Comparative Analysis of the Interaction of the ... - ACS Publications

Nov 7, 2016 - in Intact and Mn-Depleted Photosystem II Membranes Using Light-. Induced ATR-FTIR ... primary quinone QA shifts by approximately +150 mV...
0 downloads 0 Views 467KB Size
Subscriber access provided by University of Otago Library

Rapid Report

Comparative analysis of the interaction of the primary quinone Q in intact and Mn-depleted photosystem II membranes using light-induced ATR-FTIR spectroscopy A

Yuki Kato, Rina Ishii, and Takumi Noguchi Biochemistry, Just Accepted Manuscript • DOI: 10.1021/acs.biochem.6b01052 • Publication Date (Web): 07 Nov 2016 Downloaded from http://pubs.acs.org on November 10, 2016

Just Accepted “Just Accepted” manuscripts have been peer-reviewed and accepted for publication. They are posted online prior to technical editing, formatting for publication and author proofing. The American Chemical Society provides “Just Accepted” as a free service to the research community to expedite the dissemination of scientific material as soon as possible after acceptance. “Just Accepted” manuscripts appear in full in PDF format accompanied by an HTML abstract. “Just Accepted” manuscripts have been fully peer reviewed, but should not be considered the official version of record. They are accessible to all readers and citable by the Digital Object Identifier (DOI®). “Just Accepted” is an optional service offered to authors. Therefore, the “Just Accepted” Web site may not include all articles that will be published in the journal. After a manuscript is technically edited and formatted, it will be removed from the “Just Accepted” Web site and published as an ASAP article. Note that technical editing may introduce minor changes to the manuscript text and/or graphics which could affect content, and all legal disclaimers and ethical guidelines that apply to the journal pertain. ACS cannot be held responsible for errors or consequences arising from the use of information contained in these “Just Accepted” manuscripts.

Biochemistry is published by the American Chemical Society. 1155 Sixteenth Street N.W., Washington, DC 20036 Published by American Chemical Society. Copyright © American Chemical Society. However, no copyright claim is made to original U.S. Government works, or works produced by employees of any Commonwealth realm Crown government in the course of their duties.

Page 1 of 5

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

Biochemistry

Comparative analysis of the interaction of the primary quinone QA in intact and Mn-depleted photosystem II membranes using lightinduced ATR-FTIR spectroscopy Yuki Kato*, Rina Ishii, and Takumi Noguchi* Division of Material Science, Graduate School of Science, Nagoya University, Furo-cho, Chikusa-ku, Nagoya 464-8602, Japan Supporting Information Placeholder This Em decrease suppresses forward electron transfer from QA− to QB, as demonstrated by fluorescence kinetics measurements,19 and promotes backward electron transfer. Because the positive Em(QA−/QA) shift increases Em between Pheo and QA, direct charge recombination between QA− and P680+ is facilitated, preventing oxidative damage by P680+ as a strong oxidant.3,4,8-10 By contrast, indirect recombination via P680+Pheo−, which forms a chlorophyll triplet state, a precursor of harmful singlet oxygen, is prevented.3,4,8-10 In spite of clear observations of the Em(QA−/QA) shift by the impairment of the Mn4CaO5 cluster,10-16 its molecular mechanism remains poorly understood.3 Because the distance between the Mn4CaO5 cluster and QA is about 40 Å, a direct interaction between them is unlikely to influence the Em(QA−/QA). It is possible that the perturbation of the Mn4CaO5 cluster site propagates to the QA site through the membrane spanning helices and induces its structural modification.3,11,18,20 In addition to the mechanism of such structural propagation, factors to induce the Em(QA−/QA) shift by ~+150 mV remain unclear. A previous theoretical calculation21 predicted that additional H-bond formation by D2-Thr217 to the CO group of QA− leads to the positive Em(QA−/QA) shift. A light-induced Fourier transform infrared (FTIR) study, however, did not detect an appreciable change in the frequency of a major CO peak of QA− at ~1478 cm−1 between the S2QA−/S1QA and QA−/QA difference spectra of intact and Mn-depleted PSII samples, respectively, suggesting that the H-bond interaction of QA− is virtually unchanged by Mn4CaO5 cluster depletion.22 This was a sharp contrast to small but clear shifts in the CO peak of QA− by binding of different herbicide species, DCMU and bromoxynil, to the QB site,22 which provided opposite Em(QA−/QA) shifts by +50 and −45 mV, respectively.17 Meanwhile, density functional theory (DFT) calculations of PQ models with different H-bond structures showed that the main CO peak of a PQ− anion is rather insensitive to the H-bond interaction, whereas its side bands more prominently reflect the interactions with surrounding amino acid residues due to the couplings of their vibrations with the CO stretches of PQ−.23 It was further shown that the CO vibrations of neutral PQ are significantly affected by H-bond interactions, and thus are good markers to study the H-bond structure.23 However, it was difficult to identify the change in the CO bands of neutral QA by comparing the S2QA−/S1QA and QA−/QA spectra, because these CO bands are located at 1700-1600 cm−1 overlapping strong amide I bands (C=O stretches of main chains) of proteins.22,24 Therefore, more sophisticated FTIR analysis is necessary to detect the interaction changes of QA and QA− upon Mn depletion to clarify the molecular mechanism of the Em(QA−/QA) shift.

