Î²-Carotene Probes Energy Transfer Pathway in Photosystem II Core

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Biophysical Chemistry, Biomolecules, and Biomaterials; Surfactants and Membranes

#-Carotene Probes Energy Transfer Pathway in Photosystem II Core Complex Yusuke Yoneda, Yutaka Nagasawa, Yasufumi Umena, and Hiroshi Miyasaka J. Phys. Chem. Lett., Just Accepted Manuscript • DOI: 10.1021/acs.jpclett.9b01072 • Publication Date (Web): 28 May 2019 Downloaded from http://pubs.acs.org on May 28, 2019

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The Journal of Physical Chemistry Letters

β-Carotene Probes Energy Transfer Pathway in Photosystem II Core Complex Yusuke Yoneda1, Yutaka Nagasawa*2, Yasufumi Umena3, Hiroshi Miyasaka1

1Graduate 2College

School of Engineering Sciences, Osaka University, Toyonaka Osaka 560-8531, Japan

of Life Sciences, Ritsumeikan University, Kusatsu, Shiga 525-8577, Japan

3Research

Institute for Interdisciplinary Science, Okayama University, Okayama, Okayama 700-8530

Japan

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The Journal of Physical Chemistry Letters 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

ABSTRACT. The dynamics of intact photosystem II core complex (PSII-CC) has been investigated extensively to elucidate its excellent photofunction. However, it is significantly difficult to observe the primary photosynthetic processes in PSII-CC, because vast number of chlorophylls (Chl) in the core complex show similar spectral features. In the present work, dynamics of the energy transfer (ET) from β-carotene (Bcr) in intact PSII-CC followed by charge separation (CS) at reaction center (RC) with different excitation wavelengths were compared. Upon excitation at 510 nm, which selectively excite Bcr (Bcr651) inside the D1-D2 RC, pheophytin anion absorption band appeared within 9.6 ps. On the other hand, upon excitation at 490 nm, mainly exciting unspecified Bcr in the antenna complex, the anion band appeared after 20 ps. These excitation wavelength dependence experiments revealed a new ET pathway of PSII-CC which indicates that the initial CS of PSII-CC is limited by ET to the RC.


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Photosystem II core complex (PSII-CC) is one of the representative photosynthetic systems composed of antenna complexes (CP43 and CP47) and reaction center (RC) polypeptides (D1-D2 RC, Fig. 1a). It harvests light energy and produces charge separated (CS) states, resulting in the oxidization of water. Unveiling the precise structure1–6 and reaction dynamics7–15 of PSII-CC have been attracting much attention toward understanding the mechanism of its excellent photofunction. A number of time resolved spectroscopic studies have been conducted and kinetic models of energy transfer (ET) and CS in PSII-CC were deduced. There are two representative models; (i) exciton-radical pair equilibrium (ERPR) model: the excited state reaches its energy equilibrium in a few picoseconds among antenna and RC chlorophylls (Chls) and CS proceeds with the equilibrium between exciton and radical pair (RP) states,7–9 and (ii) transfer-to-the-trap limited (TTTL) model: the overall CS is severely limited by ET to the RC.10–12 The state in reality could be in between these two extreme cases, and to the best of our knowledge, the mechanism is still under active discussion.8,16–19 Although the measurements of individual complexes and combination of these results seem to be an effective approach to elucidate the dynamics, it is still difficult to combine these results into one comprehensive picture.19 The reasons may be the differences between complexes from different organisms (i.e., the measurements of PSII-RC and



