pH-Dependent Regulation of the Relaxation Rate of the Radical Anion

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pH-Dependent regulation of the relaxation rate of the radial anion of the secondary quinone electron acceptor QB in photosystem II as revealed by Fourier transform infrared spectroscopy Yosuke Nozawa, and Takumi Noguchi Biochemistry, Just Accepted Manuscript • DOI: 10.1021/acs.biochem.8b00263 • Publication Date (Web): 20 Apr 2018 Downloaded from http://pubs.acs.org on April 20, 2018

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Biochemistry

pH-Dependent Regulation of the Relaxation Rate of the Radial Anion of the Secondary Quinone Electron Acceptor QB in Photosystem II as Revealed by Fourier Transform Infrared Spectroscopy

Yosuke Nozawa, and Takumi Noguchi*

Division of Material Science, Graduate School of Science, Nagoya University, Furo-cho, Chikusa-ku, Nagoya, 464-8602, Japan

*Corresponding Author: Takumi Noguchi E-mail: [email protected]. Telephone: +81-52-789-2881.

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ABBREVIATIONS ChlD1, monomeric chlorophyll on the D1 side; DCMU, 3-(3, 4-dichlorophenyl)-1, 1-dimethylurea; Em, redox potential; FTIR, Fourier transform infrared; Hepes, 4-(2-hydroxyethyl)-1-piperazineethanesulfonic acid; Mes, 2-(N-morpholino)ethanesulfonic acid; P680, special-pair chlorophyll in photosystem II; PheoD1, pheophytin on the D1 side; PheoD2, pheophytin on the D2 side; PSII, photosystem II; PQ, plastoquinone; QA, primary quinone electron acceptor; QB, secondary quinone electron acceptor.

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Biochemistry

ABSTRACT: Photosystem II (PSII) is a protein complex that preforms water oxidation using light energy in photosynthesis. In PSII, electrons abstracted from water are eventually transferred to the secondary quinone electron acceptor, QB, and upon double reduction, QB is converted to quinol by binding two protons. Thus, excess electron transfer in PSII increases the pH of the stroma. In this study, to investigate the pH-dependent regulation of the electron flow in PSII, we have estimated the relaxation rate of the QB− radical anion in the pH region between 5 and 8 by direct monitoring of its population using light-induced Fourier transform infrared (FTIR) difference spectroscopy. The decay of QB− by charge recombination with the S2 state of the water oxidation center in PSII membranes was shown to be accelerated at higher pH, whereas that of QA− examined in the presence of a herbicide was virtually unaffected at pH ≤ 7.5 and slightly slowed down at pH 8. These observations were consistent with the previous studies by rather indirect monitoring of the QB− and QA− decays using such as fluorescence detection. The accelerated relaxation of QB− was explained by the shift of a redox equilibrium between QA− and QB− to the QA− side due to the decrease in the redox potential of QB at higher pH, which is induced by deprotonation of a single amino acid residue near QB. It is proposed that this pH-dependent QB− relaxation is one of the mechanisms of electron flow regulation in PSII for its photoprotection.