ABSTRACT: In photosystem II, the redox potential Em of the

primary quinone QA shifts by ~+150 mV upon inactivation of the Mn4CaO5 cluster. Although this phenomenon is important in photoprotection, the molecular mechanism of the positive Em(QA−/QA) shift remains unclear. Here, we investigated the effect of Mn depletion on the interaction of QA using light-induced ATR-FTIR spectroscopy. It was shown that Mn depletion hardly changed a QA−/QA FTIR difference spectrum, indicating that the H-bond interaction of QA and its immediate surroundings were virtually unchanged by Mn4CaO5 cluster inactivation. Based on this result, a possible mechanism of the Em(QA−/QA) shift is discussed.

Photosystem II (PSII) performs water oxidation through photoinduced electron transfer reactions. Illumination of PSII forms a charge-separated state between the primary electron donor chlorophyll P680 and the primary acceptor pheophytin (Pheo).1-4 An electron on Pheo− is transferred to plastoquinone (PQ) electron acceptors: first to the primary quinone electron acceptor QA and then to the secondary quinone acceptor QB.5,6 On the electron donor side, an electron hole on P680+ is transferred to the Mn4CaO5 cluster, the catalytic site of water oxidation, via the redox-active tyrosine YZ. This donor-side reaction induces stepwise oxidation of the Mn4CaO5 cluster, forming a cycle of five intermediates called Si states (i = 0-4), where molecular oxygen is evolved during the relaxation of the transient S4 state to the S0 state.7 These photoreactions leading to the forward electron flow are essential in light energy conversion, while backward electron transfer also plays an important physiological role.3,8,9 The backward electron transfer leads to charge recombination in PSII to dissipate an energy, and eventually prevents photodamage of PSII proteins; Such a charge recombination process functions as a photoprotection mechanism in PSII. Forward and backward electron flows are regulated by the redox potentials (Em’s) of the cofactors.3,4,8-10 In particular, the Em of QA often changes under some conditions,10-17 and hence the Em gaps (Em) among Pheo, QA, and QB are modulated. For instance, it has been demonstrated that when the Mn4CaO5 cluster is impaired by depletion of Mn and/or Ca ions, Em(QA−/QA) is shifted positively by ~150 mV from ~−100 mV to ~+50 mV.10-16 In contrast, we recently showed, by direct measurement of the Em of QB, that Em(QB−/QB) is only slightly affected by Mn depletion (from +93 to +87 mV).18 Therefore, the Em between QA and QB in intact PSII is decreased from ~190 to ~40 mV upon inactivation of the Mn4CaO5 cluster.18 1

