Faculty Profiles - SHEN Jian-Ren

The structure and activation of substrate water molecules in Sr2+-substituted photosystem II Reviewed International journal

Ruchira Chatterjee, Sergey Milikisiyants, Christopher S. Coates, Faisal H. M. Koua, Jian-Ren Shen, K. V. Lakshmi

PHYSICAL CHEMISTRY CHEMICAL PHYSICS 16 ( 38 ) 20834 - 20843 2014

Language：English Publishing type：Research paper (scientific journal) Publisher：ROYAL SOC CHEMISTRY

The mechanism of solar water oxidation by photosystem II (PSII) is of fundamental interest and it is the object of extensive studies both in the past and present. The solar water oxidation reaction of PSII occurs in the oxygen-evolving complex (OEC). The OEC consists of a tetranuclear manganese calcium-oxo (Mn4Ca-oxo) cluster that is surrounded by amino acid residues and inorganic cofactors. The role of the Ca2+ ion in the water oxidation reaction is one of the most interesting questions that is yet to be answered. In this study, we probe the structural and functional differences induced by metal ion substitution in the Mn4Ca-oxo cluster by substituting the Ca2+ ion in the OEC by a Sr2+ ion. We apply two-dimensional (2D) hyperfine sublevel correlation (HYSCORE) spectroscopy to detect weak magnetic interactions between the paramagnetic Mn4Sr-oxo cluster and the surrounding protons in the S-2 state of the OEC of Sr2+-substituted PSII. We identify three groups of protons that are magnetically interacting with the Mn4Sr-oxo cluster. Using the recently reported 1.9 angstrom resolution X-ray structure of the OEC in the S-1 state [Umena et al.] and the high-resolution 2D HYSCORE spectroscopy studies of the S-2 state of the OEC of Ca2+-containing PSII [Milikisiyants et al., Energy Environ. Sci., 2012, 5, 7747], we discuss the assignments of the three groups of protons that are magnetically coupled to the Mn4Sr-oxo cluster. Since hyperfine interactions are highly sensitive to small perturbations in the electronic and geometric structure of paramagnetic centers, a comparison of the 2D HYSCORE spectra of Sr2+-substituted and Ca2+-containing PSII allows us to draw important conclusions with respect to the structure of the substrate water molecules in the OEC and the role of the Ca2+ ion in the water oxidation reaction. In addition, for the first time, we determine the experimental value of the spin projection factor for the Mn(III) ion of the Mn4Ca-oxo cluster as rho(1) = +/- 1.7 from the assignment of the hyperfine interaction of the paramagnetic cluster with the protons of the D1-His332 residue of PSII.

DOI： 10.1039/c4cp03082f

Hydration of the oxygen-evolving complex of photosystem II probed in the dark-stable S-1 state using proton NMR dispersion profiles Reviewed International journal

Guangye Han, Yang Huang, Faisal Hammad Mekky Koua, Jian-Ren Shen, Per-Olof Westlund, Johannes Messinger

PHYSICAL CHEMISTRY CHEMICAL PHYSICS 16 ( 24 ) 11924 - 11935 2014

Language：English Publishing type：Research paper (scientific journal) Publisher：ROYAL SOC CHEMISTRY

