful tool to investigate redox reactions in photosensitive proteins. The determination of and its shift upon depletion of the Mn4CaO5 cluster showed a clear view of electron transfer regulation in PSII (Fig. 8), which functions as a photoprotection mechanism when the Mn4CaO5 cluster is impaired. Another merit of FTIR spectroelectrochemistry is that structural information can be obtained in addition to the redox property. It was shown that Mn depletion affected the protonation states of amino acid residues near the non-heme iron, which may cause the shift of the .
Although the mechanism of electron transfer regulation in PSII was clarified by determination of the of QB, the molecular mechanism of the long-range interaction between the Mn4CaO5 cluster on the electron-donor side and the quinone molecules on the electron-acceptor side remains unclear. First it was predicted that the structural change by Mn depletion is transferred to the QB site via the membrane-spanning helices of the D1 protein and then to QA via the non-heme iron bridge (Fig. 1) , resulting in a large shift by +150 mV. However, this prediction was not consistent with the observations of relatively small shifts of and (+6 and +18 mV, respectively) upon Mn depletion (Figs 4 and 7) . Thus, there could be other pathways of long-range interaction to affect without using the α-helices of the D1 protein. Meanwhile, it was suggested that the of a Glu residue near the non-heme iron is changed upon Mn depletion . It is possible that such a Glu residue together with other several Glu residues located on the stromal side of PSII electrostatically controls the by changing the protonation state. Further FTIR studies using spectroelectrochemical and light-induced difference methods in combination with site-directed mutagenesis at these amino acid residues are necessary to clarify the whole mechanism of electron transfer regulation and the donor- and acceptor-side communication in PSII.
This study was supported by JSPS KAKENHI (25410009 to Y.K., 24000018, 24107003, and 25291033 to T.N.).
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