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INTRODUCTION Photosystem II (PSII) is a multisubunit protein complex that is embedded in thylakoid membranes in plants and cyanobacteria. Its function is light-driven oxidation of water and reduction of plastoquinone (PQ) to produce plastoquinol, thus providing electrons to the photosynthetic electron transport chain. Photochemistry in PSII starts with light-induced charge separation between the special pair chlorophyll, P680, and the pheophytin electron acceptor, PheoD1, to form a charged pair, P680+PheoD1−.2 On the electron donor side, P680+ oxidizes the Mn4CaO5 cluster, which is the catalytic site of water oxidation, via the redox-active tyrosine YZ.3 Upon abstraction of four electrons from the Mn4CaO5 cluster, two water molecules are oxidized to one oxygen molecule and four protons through the so-called S-state cycle.4-7 In this cycle, an intermediate called Si state (i = 0–3) advances to the next intermediate upon single-turnover electron transfer starting from the dark stable S1 state: S1 → S2 → S3 → S0 → S1. On the electron acceptor side, an electron is transferred from PheoD1− to the primary quinone electron acceptor QA and then to the secondary quinone electron acceptor QB. Upon two-turnover reactions, QB is converted to plastoquinol by binding two protons and then released into the thylakoid membrane.8-10 PSII is known to be a major target of photodamage in the photosynthetic apparatus.11 Hence, PSII has developed various mechanisms to regulate its reactions at different levels for photoprotection. In the antenna system, excessive excitation energy on antenna chlorophylls is dissipated by non-photochemical quenching.12 In the reaction center, the secondary electron transfer pathway consisting of carotenoid, Chlz, and Cytb559 functions to remove a positive charge from the strong oxidant P680+ to prevent oxidative damage to a center with an inactive Mn4CaO5 cluster.13 Also, a triplet state produced on a monomer chlorophyll ChlD1 located between P680 and PheoD1 by charge recombination is quenched by a photo-accumulated QA− semiquinone anion to prevent the formation of harmful singlet oxygen.14,

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Certain cyanobacteria have a specific

mechanism to regulate charge recombination by changing the redox potential (Em) of PheoD1 through exchanging the D1 protein isoforms.16, 17 Furthermore, Em(QA−/QA) has been proposed to increase upon inactivation of the Mn4CaO5 cluster,18,

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which

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Biochemistry

promotes direct relaxation of QA−,20 whereas no such change was found in Em(QB−/QB).21 As for the regulation of the QB reaction, it was previously observed in chloroplasts that charge recombination of QB− with the S2 state was accelerated at higher pH, whereas that of QA− was rather slowed down.22-24 In these experiments, however, the QB− and QA− decays were monitored by rather indirect ways due to detection of fluorescence or O2 evolution. It is well known that the fluorescence intensity from PSII reflects the redox state of QA, but is not necessarily proportional to the QA− population.25, 26 In addition, the reported pH dependence of the apparent equilibrium constant between QA− and QB− was virtually unaffected by Mn depletion,22 which is in contradictory to the proposed large Em(QA−/QA) shift (by −150 mV) upon Mn depletion18, 19 with little change in Em(QB−/QB).21 Thus, to understand the pH-dependent regulation mechanism of electron transfer reactions of QA and QB in PSII, it is important to reinvestigate the pH dependence of the relaxation rates of the QA− and QB− semiquinone anions using a more direct method to detect them. Light-induced Fourier transform infrared (FTIR) difference spectroscopy is a powerful method to investigate the electron transfer and water oxidation reactions in PSII.27-34 With this method, the redox reactions of QA and QB can be separately monitored using their specific signals at ~1717 and ~1745 cm−1, respectively, which arise from the 132-ester C=O vibrations of nearby PheoD1 and PheoD2, respectively, having different hydrogen bonding interactions.35 These Pheo signals in the QA−/QA and QB−/QB difference spectra are directly coupled with the QA− and QB− formations, respectively, and thus are useful markers to detect them. In this study, we applied this FTIR method of direct detection of QA− and QB− to investigate the pH dependence of the relaxation rates of QA− and QB− in PSII membranes. It was found that the QB− relaxation was indeed accelerated as the pH increased, whereas the QA− relaxation was rather insensitive to pH at pH ≤ 7.5 and slightly slowed down at higher pH. The obtained results were discussed in the context of electron flow regulation in PSII for its photoprotection through the pH-dependent shift of Em(QB−/QB).