The hydration of the oxygen-evolving complex (OEC) was characterized in the dark stable S-1 state of photosystem II using water R-1(omega) NMR dispersion (NMRD) profiles. The R-1(omega) NMRD profiles were recorded over a frequency range from 0.01 MHz to 40 MHz for both intact and Mn-depleted photosystem II core complexes from Thermosynechococcus vulcanus (T. vulcanus). The intact-minus-(Mn)-depleted difference NMRD profiles show a characteristic dispersion from approximately 0.03 MHz to 1 MHz, which is interpreted on the basis of the Solomon-Bloembergen-Morgan (SBM) and the slow motion theories as being due to a paramagnetic enhanced relaxation (PRE) of water protons. Both theories are qualitatively consistent with the S-T = 1, g = 4.9 paramagnetic state previously described for the S-1 state of the OEC; however, an alternative explanation involving the loss of a separate class of long-lived internal waters due to the Mn-depletion procedure can presently not be ruled out. Using a point-dipole approximation the PRE-NMRD effect can be described as being caused by 1-2 water molecules that are located about 10 angstrom away from the spin center of the Mn4CaO5 cluster in the OEC. The application of the SBM theory to the dispersion observed for PSII in the S-1 state is questionable, because the parameters extracted do not fulfil the presupposed perturbation criterion. In contrast, the slow motion theory gives a consistent picture indicating that the water molecules are in fast chemical exchange with the bulk (tau(w) < 1 mu s). The modulation of the zero-field splitting (ZFS) interaction suggests a (restricted) reorientation/ structural equilibrium of the Mn4CaO5 cluster with a characteristic time constant of tau(ZFS) = 0.6-0.9 mu s.

DOI： 10.1039/c3cp55232b

2P257 Theoretical investigation on the conformation-charge relationship of the photosystem II oxygen evolving complex (PSII-OEC)(18B. Photobiology:Photosynthesis,Poster)

Photosynthesis: from natural to artificial International journal

Johannes Messinger, Wolfgang Lubitz, Jian-Ren Shen

PHYSICAL CHEMISTRY CHEMICAL PHYSICS 16 ( 24 ) 11810 - 11811 2014

Shoji Mitsuo, Isobe Hiroshi, Yamanaka Shusuke, Shen Jian-Ren, Yamaguchi Kizashi

Seibutsu Butsuri 54 ( 1 ) S237 2014

2P258 ENDOR studies on Ca depleted and Sr substituted Mn cluster in photosystem II(18B. Photobiology:Photosynthesis,Poster)

Nagashima Hiroki, Nakajima Yoshiki, Shen Jian-Ren, Mino Hiroyuki

Seibutsu Butsuri 54 ( 1 ) S237 2014

Generalized approximate spin projection calculations of effective exchange integrals of the CaMn4O5 cluster in the S1 and S3 states of the oxygen evolving complex of photosystem II Reviewed

H. Isobe, M. Shoji, S. Yamanaka, H. Mino, Y. Umena, K. Kawakami, N. Kamiya, J.-R. Shen, K. Yamaguchi

Phys. Chem. Chem. Phys. 16 ( 24 ) 11911 - 11923 2014

Evidence for an Unprecedented Histidine Hydroxyl Modification on D2-His336 in Photosystem II of Thermosynechoccocus vulcanus and Thermosynechoccocus elongatus Reviewed International journal

Miwa Sugiura, Kazumi Koyama, Yasufumi Umena, Keisuke Kawakami, Jian-Ren Shen, Nobuo Kamiya, Alain Boussac

BIOCHEMISTRY 52 ( 52 ) 9426 - 9431 2013.12

Language：English Publishing type：Research paper (scientific journal) Publisher：AMER CHEMICAL SOC

The electron density map of the 3D crystal of Photosystem II from Thermosynechococcus vulcanus with a 1.9 angstrom resolution (PDB: 3ARC) exhibits, in the two monomers in the asymmetric unit cell, an, until now, unidentified and uninterpreted strong difference in electron density centered at a distance of around 1.5 angstrom from the nitrogen N delta of the imidazole ring of D2-His336. By MALDI-TOF/MS upon tryptic digestion, it is shown that similar to 20-30% of the fragments containing the D2-His336 residue of Photosystem II from both Thermosynechococcus vulcanus and Thermosynechococcus elongatus bear an extra mass of +16 Da. Such an extra mass likely corresponds to an unprecedented post-translational or chemical hydroxyl modification of histidine.

