X-ray emission spectroscopy of biomimetic Mn coordination complexes

Jensen, Scott C.; Davis, Katherine M.; Sullivan, Brendan; Hartzler, Daniel A.; Seidler, Gerald T.; Casa, Diego M.; Kasman, Elina; Colmer, Hannah E.; Massie, Allyssa A.; Jackson, Timothy A.; Pushkar, Yulia

doi:10.1021/acs.jpclett.7b01209

Title: X-ray emission spectroscopy of biomimetic Mn coordination complexes

Journal Article · Fri May 19 00:00:00 EDT 2017 · Journal of Physical Chemistry Letters

DOI:https://doi.org/10.1021/acs.jpclett.7b01209· OSTI ID:1364024

Jensen, Scott C.; Davis, Katherine M.; Sullivan, Brendan; Hartzler, Daniel A.; Seidler, Gerald T.; Casa, Diego M.; Kasman, Elina; Colmer, Hannah E.; Massie, Allyssa A.; Jackson, Timothy A.; Pushkar, Yulia

Understanding the function of Mn ions in biological and chemical redox catalysis requires precise knowledge of their electronic structure. X-ray emission spectroscopy (XES) is an emerging technique with a growing application to biological and biomimetic systems. Here, we report an improved, cost-effective spectrometer used to analyze two biomimetic coordination compounds, [Mn^IV(OH)₂(Me₂EBC)]²⁺ and [Mn^IV(O)(OH)(Me₂EBC)]⁺, the second of which contains a key Mn^IV=O structural fragment. Despite having the same formal oxidation state (Mn^IV) and tetradentate ligands, XES spectra from these two compounds demonstrate different electronic structures. Experimental measurements and DFT calculations yield different localized spin densities for the two complexes resulting from Mn^IV–OH conversion to Mn^IV=O. The relevance of the observed spectroscopic changes is discussed for applications in analyzing complex biological systems such as photosystem II. In conclusion, a model of the S₃ intermediate state of photosystem II containing a Mn^IV=O fragment is compared to recent time-resolved X-ray diffraction data of the same state.

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Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Fusion Energy Sciences (FES)

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1364024

Journal Information:: Journal of Physical Chemistry Letters, Vol. 8, Issue 12; ISSN 1948-7185

Publisher:: American Chemical SocietyCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 28 works

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References (45)