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MATERIALS AND METHODS Samples. Oxygen-evolving PSII membranes of spinach36 were prepared as reported previously37 and suspended in a Mes (pH 5.0–6.5) or Hepes (pH 7.0–8.0) buffer (60 mM Mes/Hepes, 400 mM sucrose, and 15 mM NaCl, and 5 mM NaHCO3). For measurements of S2QB−/S1QB difference spectra, 1 mL of the sample suspension (0.5 mg Chl/ml) in the above buffer was centrifuged at 170,000 g for 35 min, and the resultant pellet was sandwiched between CaF2 plates (25 mm in diameter). One of the CaF2 plates has a circular groove (10 mm inner diameter, 1 mm width), and the sample cell was sealed with silicone grease laid on the outer part of the groove.38 The sample temperature was adjusted to 20 °C by circulating water in a copper holder. The same procedure was used in the sample preparation for S2QA−/S1QA difference spectra, except for using a buffer additionally involving 0.1 mM 3-(3, 4-dichlorophenyl)-1, 1-dimethylurea (DCMU) and 5 mM potassium ferrocyanide. A small amount of ferricyanide in equilibrium with ferrocyanide functions as an electron acceptor for full reoxidation of QA− required for repetitive measurements. FTIR measurements. FTIR spectra were recorded using Bruker IFS-66/S or VERTEX 80 spectrophotometer equipped with an MCT detector (InfraRed D313-L). Flash illumination was performed using a Q-switched Nd:YAG laser (Quanta-Ray GCR-130 or INDI-40-10; 532 nm; ~7 ns fwhm; ~14 mJ pulse−1 cm−2). The sample was loaded so that the absorbance at the amide II peak at ~1550 cm−1 was about 1 (thus the amide I region at ~1650 cm−1 was saturated), to detect the QB− (~1746 cm−1) and QA− (~1719 and ~1477 cm−1) signals with high signal-to-noise ratios. For monitoring the time course of the S2QB− charge recombination, 2 and 30 single beam spectra (10-s scans for each) before and after single-flash illumination, respectively, were measured. S2QB−/S1QB difference spectra calculated as after-minus-before illumination showed the S2QB− relaxation, while the difference of the two spectra before illumination represented a noise level. The same measurement but without illumination, providing only baseline changes during measurement, was performed before the S2QB− measurement. The thus obtained spectra were used to correct the baseline changes of the S2QB−/S1QB difference

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spectra. The measurements were repeated 5 times with 2-h intervals, and the spectra were averaged. For monitoring the time course of the S2QA− charge recombination, 2 single-beam spectra (10-s scans) were measured before single-flash illumination and 10 and then 2 single-beam spectra (1-s and 10-s scans, respectively) were measured after illumination.

S2QA−/S1QA

illumination showed the

difference

S2QA−

spectra

calculated

as

after-minus-before

relaxation, while the difference of the two spectra before

illumination represented a noise level. The measurements were repeated 6 times with 5-min intervals, and the spectra were averaged.

RESULTS The S2QA− charge separated state was formed by single-flash illumination on spinach PSII membranes in buffers at pH 5.0–8.0 in the presence of DCMU at 20 °C,

1700 1600 1500 1400

1700 1600 1500 1400

1477

-4

1477

f. pH 7.5

1700 1600 1500 1400 -1

-4

2x10

1402

1477

g. pH 8.0 1719

2x10

-4

1403 1402

1718

-4

2x10

1403

1719

1477

e. pH 7.0

-4

2x10

1477 1402

1718

d. pH 6.5

2x10

c. pH 6.0 1718

-4

2x10

1402

1719

1478

b. pH 5.5

-4

2x10

1401

1719

a. pH 5.0

1478

and the S2QA−-minus-S1QA (hereafter, S2QA−/S1QA) FTIR difference spectra and their

∆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

1700 1600 1500 1400

Wavenumber (cm )

Figure 1. Time courses of the S2QA−/S1QA FTIR difference spectra after illumination of a single flash on the PSII membranes in the presence of DCMU at pH (a) 5.0, (b) 5.5, (c) 6.0, (d) 6.5, (e) 7.0, (f) 7.5, and (g) 8.0. Spectra recorded at 0.5, 1.5, 2.5, 3.5, 4.5, 5.5, 6.5, 7.5, 8.5, 9.5, 15, and 25 s after illumination are shown from upper to lower traces. The sample temperature was 20 °C. The blank around 1650 cm−1 is a region saturated by strong absorption due to the amide I and water bending vibrations. 7