DOI： 10.1021/bi401213m

Spectral and functional studies on siphonaxanthin-type light-harvesting complex of photosystem II from Bryopsis corticulans Reviewed International journal

Wenda Wang, Xiaochun Qin, Min Sang, Dongqin Chen, Kebin Wang, Rongchen Lin, Congming Lu, Jian-Ren Shen, Tingyun Kuang

PHOTOSYNTHESIS RESEARCH 117 ( 1-3 ) 267 - 279 2013.11

Language：English Publishing type：Research paper (scientific journal) Publisher：SPRINGER

Carotenoids with conjugated carbonyl groups possess special photophysical properties which have been studied in some water-soluble light-harvesting proteins (Polivka and Sundstrom, Chem Rev 104:2021-2071, 2004). However, siphonaxanthin-type light-harvesting complexes of photosystem II (LHCII) in siphonous green alga have received fewer studies. In the present study, we determined sequences of genes for several Bryopsis corticulans Lhcbm proteins, which showed that they belong to the group of major LHCII and diverged early from green algae and higher plants. Analysis of pigment composition indicated that this siphonaxanthin-type LHCII contained in total 3 siphonaxanthin and siphonein but no lutein and violaxanthin. In addition, 2 chlorophylls a in higher plant LHCII were replaced by chlorophyll b. These changes led to an increased absorption in green and blue-green light region compared with higher plant LHCII. The binding sites for chlorophylls, siphonaxanthin, and siphonein were suggested based on the structural comparison with that of higher plant LHCII. All of the ligands for the chlorophylls were completely conserved, suggesting that the two chlorophylls b were replaced by chlorophyll a without changing their binding sites in higher plant LHCII. Comparisons of the absorption spectra of isolated siphonaxanthin and siphonein in different organic solutions and the effect of heat treatment suggested that these pigments existed in a low hydrophobic protein environment, leading to an enhancement of light harvesting in the green light region. This low hydrophobic protein environment was maintained by the presence of more serine and threonine residues in B. corticulans LHCII. Finally, esterization of siphonein may also contribute to the enhanced harvesting of green light.

DOI： 10.1007/s11120-013-9808-3

Gold or silver deposited on layered manganese oxide: a functional model for the water-oxidizing complex in photosystem II Reviewed International journal

Mohammad Mahdi Najafpour, Fahimeh Rahimi, Davood Jafarian Sedigh, Robert Carpentier, Julian J. Eaton-Rye, Jian-Ren Shen, Suleyman I. Allakhverdiev

PHOTOSYNTHESIS RESEARCH 117 ( 1-3 ) 423 - 429 2013.11

Language：English Publishing type：Research paper (scientific journal) Publisher：SPRINGER

In this report, gold or silver deposited on layered manganese oxide has been synthesized by a simple method and characterized by scanning electron microscopy, transmission electron microscopy, X-ray diffraction spectrometry, atomic absorption spectroscopy, and energy-dispersive X-ray mapping. The gold deposited on layered manganese oxide showed efficient catalytic activity toward water oxidation in the presence of cerium(IV) ammonium nitrate. The properties associated with this compound suggest it is a functional model for the water-oxidizing complex in photosystem II.

DOI： 10.1007/s11120-013-9899-x

Crystal structure at 1.5 angstrom resolution of the PsbV2 cytochrome from the cyanobacterium Thermosynechococcus elongatus Reviewed International journal

Michihiro Suga, Thanh-Lan Lai, Miwa Sugiura, Jian-Ren Shen, Alain Boussac

FEBS LETTERS 587 ( 19 ) 3267 - 3272 2013.10

Language：English Publishing type：Research paper (scientific journal) Publisher：WILEY

PsbV2 is a c-type cytochrome present in a very low abundance in the thermophilic cyanobacterium Thermosynechococcus elongatus. We purified this cytochrome and solved its crystal structure at a resolution of 1.5 angstrom. The protein existed as a dimer in the crystal, and has an overall structure similar to other c-type cytochromes like Cytc(6) and Cytc(550), for example. However, the 5th and 6th heme iron axial ligands were found to be His51 and Cys101, respectively, in contrast to the more common bis-His or His/Met ligands found in most cytochromes. Although a few other c-type cytochromes were suggested to have this axial coordination, this is the first crystal structure reported for a c-type heme with this unusual His/Cys axial coordination. Previous spectroscopic characterizations of PsbV2 are discussed in relation to its structural properties. (C) 2013 Federation of European Biochemical Societies. Published by Elsevier B. V. All rights reserved.