ACS Paragon Plus Environment

Biochemistry

1364

-5

1183

1277

1237

1276

1239

1363

1420 1402

1439

1502

2x10

1600

1500

1400

1300

Wavenumber/cm

1183

1173

1320

1174

1320

1456 1438 1433 1417 1401

1363

1503

1550 1531

1477

1416

1586

1502 1477

1457 1439

1560 1543 1521 1550 1531

1561 1542 1517

1700

1559 1541 1516

1719

1800

1664 1649 1637 1625

1744 1725 1719 1744 1725

c

1682 1671 1657 1644 1632

b

1663 1673 1649 1657 1643 1637 1624

1677 1659 1637

a

1529

The obtained S2/S1 difference spectrum of intact PSII membranes (Figure 2a) showed prominent bands around 1400 cm−1, which have been assigned to the symmetric COO− stretching vibrations of carboxylate groups surrounding the Mn4CaO5 cluster.27-29 Strong bands at 1700-1620 and 1600-1500 cm−1 were mainly assigned to the amide I (C=O stretches of protein main chains) and amide II (NH bends and CN stretches of protein main chains) vibrations, respectvely,28 representing the perturbations of the protein main chains induced by S2 formation. In the latter region, the asymmetric COO− stretching vibrations of carboxylate groups also overlap.27,28 The S2QA−/S1QA difference spectrum (Figure 2b), which was measured using bromoxynil (the corresponding data set using DCMU is shown in Figure S1), showed a strong positive peak of QA− at 1477 cm−1 arising from a coupled vibration of the CO and CC stretches.22-24 A pure QA−/QA difference spectrum of intact PSII (Figure 2c) was obtained by subtracting the S2/S1 difference spectrum (Figure 2a) from the S2QA−/S1QA spectrum (Figure 2b) with an appropriate factor to cancel the typical S2/S1 feature around 1400 cm−1 (for the detail of the subtraction procedure, see Materials and Methods in Supporting Information). The spectrum showed several sub-peaks at 1503, 1456, 1438, 1433, and 1417 cm−1 around the main CO/CC peak at 1477 cm−1. These sub-peaks were previously assigned to the CO vibrations coupled with the methyl deformations and the vibrations of interacting amino-acid side chains.23 Strong bands due to the amide I and II vibrations were also observed at 1700-1620 and 1570-1510 cm−1, respectively. Negative bands of the CO and CC stretching vibrations of neutral QA, which have not been definitely identified yet, should overlap the amide I region.22-24 Peaks at 1725/1719 cm−1 were previously assigned to the ester C=O vibration of the nearby Pheo, which was affected by the formation of the QA− anion.30 1693 1667 1650

In this study, we investigated the effect of Mn depletion on the interactions of QA and QA− with surrounding proteins using lightinduced attenuated total reflection (ATR) FTIR difference spectroscopy, to answer the question whether the impairment of the Mn4CaO5 cluster induces the modulation of the QA binding site to shift the Em(QA−/QA). The light-induced ATR-FTIR difference spectroscopy is a useful method to obtain FTIR spectra of different cofactors in PSII using the same sample attached on the surface of an ATR crystal.25,26 In addition, this method enables various sample treatments such as Mn depletion as well as measurements under different buffer conditions without changing samples. Thus, subtle spectral changes by some treatment or a change in a condition can be detected without fluctuations, which would be caused by a sample change in other methods. We compared the QA−/QA FTIR difference spectra of intact and Mn-depleted PSII membranes, which were obtained using the same PSII sample but under different conditions. From the results, we discuss a possible mechanism of the Em(QA−/QA) shift by Mn4CaO5 cluster inactivation. Oxygen-evolving PSII membranes obtained from spinach were attached to the surface of the Si ATR prism (for details, see Materials and Methods in Supporting Information). By exchanging buffers in a flow cell, we obtained a series of difference spectra using this sample (Figure 1). We first measured an S2/S1 difference spectrum with a ferricyanide/ferrocyanide mixture and then an S2QA−/S1QA difference spectrum in the presence of herbicide (bromoxynil or DCMU). Subsequently, Mn depletion was performed with 10 mM NH2OH, and a QA−/QA difference spectrum was obtained for the Mn-depleted PSII membranes.

A

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

Page 2 of 5

1200

1100

1000

-1

Figure 2. Light-induced S2/S1 (a) and S2QA−/S1QA (b) FTIR difference spectra of intact PSII membranes on the Si ATR prism obtained by exchanging buffers. The spectrum (b) was measured in the presence of bromoxynil. The QA−/QA difference spectrum of intact PSII (c) was obtained by subtraction of the S2/S1 spectrum (a) from the S2QA−/S1QA spectrum (b) with an appropriate factor to cancel the S2/S1 signals. See Figure 1 for the buffer condition used for each measurement.