Biochemistry

decays were recorded (Figure 1). Spectra at all the pHs showed similar features with a prominent positive peak at 1478–1477 cm−1 arising from the CO/CC vibration of the QA− semiquinone anion39-41 and a negative peak at 1403–1401 cm−1 due to the COO− vibrations of carboxylate groups around the Mn4CaO5 cluster.42, 43 The peak at 1719– 1718 cm−1 is also attributed to the QA−/QA difference, and arises from the nearby 132-ester C=O group of PheoD1 that is perturbed by QA− formation.35 The decays of the relative intensities of the QA−/QA signals at ~1477 and ~1719 cm−1 and the intensity of the S2/S1 signal at ~1402 cm−1 are plotted in Figure 2. These decays were well fitted with single exponential functions. Note that the QA− signals did not decay to zero in 30 s, probably because the Mn4CaO5 cluster is inactivated in some centers, which stabilized QA− without charge recombination with the S2 state. The decay rates were similar between QA− and S2 (Figure 3), confirming that S2QA− charge recombination is the main decay mechanism. The estimated time constant, τA, was about 4 s between pH 5.0 and 7.5 with virtually no pH dependence, whereas a little slower τA (~6 s) was observed at 1.0

a. pH 5.0

b. pH 5.5

c. pH 6.0

d. pH 6.5

e. pH 7.0

f. pH 7.5

0.8 0.6

Relative Intensity

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

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0.4 0.2 0.0 1.0

g. pH 8.0

0.8 0.6 0.4 0.2 0.0 0

10

20

0

10

20

0

10

20

0

10

20

Time (s)

Figure 2. Relaxation of the S2QA− state as the time courses of the relative intensities of the QA−/QA bands at ~1477 (red circles) and ~1719 (blue circles) cm−1 and the S2/S1 band at ~1402 cm−1 (green circles) at pH (a) 5.0, (b) 5.5, (c) 6.0, (d) 6.5, (e) 7.0, (f) 7.5, and (g) 8.0. The intensities of the ~1477, ~1719, and ~1402 cm−1 bands were estimated as ∆A differences from 1492, 1726 and 1383 cm−1, respectively, in the spectra in Figure 1. Curves obtained by single-exponential fitting are also shown in the corresponding colors. 8


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Figure 3. pH dependence of the time constant of S2QA− charge recombination in the PSII membranes in the presence of DCMU at 20 °C estimated from the QA−/QA signals at ~1477 (red circles) and ~1719 (blue circles) cm−1 and from the S2/S1 signal at ~1402 cm−1 (green circles). Error bars are the standard deviations of the time constants obtained by the single-exponential fitting of the signal decays (Figure 2).

Time constant (s)

8 7 6 5 4 3 2 5

6

7

8

pH

pH 8.0. Single-flash illumination on untreated PSII membranes mainly forms an S2QB− charge separated state. Flash-induced FTIR difference spectra and their decays were recorded at pH 5.0–8.0 at 20 °C (Figure 4). The typical S2/S1 signal at 1402 cm−1 were

1600

1500

1400

1600

1500

1600

1500

-5

1400

1747

1700

1600

1500

2x10

1402

-5

1478

2x10

1403

1700

-5

1402

1746

1400

g. pH 8.0

2x10

1482 1480

-5

2x10

f. pH 7.5

1746

1402

-5

1402

1746

1700

c. pH 6.0

2x10

1480

e. pH 7.0

1481

-5

2x10

1402

1745 1746

1700

b. pH 5.5 1745

-5

2x10

1479

d. pH 6.5

1402

a. pH 5.0

1481

observed in all the spectra similarly to the S2QA− case. The CO/CC stretching band of a

∆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

1400

-1

Wavenumber (cm )

Figure 4. Time courses of the S2QB−/S1QB FTIR difference spectra after illumination of a single flash on the PSII membranes at (a) 5.0, (b) 5.5, (c) 6.0, (d) 6.5, (e) 7.0, (f) 7.5, and (g) 8.0. Spectra measured at 5, 15, 25, 35, 45, 95, 145, 195, 245, and 295 s after illumination are shown from upper to lower trances. The blank around 1650 cm−1 is a region saturated by strong absorption due to the amide I and water bending vibrations. 9