DOI： 10.1016/j.febslet.2013.08.023

Special issues on Photosynthesis Education honoring Govindjee International journal

Suleyman I. Allakhverdiev, Jian-Ren Shen, Gerald E. Edwards

PHOTOSYNTHESIS RESEARCH 116 ( 2-3 ) 107 - 110 2013.10

Crystal Structure of Psb31, a Novel Extrinsic Protein of Photosystem II from a Marine Centric Diatom and Implications for Its Binding and Function Reviewed International journal

Ryo Nagao, Michihiro Suga, Ayako Niikura, Akinori Okumura, Faisal Hammad Mekky Koua, Takehiro Suzuki, Tatsuya Tomo, Isao Enami, Jian-Ren Shen

BIOCHEMISTRY 52 ( 38 ) 6646 - 6652 2013.9

Language：English Publishing type：Research paper (scientific journal) Publisher：AMER CHEMICAL SOC

Psb31 is a fifth extrinsic protein found in photosystem II (PSII) of a centric diatom, Chaetoceros gracilis. The protein has been shown to bind directly to PSII in the absence of other extrinsic proteins and serves in part as a substitute for PsbO in supporting oxygen evolution. We report here the crystal structure of Psb31 at a resolution of 1.55 angstrom. The structure of Psb31 was composed of two domains, one major, N-terminal four helical domain and one minor, flexible C-terminal domain. The four helices in the N-terminal domain were arranged in an up down-up-down-fold, which appeared unexpectedly to be similar to the structure of spinach PsbQ in spite of their low sequence homology. This suggests that the centric diatom PSII contains another PsbQ- type extrinsic protein in addition to the original PsbQ protein found in the organism. On the other hand, the C-terminal domain of Psb31 has a unique structure composed of one loop and one short helix. Based on these structural analysis and chemical cross-linking experiments, residues responsible for the binding of Psb31 to PSII intrinsic proteins were suggested. The results are discussed in relation to the copy number of extrinsic proteins in higher plant PSII.

DOI： 10.1021/bi400770d

Application of Peptide Gemini Surfactants as Novel Solubilization Surfactants for Photosystems I and II of Cyanobacteria Reviewed International journal

Shuhei Koeda, Katsunari Umezaki, Tomoyasu Noji, Atsushi Ikeda, Keisuke Kawakami, Masaharu Kondo, Yasushi Yamamoto, Jian-Ren Shen, Keijiro Taga, Takehisa Dewa, Shigeru Ito, Mamoru Nango, Toshiki Tanaka, Toshihisa Mizuno

LANGMUIR 29 ( 37 ) 11667 - 11680 2013.9

Language：English Publishing type：Research paper (scientific journal) Publisher：AMER CHEMICAL SOC

We designed novel peptide gemini surfactants (PG-surfactants), DKDKC12K and DKDKC12D, which can solubilize Photosystem I (PSI) of Thermosynecoccus elongatus and Photosystem II (PRI) of Thermosynecoccus vulcanus in an aqueous buffer solution. To assess the detailed effects of PC-surfactants on the original supramolecular membrane protein complexes and functions of PSI and PSII, we applied the surfactant exchange method to the isolated PSI and PSII. Spectroscopic properties, light-induced electron transfer activity, and dynamic light scattering measurements showed that PSI and PSII could be solubilized not only with retention of the original supramolecular protein complexes and functions but also without forming aggregates. Furthermore, measurement of the lifetime of light-induced charge-separation state in PSI revealed that both surfactants, especially DKDKC12D, displayed slight improvement against thermal denaturation below 60 degrees C compared with that using beta-DDM. This degree of improvement in thermal resistance still seems low, implying that the peptide moieties did not interact directly with membrane protein surfaces. By conjugating an electron mediator such as methyl viologen (MV2+) to DKDKC12K (denoted MV-DKDKC12K), we obtained derivatives that can trap the generated reductive electrons from the light-irradiated PSI. After immobilization onto an indium tin oxide electrode, a cathodic photocurrent from the electrode to the PSI/MV-DKDKC12K conjugate was observed in response to the interval of light irradiation. These findings indicate that the PG-surfactants DKDKC12K and DKDKC12D provide not only a new class of solubilization surfactants but also insights into designing other derivatives that confer new functions on PSI and PSII.