PSII-CC are typically carried out with isolated complexes from higher plants and cyanobacteria, respectively), or the properties of some specific complexes can change depending on whether they are isolated or embedded as one of the components in larger complexes. Especially, small environmental change can affect the CS dynamics of RC, i.e., mutagenesis at D1 amino residue modulates the redox potential of pheophytin.20,21 PSII-CC contains 35 Chl molecules with all the absorption spectra overlapped, and accordingly, it is impossible to selectively excite or observe an individual Chl at a certain binding position. This is one of the major reasons why the dynamics of PSII-CC is so difficult to understand. However, the number of β-carotene (Bcr) molecules is only 11, which is one third of that of the Chls. In the absorption spectrum of PSII-CC (Fig. 1b), a local maximum appears at 492 nm, which corresponds to the absorption band of common Bcrs. The D1-D2 RC binds two types of Bcr molecules, which exhibit their absorption maxima at 489 nm and 507 nm, the former being perpendicular and the latter being parallel to the membrane plane.3,4,22 In common Bcrs, the -conjugation is reduced by β-ionone ring being twisted out of the plane of the C=C chain, and they exhibit absorption maxima at 480-490 nm. The red-shifted Bcr in the RC is known as Bcr651 indicated by the red ellipse in Fig. 1a. Mendes-Pinto et al. proposed that the binding pocket in the protein scaffold forces the


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out-of-plane rotated end cycle to return to the plane of the C=C chain,23 which induces elongation of -conjugation that results in a red-shifted absorption band at 507 nm. In this work, we have investigated ET and CS dynamics of PSII-CC by means of femtosecond transient absorption (TA) spectroscopy. We have compared TA dynamics upon excitation at 490 and 510 nm (Fig. 1b), which could either induce random excitation of dominant antenna Bcrs or selective excitation of Bcr651 in the D1-D2 RC, respectively. Selective excitation of Bcr651 could lead to simplified ET pathway in the intact PSII-CC, which can give detailed insight about CS dynamics of the core complex.

Figure 1. (a) Crystallographic structure of photosystem II core complex. One monomer unit contains 35 chlorophylls (green), including special pair (purple) and accessory chlorophylls 5 ACS Paragon Plus Environment


(pink), 2 pheophytins (red) and 11 Bcrs (orange). Bcr651 is indicated by red ellipse. The arrangement was depicted by PyMOL on the basis of the crystallographic structure of 3WU2.4 (b) Ground state absorption spectrum of photosystem II (blue) and spectra of excitation laser pulse used in the femtosecond transient absorption spectroscopy centered at 510 nm (green) and 490 nm (slate blue).

TA spectra of PSII-CC in the time range of femtoseconds to picoseconds by exciting the antenna Bcrs at 490 nm are shown in Fig. 2. Immediately after the photoexcitation, negative signal at 400-600 nm was observed which can be assigned to the mixture of ground state bleach (GSB) and stimulated emission (SE) of Bcr as observed in preceding studies (Fig. 2a).24 Excited state absorption (ESA) of Bcr due to S2 →Sn transition was also observed at >700 nm. The SE and ESA signals disappeared within 500 fs and simultaneously positive signal due to S1→Sn transition of Bcr at 500-600 nm appeared and the negative band at 680 nm (GSB of Chls) deepened. These results indicate that ultrafast ET from Bcr S2 state to Chl takes place competing with S2→S1 internal conversion (IC).


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Figure 2. Transient absorption spectra of photosystem II core complex excited at 490 nm in time range of (a) 50-500 fs and (b) 1-100 ps. Inset in (b) is 5 magnified transient absorption spectrum at 100 ps in the wavelength range of 445-500 nm, where the weak signal of pheophytin anion appears. The absorption band of the pheophytin anion (455 nm) is indicated by an arrow.25

The S1→Sn transition band of Bcr disappeared within 50 ps while the GSB of Chl was nearly identical (Fig. 2b). This indicates ET from Bcr in the S1 state is ineffective. At 100 ps after the photoexcitation, the TA spectrum observed by the excitation of Bcr was almost the same with that by the excitation of Chl except for a small positive band at 520 nm (Fig.