X-ray Absorption and Emission Study of Dioxygen Activation by a Small-Molecule Manganese Complex Rees, Julian A.; Martin-Diaconescu, Vlad; Kovacs, Julie A. Inorganic Chemistry, Vol. 54, Issue 13 https://doi.org/10.1021/acs.inorgchem.5b00699	journal	June 2015
A Highly Reactive Mononuclear Non-Heme Manganese(IV)–Oxo Complex That Can Activate the Strong C–H Bonds of Alkanes Wu, Xiujuan; Seo, Mi Sook; Davis, Katherine M. Journal of the American Chemical Society, Vol. 133, Issue 50 https://doi.org/10.1021/ja208523u	journal	December 2011
Photosystem II: Structure and mechanism of the water:plastoquinone oxidoreductase Kern, Jan; Renger, Gernot Photosynthesis Research, Vol. 94, Issue 2-3 https://doi.org/10.1007/s11120-007-9201-1	journal	July 2007
A Mononuclear Non-Heme Manganese(IV)–Oxo Complex Binding Redox-Inactive Metal Ions Chen, Junying; Lee, Yong-Min; Davis, Katherine M. Journal of the American Chemical Society, Vol. 135, Issue 17 https://doi.org/10.1021/ja312113p	journal	January 2013
Mn K-Edge X-ray Absorption Studies of Oxo- and Hydroxo-manganese(IV) Complexes: Experimental and Theoretical Insights into Pre-Edge Properties Leto, Domenick F.; Jackson, Timothy A. Inorganic Chemistry, Vol. 53, Issue 12 https://doi.org/10.1021/ic5006902	journal	May 2014
Activation of a water molecule using a mononuclear Mn complex: from Mn-aquo, to Mn-hydroxo, to Mn-oxyl via charge compensation Lassalle-Kaiser, Benedikt; Hureau, Christelle; Pantazis, Dimitrios A. Energy & Environmental Science, Vol. 3, Issue 7 https://doi.org/10.1039/b926990h	journal	January 2010
Geometric and Electronic Structure of the Mn(IV)Fe(III) Cofactor in Class Ic Ribonucleotide Reductase: Correlation to the Class Ia Binuclear Non-Heme Iron Enzyme Kwak, Yeonju; Jiang, Wei; Dassama, Laura M. K. Journal of the American Chemical Society, Vol. 135, Issue 46 https://doi.org/10.1021/ja409510d	journal	November 2013
Dimanganese catalase—spectroscopic parameters from broken-symmetry density functional theory of the superoxidized MnIII/MnIV state Sinnecker, Sebastian; Neese, Frank; Lubitz, Wolfgang JBIC Journal of Biological Inorganic Chemistry, Vol. 10, Issue 3 https://doi.org/10.1007/s00775-005-0633-9	journal	April 2005
Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å Umena, Yasufumi; Kawakami, Keisuke; Shen, Jian-Ren Nature, Vol. 473, Issue 7345 https://doi.org/10.1038/nature09913	journal	April 2011
Light-induced structural changes and the site of O=O bond formation in PSII caught by XFEL Suga, Michihiro; Akita, Fusamichi; Sugahara, Michihiro Nature, Vol. 543, Issue 7643 https://doi.org/10.1038/nature21400	journal	February 2017
Absence of Mn-Centered Oxidation in the S₂ → S₃ Transition: Implications for the Mechanism of Photosynthetic Water Oxidation Messinger, Johannes; Robblee, John H.; Bergmann, Uwe Journal of the American Chemical Society, Vol. 123, Issue 32 https://doi.org/10.1021/ja004307+	journal	July 2001
Room-Temperature Energy-Sampling Kβ X-ray Emission Spectroscopy of the Mn ₄ Ca Complex of Photosynthesis Reveals Three Manganese-Centered Oxidation Steps and Suggests a Coordination Change Prior to O ₂ Formation Zaharieva, Ivelina; Chernev, Petko; Berggren, Gustav Biochemistry, Vol. 55, Issue 30 https://doi.org/10.1021/acs.biochem.6b00491	journal	July 2016
Photosynthetic O2 Formation Tracked by Time-Resolved X-ray Experiments Haumann, M. Science, Vol. 310, Issue 5750 https://doi.org/10.1126/science.1117551	journal	November 2005
Structural Changes of the Oxygen-evolving Complex in Photosystem II during the Catalytic Cycle Glöckner, Carina; Kern, Jan; Broser, Matthias Journal of Biological Chemistry, Vol. 288, Issue 31 https://doi.org/10.1074/jbc.M113.476622	journal	June 2013
Simultaneous Femtosecond X-ray Spectroscopy and Diffraction of Photosystem II at Room Temperature Kern, J.; Alonso-Mori, R.; Tran, R. Science, Vol. 340, Issue 6131 https://doi.org/10.1126/science.1234273	journal	February 2013
X-ray Emission Spectroscopy of Mn Coordination Complexes Toward Interpreting the Electronic Structure of the Oxygen-Evolving Complex of Photosystem II Davis, Katherine M.; Palenik, Mark C.; Yan, Lifen The Journal of Physical Chemistry C, Vol. 120, Issue 6 https://doi.org/10.1021/acs.jpcc.5b10610	journal	February 2016