DOI： 10.1021/la402167v

Photosystem II Does Not Possess a Simple Excitation Energy Funnel: Time-Resolved Fluorescence Spectroscopy Meets Theory Reviewed International journal

Yutaka Shibata, Shunsuke Nishi, Keisuke Kawakami, Jian-Ren Shen, Thomas Renger

JOURNAL OF THE AMERICAN CHEMICAL SOCIETY 135 ( 18 ) 6903 - 6914 2013.5

Language：English Publishing type：Research paper (scientific journal) Publisher：AMER CHEMICAL SOC

The experimentally obtained time-resolved fluorescence spectra of photosystem H (PS II) core complexes, purified from a thermophilic cyanobacterium Thermosynechococcus vulcanus, at 5-180 K are compared with simulations. Dynamic localization effects of excitons are treated implicitly by introducing exciton domains of strongly coupled pigments. Exciton relaxations within a domain and exciton transfers between domains are treated on the basis of Redfield theory and generalized Forster theory, respectively. The excitonic couplings between the pigments are calculated by a quantum chemical/electrostatic method (Poisson-TrEsp). Starting with previously published values, a refined set of site energies of the pigments is obtained through optimization cycles of the fits of stationary optical spectra of PS II. Satisfactorily agreement between the experimental and simulated spectra is obtained for the absorption spectrum including its temperature dependence and the linear dichroism spectrum of PS II core complexes (PS II-CC). Furthermore, the refined site energies well reproduce the temperature dependence of the time-resolved fluorescence spectrum of PS II-CC, which is characterized by the emergence of a 695 nm fluorescence peak upon cooling down to 77 K and the decrease of its relative intensity upon further cooling below 77 K. The blue shift of the fluorescence band upon cooling below 77 K is explained by the existence of two red-shifted chlorophyll pools emitting at around 685 and 695 nm. The former pool is assigned to Chl45 or Chl43 in CP43 (Chl numbering according to the nomenclature of Loll et al. Nature 2005, 438, 1040) while the latter is assigned to Chl29 in CP47. The 695 nm emitting chlorophyll is suggested to attract excitations from the peripheral light-harvesting complexes and might also be involved in photoprotection.

DOI： 10.1021/ja312586p

Electronic structure of S-2 state of the oxygen-evolving complex of photosystem II studied by PELDOR Reviewed International journal

Mizue Asada, Hiroki Nagashima, Faisal Hammad Mekky Koua, Jian-Ren Shen, Asako Kawamori, Hiroyuki Mino

BIOCHIMICA ET BIOPHYSICA ACTA-BIOENERGETICS 1827 ( 3 ) 438 - 445 2013.3

Language：English Publishing type：Research paper (scientific journal) Publisher：ELSEVIER SCIENCE BV

Photosynthetic water splitting is catalyzed by a Mn4CaO5 cluster in photosystem II, whose structure was recently determined at a resolution of 1.9 angstrom [Umena, Y. et al. 2011, Nature, 473:55-60]. To determine the electronic structure of the Mn4CaO5 cluster, pulsed electron-electron double resonance (PELDOR) measurements were performed for the tyrosine residue Y-D(center dot) and S-2 state signals with non-oriented and oriented photosystem II (PS H) samples. Based on these measurements, the spin density distributions were calculated by comparing with the experimental results. The best fitting parameters were obtained with a model in which Mn1 has a large positive projection, Mn3 has a small positive projection, and Mn2 and Mn4 have negative projections (the numbering of Mni (i=1-4) is based on the crystal structure at a 1.9 angstrom resolution), which yielded spin projections of 1.97, -120, 1.19 and -0.96 for Mn1-4 ions. The results show that the Mn1 ion, which is coordinated by H332, 0342 and E189, has a valence of Mn(III) in the S-2 state. The sign of the exchange interactions J(13) is positive, and the other signs are negative. 2(C) 013 Els,evier B.V. All rights reserved.