S1). This signal can be assigned to T1→Tn transition band of Bcr.26 Furthermore, weak positive band at 455 nm was observed which can be assigned to pheophytin anion (indicated by an arrow in the inset of Figure 2b).15,25 Hence, ET from Bcr actually induces CS at RC. Due to the overlap with T1→Tn transition band of Bcr, GSB of pheophytin at 540 nm was not clearly observable, thus, the band at 455 nm was utilized to monitor the CS dynamics in the RC. The TA spectra of PSII-CC excited at 510 nm (Fig. S2) were almost the same with that excited at 490 nm. However, by comparing the TA spectra in the range of 440-470 nm at 30-100 ps (Fig. S3a and S3b), it was found that pheophytin anion band at 455 nm with 510 nm excitation appeared faster than that with 490 nm excitation. These results suggest that excitation at 510 nm can selectively excite Bcr651 and its excitation energy is directly transferred to the RC (Scheme 1). When Bcrs in the antenna complexes, CP43 or CP47, are excited at 490 nm, the initial ET occurs to the Chls in these antenna complexes prior to those in the RC (Scheme 1b). Thus, CS in the RC is limited by the ET from CP43 or CP47 to RC in a few tens of picoseconds.

Scheme 1. Energy transfer pathways in photosystem II core complex with selective


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excitation of β-carotene molecules.

The minima of GSB of Bcr at 1 ps after the photoexcitation was 496 nm for excitation at 510 nm (Fig. 3a, red) while that was 488 nm for 490 nm excitation (Fig. 3a, blue). This result confirms that different Bcrs are indeed excited by selecting the excitation wavelength. Figure 3b shows TA spectra of PSII-CC at 1 ps in the wavelength range of 640-720 nm, where the overlapping GSB and SE of Chl Qy band appear. The width of the GSB/SE of Chl with excitation at 510 nm is narrower than that at 490 nm (TA spectra at other time delays are shown in Fig. S4). The inhomogeneity of Chl, which is populated after the excitation ET from Bcr, is considered to be smaller for 510 nm excitation. By fitting the GSB/SE of Chl by lognormal function, time evolution of the bandwidth was elucidated and 9 ACS Paragon Plus Environment


shown in Fig. S5. The bandwidth reduced with time and reached a constant value of 340 cm-1 with time constant for 510 nm excitation (0.82 ps) being much shorter than those for 490 nm (1.1 ps (49%) and 16 ps (51%)). These observations also suggest that Bcr651 in the RC is selectively excited at 510 nm to induce direct energy transfer to the Chls in the RC which is expected to be faster than that from the pigments in the surrounding antenna complexes as shown in Scheme 1.

Figure 3. Transient absorption spectra of photosystem II core complex in the wavelength range of (a) 410-540 nm and (b) 640-720 nm with excitation at 490 nm (blue) and 510 nm (green).

To obtain further detailed insights, global analysis with sequential modeling was 10 ACS Paragon Plus Environment

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performed and evolution associated difference spectra (EADS) were obtained (Fig. 4). In the case of 510 nm excitation, 5 components were required for a reasonable fit and the obtained EADS are shown in Fig. 4a. Some of the analyzed results of the time evolution of the differential absorbance at various wavelengths are depicted in Fig. S6. The spectral shapes and time constants of first 3 components were almost identical to the previously reported EADS of PSII-RC in the wavelength range of 530-720 nm.24 Our present experimental setup had wider probe wavelength range of 410-950 nm, which enables to obtain some new spectral signatures. The 1st EADS with lifetime of 85 fs shows negative signal at 400-650 nm, attributable to GSB and SE of Bcr, and positive signal at 700-950 nm, due to ESA of S2→Sn transition of Bcr. The lifetime of 85 fs for this EADS is in good agreement with the previously reported one.24 The 2nd EADS with lifetime of 430 fs shows ESA of S1→Sn transition of Bcr at 500-650 nm and the GSB/SE of Chl at 680 nm. The absence and presence of GSB/SE of Chl in 1st and 2nd EADS clearly indicate energy transfer from the S2 state to Chl taking place in competition with the IC to the S1 state. The 2nd EADS evolves with time constant of 430 fs into 3rd EADS which also contains ESA of S1→Sn transition of Bcr with more sharpened spectral feature. This spectral evolution is characteristic for photoexcited Bcr and ascribed to the cooling of vibrationally hot S1 state.24 The 3rd EADS evolves into 4th