Figure 1. (A) Schematic diagram of an ATR cell used for lightinduced ATR-FTIR difference spectroscopy, and (B) procedure for the measurements of S2/S1, S2QA−/S1QA, and QA−/QA difference spectra using the PSII same sample attached on the Si ATR prism by exchanging buffers.

This QA−/QA difference spectrum of intact PSII membranes is compared with that of Mn-depleted PSII membranes, which was measured in the presence of bromoxynil as a herbicide and NH2OH as an electron donor, in Figure 3 (the corresponding data set using DCMU is shown in Figure S2). The spectral features in 2

ACS Paragon Plus Environment

Page 3 of 5

the whole region of 1800-1000 cm−1 were virtually identical between the intact and Mn-depleted PSII membranes. Indeed, an intact-minus-Mn-depleted double difference spectrum (Figure 3A, black line) did not show any meaningful bands, as compared with the noise level represented by a double difference spectrum between the dark-dark spectra of the intact and Mn-depleted PSII membranes (Figure 3A, dotted line). No appreciable changes by Mn depletion in the CO stretching region of QA− (1510-1400 cm−1) and in the amide I region involving the CO stretching vibrations of neutral QA (1700-1620 cm−1) were further confirmed by superposition of the two spectra in Figures 3C and 3B, respectively. In the former region, not only the main CO peak at 1477 cm−1 but also the sub-peaks, coupled with interacting amino acid residues,22 were unaffected by Mn depletion. Concerning

1800

1700

1600

1183 1183 1174

1320

1362

1320

1174

1276

1239

1276

1240

1363

1456 1438 1433 1417 1477 1456 1439 1432 1417

1550 1531 1502

1558 1541 1516

-5

2x10

1559 1541 1519

1682 1671 1657 16441631

1744 1725

A

1744 1719 1725 1682 1663 1671 1649 1657 1637 1644 1632 1621

1550 1531 1503

1663 1649 1637 1624

1719

1477

A

1500

1400

1300

Wavenumber/cm

1200

1100

1000

-1

C -5

-5

1x10

1417

1438

1433

1503

1644 1657

1671

1680

A

1632 1682

1700

1456

1649

1663

1637

1x10

1477

B

A

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

Biochemistry

1660

1640

1620 -1

Wavenumber/cm

1500 1480 1460 1440 1420 -1

Wavenumber/cm

Figure 3. Comparison of the QA−/QA difference spectra of intact (blue line) and Mn-depleted (red line) PSII membranes in the presence of bromoxynil (A; 1800-1000 cm−1). The spectrum of intact PSII (blue line) is identical to Figure 2c. The QA−/QA difference spectrum of Mn-depleted PSII (red line) was obtained after measurements of the S2/S1 and S2QA−/S1QA spectra of intact PSII by exchanging buffers (see Figure 1 for the buffer condition). The black line is a double difference spectrum between the QA−/QA difference spectra of intact and Mn-depleted PSII membranes (blue-minus-red). The dotted line is a double difference spectrum between the dark-minus-dark spectra of intact and Mndepleted PSII membranes calculated with the same factor as for the black line, representing a noise level. The two QA−/QA difference spectra of intact (blue line) and Mn-depleted (red line) PSII membranes are superimposed in the 1700-1620 (B) and 15151410 cm−1 (C) regions, which involve the CO stretching vibrations of neutral QA and anionic QA−, respectively.