Biochemistry

semiquinone anion was observed at 1482–1478 cm−1. The slightly higher frequencies than the corresponding QA− signal at 1478–1477 cm−1 (Figure 1) are consistent with the previous observation of the QB−/QB FTIR difference spectra,21, 35, 44, 45 suggesting the major contribution of the QB−/QB signal in the spectra. However, the presence of the QA−/QA specific peak at ~1719 cm−1 in all the spectra (Figure 4) also indicates some contribution of the QA−/QA signal, due probably to the presence of QB-nonreducing centers46,

47

as well as QA− in equilibrium with QB−. Besides these signals, the

QB-specific signal was observed as a positive peak at 1747–1745 cm−1 (an expanded view is shown in Figure 5). This signal has been attributed to the 132-ester CO group of PheoD2 that is perturbed by QB− formation.35 The large frequency difference from the QA-specific

cm−1

signal at ~1719

originates from

the

difference

in

the

hydrogen-bonding interaction of the 132-ester C=O group of PheoD2 (non-hydrogen a. pH 5.0

b. pH 5.5

1745

bonding)

c. pH 6.0 1746

2x10

-5

2x10

-5

2x10

from

that

of

PheoD1

(hydrogen bonding).1 Because of this

-5

1745

frequency difference, the signal at ~1746 cm−1 can be a useful marker to specifically detect QB−.21, 35 Using this marker band, the decay of the QB− f. pH 7.5

1746

1747 -5 -5

-5

2x10

2x10

population was examined (Figure 5).

g. pH 8.0

1746

2x10

e. pH 7.0

1746

2x10

d. pH 6.5 -5

∆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

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Note that although the contribution of the QA−/QA signal is relatively large in the spectrum at pH 8.0 (Figure 4g), a minor QA−/QA signal with a differential shape at 1752/1743 cm−1 (Figure 1g)

1750

1740

1750

1740

1750

1740

1750

1740

-1

Wavenumber (cm )

Figure 5. The expanded view of the QB−/QB band at ~1746 cm−1 at pH (a) 5.0, (b) 5.5, (c) 6.0, (d) 6.5, (e) 7.0, (f) 7.5, and (g) 8.0. Spectra recorded at 5, 15, 25, 35, 45, 95, 145, 195, 245, and 295 s after single-flash illumination are shown from upper to lower trances.

little affects the intensity of the QB−/QB peak at 1747 cm−1. The relative intensity of the ~1746 cm−1 peak at each pH was plotted against the time from flash illumination, and the plot was fitted

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a. pH 5.0

1.0

b. pH 5.5

c. pH 6.0

0.8

Relative Intensity

0.6 0.4 0.2 0.0

d. pH 6.5

1.0

e. pH 7.0

f. pH 7.5

g. pH 8.0

0.8 0.6 0.4 0.2 0.0 0

100

200

0

100

200

0

100

200

0

100

200

Time (s)

Figure 6. Relaxation of QB− as the time course of the relative intensity of the QB−/QB signal at ~1756 cm−1 (closed circles) at pH (a) 5.0, (b) 5.5, (c) 6.0, (d) 6.5, (e) 7.0, (f) 7.5, and (g) 8.0. The peak intensity was estimated as a ∆A value from a baseline drawn between 1758 and 1737 cm−1 in the spectra in Figure 5. Curves obtained by single-exponential fitting are also shown in solid lines. with a single exponential function (Figure 6). The time constant of the QB− decay, τB, decreased as the pH increased from 5 to 8, although similar τB values were observed at pH 7.5 and 8.0 (Figure 7). The apparent equilibrium constant of one-electron redox reaction between QA− and QB−, Kapp, was obtained from τB and τA (the data of ~1477 cm−1 was used for τA) as K app =

τB − 1 , assuming that τA obtained using DCMU τA

represents the original rate of S2QA− recombination in PSII in which QB is occupied by Figure 7. pH dependence of the time constant of S2QB− charge recombination in the PSII membranes at 20 °C estimated from the QB−/QB signal at ~1746 cm−1. Error bars are the standard deviations of the time constants obtained by the single-exponential fitting of the signal decays (Figure 6).