EADS (mainly contains Chl/pheophytin signals as discussed later) with lifetime of 9.6 ps. This time scale corresponds to S1→S0 IC of Bcr which are consistent with previously reported EADS of PSII-RC.24

Figure 4. Evolution associated difference spectra (EADS) of photosystem II core complex excited at (a) 510 nm and (b) 490 nm. Each EADS evolves into the next one with time constants given in the figure with the same color as the curve. The final EADS had a lifetime longer than the limit of the time range of our experimental setup (2 ns). Some of the EADS in the wavelength range of 455-500 nm, where the weak signal of pheophytin anion appears, is plotted as an inset with magnification of 5.


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The 4th EADS consists of GSB/SE of Qy band at 680 nm and GSB of Soret band at 410-450 nm of Chl. The positive signal due to T1→Tn transition of Bcr is also observed at 520 nm. In addition to these signals, a weak positive band at 455 nm attributable to pheophytin anion was also observed (inset in Fig. 4a). However, the large signal amplitude of GSB and S1→Sn absorption of Bcr at 410-600 nm disturbs the precise analysis of the small spectral change due to pheophytin anion, i.e., the CS process cannot be separated from the S1→S0 IC of Bcr. Thus, from the analysis at the present stage, we can deduce the conclusion that the CS takes place in a time scale shorter than 9.6 ps. The 5th EADS contains smaller amplitude of GSB/SE of Chl, and hence, evolution from 4th to 5th EADS with lifetime of 340 ps can be ascribed to the transition from the RP2 (P+D1Pheo-) to the RP3 (P+D1Q-A), because the decrease of GSB of Qy band indicates further electron transport from pheophytin to quinone molecule as reported previously.8 The final species remained until 2 ns, which is the time limit of our experimental setup. In the case of 490 nm excitation (Fig. 4b), EADS and time constants were nearly the same as those of 510 nm excitation, although, additional component (4th EADS) with lifetime of 20 ps was required for a reasonable fit (details are discussed in SI). The component still contains bands that originate from Bcr, i.e., negative and positive bands at 400-500 nm



and 500-600 nm, respectively. However, the pheophytin anion band at 455 nm did not appear until the 5th component, and in this case, the amplitude of 5th EADS was comparable to that of 4th (inset in Fig. 4b). These observations indicate that CS takes place with ~20 ps (details are discussed in SI). The bandwidth of GSB/SE of Chls of 5th EADS is narrower than that of 4th. Renger et al. reported that energy transfer from antenna Chls (CP43 or 47) to RC take place with 41-50 ps.10 And time constant of 20 ps is comparable to that obtained from the time evolution of the bandwidth (Fig. S5), suggesting ET from antenna to RC takes place in this time scale. Thus, it can be suggested that the CS induced by 490 nm excitation is limited by the ET from antenna complexes to RC. As a conclusion, we have successfully shown that Bcr (Bcr651) in the RC can be selectively excited at 510 nm even in intact PSII-CC and such selective excitation can reveal a new ET pathway of PSII-CC. The CS induced by direct excitation of Bcr651 was strongly suggested to occur with a time constant shorter than 9.6 ps from EADS analysis. We can also conclude that CS induced by excitation of Bcrs in the antenna complex is limited by the ET from CP43 or CP47 to RC with time constant of 20 ps.

ACKNOWLEDGMENT


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This work was supported by JSPS KAKENHI Grant Numbers JP16J00627 and JP26107002 in Scientific Research on Innovative Areas "Photosynergetics" and also by JP18H05180 in "Innovations for Light-Energy Conversion."



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Î²-Carotene Probes Energy Transfer Pathway in Photosystem II Core

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