Mn K-Edge XANES and Kβ XES Studies of Two Mn−Oxo Binuclear Complexes: Investigation of Three Different Oxidation States Relevant to the Oxygen-Evolving Complex of Photosystem II Visser, Hendrik; Anxolabéhère-Mallart, Elodie; Bergmann, Uwe Journal of the American Chemical Society, Vol. 123, Issue 29 https://doi.org/10.1021/ja004306h	journal	July 2001
Mn oxidation states in tri- and tetra-nuclear Mn compounds structurally relevant to photosystem II: Mn K-edge X-ray absorption and K? X-ray emission spectroscopy studies PizarroCurrent address: Sandia Nati, Shelly A.; Glatzel, Pieter; VisserCurrent address: California I., Hendrik Physical Chemistry Chemical Physics, Vol. 6, Issue 20 https://doi.org/10.1039/b407513g	journal	January 2004
High-spin Mn–oxo complexes and their relevance to the oxygen-evolving complex within photosystem II Gupta, Rupal; Taguchi, Taketo; Lassalle-Kaiser, Benedikt Proceedings of the National Academy of Sciences, Vol. 112, Issue 17 https://doi.org/10.1073/pnas.1422800112	journal	April 2015
High resolution 1s core hole X-ray spectroscopy in 3d transition metal complexes—electronic and structural information Glatzel, Pieter; Bergmann, Uwe Coordination Chemistry Reviews, Vol. 249, Issue 1-2 https://doi.org/10.1016/j.ccr.2004.04.011	journal	January 2005
X-ray Mn $K β$ emission spectra of manganese oxides and manganates Tsutsumi, Kenjiro; Nakamori, Hiroo; Ichikawa, Kouichi Physical Review B, Vol. 13, Issue 2 https://doi.org/10.1103/PhysRevB.13.929	journal	January 1976
High-resolution manganese x-ray fluorescence spectroscopy. Oxidation-state and spin-state sensitivity Peng, G.; deGroot, F. M. F.; Haemaelaeinen, K. Journal of the American Chemical Society, Vol. 116, Issue 7 https://doi.org/10.1021/ja00086a024	journal	April 1994
Direct Detection of Oxygen Ligation to the Mn4Ca Cluster of Photosystem II by X-ray Emission Spectroscopy Pushkar, Yulia; Long, Xi; Glatzel, Pieter Angewandte Chemie International Edition, Vol. 49, Issue 4 https://doi.org/10.1002/anie.200905366	journal	December 2009
Electronic Structural Changes of Mn in the Oxygen-Evolving Complex of Photosystem II during the Catalytic Cycle Glatzel, Pieter; Schroeder, Henning; Pushkar, Yulia Inorganic Chemistry, Vol. 52, Issue 10 https://doi.org/10.1021/ic4005938	journal	April 2013
A multi-crystal wavelength dispersive x-ray spectrometer Alonso-Mori, Roberto; Kern, Jan; Sokaras, Dimosthenis Review of Scientific Instruments, Vol. 83, Issue 7 https://doi.org/10.1063/1.4737630	journal	July 2012
Methods development for diffraction and spectroscopy studies of metalloenzymes at X-ray free-electron lasers Kern, Jan; Hattne, Johan; Tran, Rosalie Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 369, Issue 1647 https://doi.org/10.1098/rstb.2013.0590	journal	July 2014
Röntgenspektroskopie und Abbildung mittels gekrümmter Kristallreflektoren. I. Geometrisch-optische Betrachtungen v. Hámos, L. Annalen der Physik, Vol. 409, Issue 6 https://doi.org/10.1002/andp.19334090608	journal	January 1933
A von Hamos x-ray spectrometer based on a segmented-type diffraction crystal for single-shot x-ray emission spectroscopy and time-resolved resonant inelastic x-ray scattering studies Szlachetko, J.; Nachtegaal, M.; de Boni, E. Review of Scientific Instruments, Vol. 83, Issue 10 https://doi.org/10.1063/1.4756691	journal	October 2012
Fast Detection Allowing Analysis of Metalloprotein Electronic Structure by X-ray Emission Spectroscopy at Room Temperature Davis, Katherine M.; Mattern, Brian A.; Pacold, Joseph I. The Journal of Physical Chemistry Letters, Vol. 3, Issue 14 https://doi.org/10.1021/jz3006223	journal	June 2012
Synthesis, Characterization, and Solution Properties of a Novel Cross-Bridged Cyclam Manganese(IV) Complex Having Two Terminal Hydroxo Ligands Yin, Guochuan; McCormick, James M.; Buchalova, Maria Inorganic Chemistry, Vol. 45, Issue 20 https://doi.org/10.1021/ic0521123	journal	October 2006