100

Time Constant (s)

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

80

60

40

20 5

6

7

8

pH 11


Biochemistry

25

Figure 8. pH dependence of Kapp of the redox equilibrium between QA− and QB− in the PSII membranes at 20 °C. Kapp was estimated as τB/τA − 1. The data of ~1477 cm−1 (Figure 3) were used for τA.

20

Kapp

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

15 10 5 0 5

6

7

8

pH PQ. The estimated Kapp showed a clear pH dependence, in which Kapp is ~20 at pH 5 and decreases to ~4 at pH 8 (Figure 8).

DISCUSSION We have directly monitored the time courses of the decays of QB− and QA− after single-flash illumination on PSII membranes in the absence and presence of DCMU, respectively, using FTIR difference spectroscopy. The QB− relaxation by charge recombination with the S2 state of the Mn4CaO5 cluster takes place through QA−, and hence its relaxation rate is governed by the one-electron equilibrium between QB− and QA−. The clear pH dependence of τB of the QB− decay (Figure 7) and of the equilibrium constant Kapp (Figure 8), in contrast to the absence of the pH dependence of τA of the QA− decay (Figure 3) at least between pH 5 and 7.5, indicates that some protonation/deprotonation reaction affects the Em(QB−/QB). The presence of the CO/CC peak of the QB− semiquinone anion at ~1480 cm−1 upon single flash illumination (Figure 4)35, 44 implies the absence of direct protonation of QB upon its single reduction. This is consistent with a relatively low pKa value (~5) of the semiquinone anion of PQ in

QA−QB H+

K1 H+

Ka1

QA−QB(H+)

QAQB−

K2

Ka2

Scheme 1. One-electron redox equilibrium between the radical anions of QA and QB in PSII. Protonation of an amino acid residue near QB is expressed by H+ in parentheses.

QAQB−(H+) 12


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Biochemistry

aqueous solution recently estimated by quantum chemical calculation.48 Thus, the protonation/deprotonation of an amino acid residue located near QB should be responsible for the observed pH dependence. The diagram of the one-electron equilibrium of QA− and QB− including the protonation of a nearby residue (represented by H+ in parentheses) is shown in Scheme 1. The equilibrium constant in the deprotonated state, K1, is the extreme case of high pH, while that in the protonated state, K2, is another extreme case of low pH. Protonation of a certain residue takes place with an acid dissociation constant Ka1 in the QA−QB state and with Ka2 in the QAQB− state. Kapp, which is the population of QB− relative to that of QA− in equilibrium ([QAQB−]+ [QAQB−(H+)])/([QA−QB]+[QA−QB(H+)]), is expressed as a function of pH using K1, pKa1, and pKa2 (derivation of the equation is given in Supporting Information):

K app =

(

K1 1 + 10pKa 2 − pH 1 + 10pKa1− pH

)

The experimental pH dependence of Kapp (Figure 8, solid circles) was fitted with this function (Figure 8, solid line), and the best-fit parameters were obtained as: P680*/P680+ Pheo−/Pheo

QA−/QA

Em

> 33±6 mV

QB−/QB (high pH) pH↑

> 77±6 mV

~44±8 mV

QB−/QB (low pH) P680/P680+

Figure 9. Schematic diagram of the pH-induced shift of Em(QB−/QB) in relevant to the acceleration of QB− relaxation. Forward and backward electron transfers are expressed by solid and dashed blue arrows, respectively. Note that the ∆Em values between Em(QA−/QA) and Em(QB−/QB) were estimated assuming that the QB site is always occupied by PQ and that Em(QA−/QA) is unchanged when DCMU is bound to the QB site. 13


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pKa1 = 6.7 ± 0.1, pKa2 = 7.5 ± 0.2, and K1 = 3.7 ± 0.9. The relationship between K1 and K2, K 2 =