surrounding amino acid residues, it was previously shown that the QA−/QA difference spectrum includes the bands of a His side chain, most probably D2-His214 H-bonded with QA, at 1359, 1256, 1179, and 1109/1102 cm−1, in the FTIR study using [15N]Hislabeled PSII (These peaks are hidden under other features and explicitly appear only in a double difference spectrum between unlabeled and [15N]His-labeled samples).31 Absence of specific signals at these positions in the double difference spectrum (Figure 3A, black line), especially at 1179 cm−1 where a mode involving the bending vibration of a strongly H-bonded imidazole NH was observed, suggests that the H-bond interaction of D2His214 was unaffected by Mn depletion. These results indicate that Mn depletion hardly changed the H-bond interactions of both neutral QA and anionic QA−. In addition, the protein structures around QA, including amino acid side chains and polypeptide main chains, which are affected by QA− formation and detected in the QA−/QA FTIR difference spectrum, were not modified by Mn depletion. The observed absence of changes in the H-bond interactions of the CO groups of QA and QA− by Mn depletion excludes additional H-bond formation as well as the alteration of the H-bond intensities as a cause of the large positive shift of Em(QA−/QA) by ~150 mV 10-16 upon Mn4CaO5 cluster impairment. Also, changes in the electrostatic interactions of QA− with amino acid residues in the vicinity of QA probably do not contribute to the Em(QA−/QA) shift. Therefore, the modulation of pKa’s of amino acid residues, which are not structurally coupled with QA and hence are not involved in the FTIR difference spectrum, can be a factor affecting Em(QA−/QA). Such residues are most likely located rather distant from QA. Indeed, on the stromal side of PSII, there are several Glu residues, D1-Glu242, D1-Glu243, D1-Glu244, D2-Glu241, and D2-Glu242 (numbering of residues in Thermosynechococcus elongatus and T. vulcanus), which could be related to the upshift of Em(QA−/QA). Our previous FTIR study of the non-heme iron20 suggested that the pKa’s of some Glu residues on the stromal side upshifted upon Mn4CaO5 cluster depletion. Such pKa changes of Glu residues could upshift the Em(QA−/QA), although it is still a question how the pKa changes in the stroma site are induced by Mn depletion. By contrast, our recent FTIR spectroelectrochemical measurements of QB showed that Mn depletion only slightly affected Em(QB−/QB).18 Thus, an asymmetric distribution of the Glu residues sensitive to Mn depletion on the stromal side could be the reason for the difference in the Em shift between QA and QB.18 The pKa changes of some Glu residues may additively affect Em(QA−/QA), while they may cancel each other out and hence hardly affect Em(QB−/QB). To clarify the regulation mechanism of the electron transfer between QA and QB by controlling Em(QA−/QA) and Em(QB−/QB), further FTIR studies using sitedirected mutants at these amino acid residues are necessary. In summary, the ATR-FTIR measurements, which enabled to compare the QA−/QA difference spectra of the intact and Mndepleted PSII membranes without changing samples, showed that Mn depletion hardly changed the H-bond interactions of QA and its immediate surroundings. Thus, modulation of the electrostatic interactions with Glu residues on the stromal side, located rather distant from QA, could be the cause of the large positive Em(QA−/QA) shift upon Mn4CaO5 cluster impairment, which plays an important role in photoprotection of PSII.

ASSOCIATED CONTENT Supporting Information Materials and Methods; S2/S1, S2QA−, and QA−/QA difference spectra of intact PSII membranes when DCMU is used; and comparison of QA−/QA difference spectra of intact and Mn-depleted PSII membranes in the presence of DCMU. The Supporting In-

3

ACS Paragon Plus Environment

Biochemistry

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

formation is available free of charge on the ACS Publications website (http://pubs.acs.org).

AUTHOR INFORMATION Corresponding Author *(Y.K.) E-mail: [email protected]. Telephone: +81-52-789-2881. Fax: +81-52-789-2883. *(T.N.) E-mail: [email protected].

Funding Sources This study was supported in part by the Grants-in-Aid for Scientific Research from Japan Society for the Promotion of Science (JSPS) (16K17857 to Y.K., 24000018, 24107003, and 25291033 to T.N.) and by Grant for Basic Science Research Projects from The Sumitomo Foundation (to Y.K.).

Notes The authors declare no competing financial interests.