DOI： 10.1016/j.bbabio.2012.12.011

Structure of Sr-substituted photosystem II at 2.1 angstrom resolution and its implications in the mechanism of water oxidation Reviewed International journal

Faisal Hammad Mekky Koua, Yasufumi Umena, Keisuke Kawakami, Jian-Ren Shen

PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 110 ( 10 ) 3889 - 3894 2013.3

Language：English Publishing type：Research paper (scientific journal) Publisher：NATL ACAD SCIENCES

Oxygen-evolving complex of photosystem II ( PSII) is a tetra-manganese calcium penta-oxygenic cluster (Mn4CaO5) catalyzing light-induced water oxidation through several intermediate states (S-states) by a mechanism that is not fully understood. To elucidate the roles of Ca2+ in this cluster and the possible location of water substrates in this process, we crystallized Sr2+-substituted PSII from Thermosynechococcus vulcanus, analyzed its crystal structure at a resolution of 2.1 angstrom, and compared it with the 1.9 angstrom structure of native PSII. Our analysis showed that the position of Sr was moved toward the outside of the cubane structure of the Mn4CaO5-cluster relative to that of Ca2+, resulting in a general elongation of the bond distances between Sr and its surrounding atoms compared with the corresponding distances in the Ca-containing cluster. In particular, we identified an apparent elongation in the bond distance between Sr and one of the two terminal water ligands of Ca2+, W3, whereas that of the Sr-W4 distance was not much changed. This result may contribute to the decrease of oxygen evolution upon Sr2+-substitution, and suggests a weak binding and rather mobile nature of this particular water molecule (W3), which in turn implies the possible involvement of this water molecule as a substrate in the O-O bond formation. In addition, the PsbY subunit, which was absent in the 1.9 angstrom structure of native PSII, was found in the Sr-PSII structure.

DOI： 10.1073/pnas.1219922110

Water oxidation and water-oxidizing complex in cyanobacteria Reviewed

Mohammad Mahdi Najafpour, Atefeh Nemati Moghaddam, Jian-Ren Shen, Govindjee

Stress Biology of Cyanobacteria: Molecular Mechanisms to Cellular Responses 41 - 60 2013.1

Language：English Publishing type：Part of collection (book) Publisher：CRC Press

Cyanobacteria, or blue-green algae as they were called, are a group of bacteria that obtain their energy through oxygenic photosynthesis (for a perspective, see [1]
for evolution, see [2]).Cyanobacteria converted the early reducing atmosphere into an oxidizing one and changed the composition of life forms on Earth. The consensus is that chloroplasts in plants and eukaryotic algae have evolved from cyanobacterial ancestors via endosymbiosis [3]. In this chapter, we will discuss the structure and function of the water-oxidizing complex (WOC) in cyanobacteria [4,5].

DOI： 10.1201/b13853

Scopus

Structural Basis of Photosynthetic Water-Splitting

Jian-Ren Shen, Yasufumi Umena, Keisuke Kawakami, Nobuo Kamiya

SOLAR CHEMICAL ENERGY STORAGE (SOLCHES) 1568 31 - 34 2013

Language：English Publishing type：Research paper (international conference proceedings) Publisher：AMER INST PHYSICS

Photosynthetic water-splitting takes place in photosystem II (PSII), a membrane protein complex consisting of 20 subunits with an overall molecular mass of 350 kDa. The light-induced water-splitting reaction catalyzed by PSII not only converts light energy into biologically useful chemical energy, but also provides us with oxygen indispensible for sustaining oxygenic life on the earth. We have solved the structure of PSII at a 1.9 angstrom resolution, from which, the detailed structure of the Mn4CaO5-cluster, the catalytic center for water-splitting, became clear. Based on the structure of PSII at the atomic resolution, possible mechanism of light-induced water-splitting was discussed.

DOI： 10.1063/1.4848085