K a1 K1 , gives K2 = 21 ± 5. This estimation indicates that the protonatable Ka2

group near QB has a pKa value of 6.7 when QB has a neutral form but it increases to 7.5 when QB is reduced to a semiquinone anion. From the above K1 and K2 values, the energy gap between QA− and QB−, and hence the redox potential gap (∆Em) between Em(QA−/QA) and Em(QB−/QB), was estimated. ∆Em was estimated to be 77 ± 6 mV at very low pH and 33 ± 6 mV at very high pH at 20 °C (Figure 9), indicating that ∆Em decreases by 44 ± 8 mV upon pH increase. Assuming that Em(QA−/QA) is pH independent (this is the case at least between pH 5.0–7.5), this implies the decrease in Em(QB−/QB) by ~44 mV. It should be noted that in this estimation we omit the equilibrium of the binding of PQ to the QB site, and thus assumed that the QB site is always occupied by PQ. Actually, however, some centers have empty QB sites and QA− recombines with the S2 state without transferring an electron to QB. Indeed, FTIR difference spectra of the PSII membranes (Figure 4) always involved some population of QA− more than expected from the redox equilibrium with QB−. Thus, real K1 and K2 values should be larger than the values estimated above. If the equilibrium of the PQ binding to the QB site is taken into consideration (Scheme S1 in Supporting Information), Kapp is expressed as:

K app =

(

)

K1 1 + 10pKa 2 − pH  1  1 +  1 + 10pKa1− pH  K 0 [PQ] 

(

)

where K0 is the binding constant of PQ and [PQ] is the concentration of PQ (derivation of the equation is given in Supporting Information).9, 49, 50 If K0 = 500 M−1 and [PQ] = 5 mM, which were previously estimated by Crofts et al.49 in chloroplasts, are adopted, K1 and K2 are estimated as 13 ± 3 and 71 ± 17, respectively, and ∆Em is estimated to be 109 ± 6 and 65 ± 6 mV at low and high pH, respectively. Even larger K1, K2, and ∆Em values are expected in the PSII membranes that should have smaller [PQ]. In addition, it has been reported that DCMU binding to the QB site increases Em(QA−/QA) by ~+50 mV.51 Thus, real τA without DCMU may be smaller than the values obtained in the present study, and ∆Em can be even larger than the values estimated above. This is 14


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Biochemistry

consistent with the previous FTIR estimation of Em(QB−/QB) as ~+90 mV using the PSII core complex from Thermosynechococcus elongatus at pH 6.0 to provide the ∆Em value of ~190 mV.21 The observation of faster relaxation of QB− at higher pH in the PSII membranes in the current FTIR study (Figure 7) is in agreement with the previous results in chloroplasts.22-24 In addition, the pKa values that we estimated, pKa1 = 6.7 ± 0.1 and pKa2 = 7.5 ± 0.2, are consistent with the previous estimation by Croft and coworkers, 6.2–6.4 (pKa1) and 7.9–8.1 (pKa2), in chloroplasts using fluorescence measurements,9, 22, 49, 52 and by Ishikita and Knapp, 5.9 (pKa1) and 7.3 (pKa2), by theoretical calculations.53 The absence of pH dependence in the QA− relaxation at pH ≤ 7.5 and a slowed rate at pH 8 (Figure 3) is also consistent with the previous fluorescence results,22, 23 which showed little change at acidic pH and slowed rates at alkaline pH, and with the report of the pH independence of Em(QA−/QA) between pH 5.5 and 7.5.18 Because the S1 → S2 transition in the Mn4CaO5 cluster is basically independent of pH,54 the mechanism of retardation of the S2QA− recombination at high pH is unknown at present; some structural changes in the protein moiety near the QA site, including changes in the secondary structure of main chains and the locations of side chains, could be related to this phenomenon. It is important that in our study we directly monitored the QB− and QA− populations by detecting the QB−/QB and QA−/QA specific FTIR signals, in contrast to rather indirect detection of QB− and QA− relaxations in the previous studies by such as the loss of the binary pattern of fluorescence,22,