ABBREVIATIONS ATR, attenuated total reflectance; Chl, chlorophyll; DCMU, 3(3,4-dichlorophyenyl)-1,1-dimethylurea; Em, redox potential; FTIR, Fourier transform infrared; Mes, 2-(Nmorpholino)ethanesulfonic acid; P680, the primary electron donor; Pheo; pheophytin; PQ, plastoquinone; PSII, photosystem II; QA, primary quinone electron acceptor; QB, secondary quinone electron acceptor

REFERENCES (1) McEvoy, J. P., and Brudvig, G. W. (2006) Water-splitting chemistry of photosystem II. Chem. Rev. 106, 4455−4483. (2) Messinger, J., Noguchi, T., and Yano, J. (2011) Photosynthetic O2 Evolution, in Molecular Solar Fuels (Wydrzynski, T., and Hillier, W., Eds.) pp 163−207, Chapter 7, Royal Society of Chemistry, Cambridge, U.K. (3) Cardona, T., Sedoud, A., Cox, N., and Rutherford, A. W. (2012) Charge separation in Photosystem II: A comparative and evolutional overview. Biochim. Biophys. Acta 1817, 26-43. (4) Renger, G. (2012) Photosynthetic water splitting: Apparatus and mechanism, in Photosynthesis: Plastid Biology, Energy Conversion and Carbon Assimilation (Eaton-Rye, J. J., Tripathy, B. C., and Sharkey, T. D., Eds.) pp 359−414, Springer, Dordrecht, The Netherlands. (5) Petrouleas, V., and Crofts, A. R. (2005) The quinone iron acceptor complex. In Photosystem II: The Light-Driven Water:Plastoquinone Oxidoreductase (Wydrzynski, T., and Satoh, K., Eds.) pp 177-206, Springer, Dordrecht, The Netherlands. (6) Müh, F., Glöckner, C., Hellmich, J., and Zouni, A. (2012) Lightinduced quinone reduction in photosystem II. Biochim. Biophys. Acta 1817, 44-65. (7) Joliot, P. (2003) Period-four oscillations of the flash-induced oxygen formation in photosynthesis. Photosynth. Res. 76, 65-72. (8) Krieger-Liszkay A., Fufezan, C., and Trebst, A. (2008) Singlet oxygen production in photosystem II and related protection mechanism. Photosynth Res. 98, 551-564. (9) Vass, I. (2011) Role of charge recombination processes in photodamage and photoprotection of the photosystem II complex. Physiol. Plant. 142, 6-16. (10) Johnson, G. N., Rutherford, A. W., and Krieger, A. (1995) A change in the midpoint potential of the quinone QA in photosystem II associated with photoactivation of oxygen evolution. Biochim. Biophys. Acta 1229, 202-207. (11) Krieger, A., and Weis, E. (1992) Energy-dependent of chlorophyll-a-fluorescence: The involvement of proton-calcium exchange at photosystem 2. Photosynthetica 27, 89-98. (12) Krieger, A., Rutherford, A. W., and Johnson, G. N. (1995) On the determination of redox midpoint potential of the primary quinone electron acceptor, QA, in photosystem II. Biochim. Biophys. Acta 1229, 193-201. (13) Shibamoto, T., Kato, Y., Sugiura, M., and Watanabe, T. (2009) Redox potential of the primary plastoquinone electron acceptor QA in