Kinetic Modeling of the X-ray-Induced Damage to a Metalloprotein Davis, Katherine M.; Kosheleva, Irina; Henning, Robert W. The Journal of Physical Chemistry B, Vol. 117, Issue 31 https://doi.org/10.1021/jp403654n	journal	July 2013
Probing the 3d Spin Momentum with X-ray Emission Spectroscopy: The Case of Molecular-Spin Transitions Vankó, György; Neisius, Thomas; Molnár, Gábor The Journal of Physical Chemistry B, Vol. 110, Issue 24 https://doi.org/10.1021/jp0615961	journal	June 2006
Uncovering the Role of Oxygen Atom Transfer in Ru-Based Catalytic Water Oxidation Moonshiram, Dooshaye; Pineda-Galvan, Yuliana; Erdman, Darren Journal of the American Chemical Society, Vol. 138, Issue 48 https://doi.org/10.1021/jacs.6b08409	journal	November 2016
Spectroscopic Analysis of Catalytic Water Oxidation by [Ru ^II (bpy)(tpy)H ₂ O] ²⁺ Suggests That Ru ^V ═O Is Not a Rate-Limiting Intermediate Pushkar, Yulia; Moonshiram, Dooshaye; Purohit, Vatsal Journal of the American Chemical Society, Vol. 136, Issue 34 https://doi.org/10.1021/ja506586b	journal	August 2014
Experimental demonstration of radicaloid character in a RuV=O intermediate in catalytic water oxidation Moonshiram, D.; Alperovich, I.; Concepcion, J. J. Proceedings of the National Academy of Sciences, Vol. 110, Issue 10 https://doi.org/10.1073/pnas.1222102110	journal	February 2013
Molecular Catalysts for Water Oxidation Blakemore, James D.; Crabtree, Robert H.; Brudvig, Gary W. Chemical Reviews, Vol. 115, Issue 23 https://doi.org/10.1021/acs.chemrev.5b00122	journal	July 2015
Mononuclear ruthenium polypyridine complexes that catalyze water oxidation Tong, Lianpeng; Thummel, Randolph P. Chemical Science, Vol. 7, Issue 11 https://doi.org/10.1039/C6SC02766K	journal	January 2016
COOPERATION OF CHARGES IN PHOTOSYNTHETIC O ₂ EVOLUTION–I. A LINEAR FOUR STEP MECHANISM Kok, Bessel; Forbush, Bliss; McGLOIN, Marion Photochemistry and Photobiology, Vol. 11, Issue 6 https://doi.org/10.1111/j.1751-1097.1970.tb06017.x	journal	June 1970
Structural changes in the Mn4Ca cluster and the mechanism of photosynthetic water splitting Pushkar, Y.; Yano, J.; Sauer, K. Proceedings of the National Academy of Sciences, Vol. 105, Issue 6 https://doi.org/10.1073/pnas.0707092105	journal	February 2008
Structural Change of the Mn Cluster during the S ₂ →S ₃ State Transition of the Oxygen-Evolving Complex of Photosystem II. Does It Reflect the Onset of Water/Substrate Oxidation? Determination by Mn X-ray Absorption Spectroscopy Liang, Wenchuan; Roelofs, Theo A.; Cinco, Roehl M. Journal of the American Chemical Society, Vol. 122, Issue 14 https://doi.org/10.1021/ja992501u	journal	April 2000
Serial time-resolved crystallography of photosystem II using a femtosecond X-ray laser Kupitz, Christopher; Basu, Shibom; Grotjohann, Ingo Nature, Vol. 513, Issue 7517 https://doi.org/10.1038/nature13453	journal	July 2014
Structure of photosystem II and substrate binding at room temperature Young, Iris D.; Ibrahim, Mohamed; Chatterjee, Ruchira Nature, Vol. 540, Issue 7633 https://doi.org/10.1038/nature20161	journal	November 2016
Electronic structure of the oxygen-evolving complex in photosystem II prior to O-O bond formation Cox, N.; Retegan, M.; Neese, F. Science, Vol. 345, Issue 6198 https://doi.org/10.1126/science.1254910	journal	August 2014
Analysis of the Reaction Coordinate of Photosynthetic Water Oxidation by Kinetic Measurements of 355 nm Absorption Changes at Different Temperatures in Photosystem II Preparations Suspended in Either H ₂ O or D ₂ O ^† Karge, Marc; Irrgang, Klaus-Dieter; Renger, Gernot Biochemistry, Vol. 36, Issue 29 https://doi.org/10.1021/bi962342g	journal	July 1997
Substrate–water exchange in photosystem II is arrested before dioxygen formation Nilsson, Håkan; Rappaport, Fabrice; Boussac, Alain Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms5305	journal	July 2014

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Explaining the Different Geometries of the Water Oxidising Complex in the Nominal S ₃ State Crystal Structures of Photosystem II at 2.25 Å and 2.35 Å Petrie, Simon; Stranger, Robert; Pace, Ron J. ChemPhysChem, Vol. 19, Issue 23 https://doi.org/10.1002/cphc.201800686	journal	October 2018
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