55

delayed luminescence,23 and flash-induced O2

evolution.24 The consistency of our results with the previous ones confirmed the presence of the pH-dependent regulation of QB− relaxation in PSII. We propose that the acceleration of QB− relaxation at higher pH is one of the regulation mechanisms of electron flow in PSII for photoprotection (Figure 9). When the pH of the stromal side increases by excessive electron flow, the QB− relaxation is accelerated as feedback regulation. This regulation will inhibit the full reduction of the PQ pool and QB, which otherwise leads to the formation of harmful singlet oxygen through the triplet state of ChlD115,

56

by repetitive charge recombination between

QA−/PheoD1− and S2/YZ•/P680+. The key mechanism of this regulation is the downshift

15


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Figure 10. Interactions of QA and QB with surrounding amino acid residues.1

of Em(QB−/QB) by deprotonation of an amino acid group near QB at higher pH, which decreases ∆Em between Em(QB−/QB) and Em(QA−/QA) and shifts the redox equilibrium to the QA− side. The remaining question is which amino acid residue is responsible for the pH-dependent shift of Em(QB−/QB). A single protonatable group with pKa of 6.7 and 7.5 for neutral and anionic QB, respectively, can explain the pH dependence of Kapp (Figure 8). One possible candidate is D1-His215, which is a ligand to the non-heme iron and directly hydrogen-bonded with QB (Figure 10). FTIR evidence has shown that this His residue is deprotonated to be an imidazolate anion at high pH when the non-heme iron is in an oxidized Fe3+ state.57 However, it remains unknown that such deprotonation takes place in a reduced Fe2+ state, which is dominant under a physiological condition. Indeed, the observation that the CO/CC frequency of QB− at ~1480 cm−1 (with some contribution of QA− signal) is rather insensitive to pH (Figure 4) may dismiss this possibility because a drastic change in the CO/CC band would be expected if the hydrogen bond is disrupted and a negative charge is formed in the immediate vicinity of the CO group of QB. Another likely candidate is D1-His252, as has been suggested by Crofts and coworkers,9, 58 which is located ~8 Å apart from QB (between the centers of the imidazole and quinone rings) and is hydrogen-bonded with the CO of QB through the hydroxide group of D1-Ser264 (Figure 10).1 This His residue is exposed to the stroma on the protein surface1 and hence is directly susceptible to the pH change. Ishikita

and

Knapp

suggested

from

their

theoretical

analysis

that

the

protonation/deprotonation of D1-His252 induces the change in the Em(QB−/QB) through rearrangement of the hydrogen-bond pattern in the His252–Ser264–QB interaction,53 in an analogous way to Asp-L213 that interacts with QB though Ser-L223 in the bacterial

16


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Biochemistry

reaction center from Rhodobacter sphaeroides.59

D1-His252 is also proposed to play a

role in the delivery of a proton to QB when it is doubly reduced.9, 60 Indeed, it has been reported that the site-directed mutants of D1-His252 lowered the rate or the yield of the QA− → QB electron transfer at the first flash and some of them showed an inhibited reaction at the second flash.8,

9, 61

Examination of the pH dependence of the QB−

relaxation and the QA− ↔ QB− equilibrium in such D1-H252 mutants is urgent to clarify the role of this residue in the pH-dependent regulation of electron flow in PSII.

Supporting Information The Supporting Information is available free of charge on the ACS Publications website at DOI:-----. The reaction scheme involving PQ binding to the QB site, and the derivations of the equations for Kapp (PDF).

ACKNOWLEDGMENTS This study was supported by JSPS KAKENHI Grant Number JP17H06435 and JP17H03662.

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For Table of Content Use Only

pH-Dependent Regulation of the Relaxation Rate of the Radial Anion of the Secondary Quinone Electron Acceptor QB in Photosystem II as Revealed by Fourier Transform Infrared Spectroscopy

Yosuke Nozawa, and Takumi Noguchi

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pH-Dependent Regulation of the Relaxation Rate of the Radical Anion

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