Page 4 of 5

photosystem II from Thermosynechococcus elongatus determined by spectroelectrochemistry. Biochemistry 48, 10682-10684. (14) Shibamoto, T., Kato, Y., Nagao, R., Yamazaki, T., Tomo, T., and Watanabe, T. (2010) Species-dependence of the redox potential of the primary quinone electron acceptor QA in Photosystem II verified by spectroelectrochemistry. FEBS Lett. 584, 1526-1530. (15) Ido, K., Gross, C. M., Guerrero F., Sedoud, A., Lai, T. -L., Ifuku, K., Rutherford, A. W., and Krieger-Liszkay, A. (2011) High and low potential forms of the QA quinone electron acceptor in Photosystem II of Thermosynechococcus elongatus and spinach. J. Photochem. Photobiol. B 104, 154-157. (16) Allakhverdiev, S. I., Tsuchiya, T., Watabe, K., Kojima, A., Los, D. A., Tomo, T., Klimov, V. V., and Mimuro, M. (2011) Redox potentials of primary electron acceptor quinone molecule (QA)− and conserved energetics of photosystem II in cyanobacteria with chlorophyll a and chlorophyll d. Proc. Natl. Acad. Sci. U.S.A. 108, 8054-8058. (17) Krieger-Liszkay A., and Rutherford, A. W. (1998) Influence of herbicide binding on the redox potential of the quinone acceptor in photosystem II. Relevance to photodamage and phytotoxicity. Biochemistry 37, 17339-17344. (18) Kato, Y., Nagao, R., and Noguchi, T. (2016) Redox potential of the terminal quinone electron acceptor QB in photosystem II reveals the mechanism of electron transfer regulation. Proc. Natl. Acad. Sci. U.S.A. 113, 620-625. (19) Andréasson, L. -E., Vass, I., Styring, S. (1995) Ca2+ depletion modifies the electron transfer on both donor and acceptor sides in Photosystem II from spinach. Biochim. Biophys. Acta 1230, 155-164. (20) Kato, Y., and Noguchi, T. (2014) Long-range interaction between the Mn4CaO5 cluster and the non-heme iron center in photosystem II as revealed by FTIR spectroelectrochemistry. Biochemistry 53, 4914-4923. (21) Ishikita, H., and Knapp, E. W. (2005) Control of quinone redox potentials in photosystem II: Electron transfer and photoprotection. J. Am. Chem. Soc. 127, 14714-14720. (22) Takano, A., Takahashi, R., Suzuki, H., and Noguchi, T. (2008) Herbicide effect on the hydrogen-bonding interaction of the primary quinone electron acceptor QA in photosystem II as studied by Fourier transform infrared spectroscopy. Photosynth. Res. 98, 159-167. (23) Ashizawa, R., and Noguchi, T. (2014) Effects of hydrogen bonding interactions on the redox potential and molecular vibrations of plastoquinone as studied by density functional theory calculations. Phys. Chem. Chem. Phys. 16, 11864-11876. (24) Berthomieu, C., Nabedryk, E., Mäntele, W., and Breton, K. (1990) Characterization by FTIR spectroscopy of the photoreduction of the primary quinone acceptor QA in photosystem II. FEBS Lett. 269, 363-367. (25) Okubo, T., and Noguchi, T. (2007) Selective detection of the structural changes upon photoreactions of several redox cofactors in photosystem II by means of light-induced ATR-FTIR difference spectroscopy. Spectrochim. Acta, Part A 66, 863–868. (26) Iizasa, M., Suzuki, H., and Takumi, N. (2010) Orientations of carboxylate groups coupled to the Mn cluster in the photosynthetic oxygenevolving center as studied by polarized ATR-FTIR spectroscopy. Biochemistry 49, 3074-3082. (27) Noguchi, T., Ono, T., and Inoue, Y. (1995) Direct detection of a carboxylate bridge between Mn and Ca2+ in the photosynthetic oxygenevolving center by means of Fourier transform infrared spectroscopy. Biochim. Biophys. Acta 1228, 189-200. (28) Noguchi, T., and Sugiura, M. (2003) Analysis of flash-induced FTIR difference spectra of the S-state cycle in the photosynthetic wateroxidizing complex by uniform 15N and 13C isotope labeling. Biochemistry 42, 6035-6042. (29) Nakamura, S., and Noguchi T. (2016) Quantum mechanics/molecular mechanics simulation of the ligand vibrations of the wateroxidizing Mn4CaO5 cluster in photosystem II. Proc. Natl. Acad. Sci. U.S.A. in press, doi: 10.1073/pnas.1607897113. (30) Suzuki, H., Nagasaka, M., Sugiura, M., and Noguchi, T. (2005) Fourier transform infrared spectrum of the secondary quinone electron acceptor QB in photosystem II. Biochemistry 44, 11323-11328. (31) Noguchi, T., Inoue, Y., and Tang, X.-S. (1999) Hydrogen bonding interaction between the primary quinone acceptor QA and a histidine side chain in photosystem II as revealed by Fourier transform infrared spectroscopy. Biochemistry 38, 399-403.

4

ACS Paragon Plus Environment

Page 5 of 5

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

Biochemistry

For Table of Contents Use Only Comparative analysis of the interaction of the primary quinone QA in intact and Mn-depleted photosystem II membranes using light-induced ATR-FTIR spectroscopy Yuki Kato, Rina Ishii, and Takumi Noguchi

5

ACS Paragon Plus Environment