Two-dimensional 67 Zn HYSCORE spectroscopy reveals that a Zn-bacteriochlorophyll a P ′ dimer is the primary donor (P 840 ) in the type-1 reaction centers of Chloracidobacterium thermophilum
Abstract
Using pulsed EPR spectroscopy and isotopic labeling we demonstrate that reaction centers of Chloracidobacterium thermophilum have an unusual primary donor that is a dimer of Zn-bacteriochlorophyll a P ′ molecules.
- Authors:
-
- Departments of Chemistry and Physics and The Baruch ’60 Center for Biochemical Solar Energy Research, Rensselaer Polytechnic Institute, Troy, USA
- Department of Biochemistry and Molecular Biology, The Pennsylvania State University, State College, USA
- Department of Chemistry, Brock University, St. Catharines, Canada
- Department of Biochemistry and Molecular Biology, The Pennsylvania State University, State College, USA, Department of Chemistry
- Department of Biochemistry and Molecular Biology, The Pennsylvania State University, State College, USA, Department of Chemistry and Biochemistry
- Publication Date:
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1603806
- Grant/Contract Number:
- FG02-07ER15903; FG02-94ER20137; SC0010575
- Resource Type:
- Publisher's Accepted Manuscript
- Journal Name:
- Physical Chemistry Chemical Physics. PCCP (Print)
- Additional Journal Information:
- Journal Name: Physical Chemistry Chemical Physics. PCCP (Print) Journal Volume: 22 Journal Issue: 11; Journal ID: ISSN 1463-9076
- Publisher:
- Royal Society of Chemistry (RSC)
- Country of Publication:
- United Kingdom
- Language:
- English
Citation Formats
Charles, Philip, Kalendra, Vidmantas, He, Zhihui, Khatami, Mohammad Hassan, Golbeck, John H., van der Est, Art, Lakshmi, K. V., and Bryant, Donald A. Two-dimensional 67 Zn HYSCORE spectroscopy reveals that a Zn-bacteriochlorophyll a P ′ dimer is the primary donor (P 840 ) in the type-1 reaction centers of Chloracidobacterium thermophilum. United Kingdom: N. p., 2020.
Web. doi:10.1039/C9CP06556C.
Charles, Philip, Kalendra, Vidmantas, He, Zhihui, Khatami, Mohammad Hassan, Golbeck, John H., van der Est, Art, Lakshmi, K. V., & Bryant, Donald A. Two-dimensional 67 Zn HYSCORE spectroscopy reveals that a Zn-bacteriochlorophyll a P ′ dimer is the primary donor (P 840 ) in the type-1 reaction centers of Chloracidobacterium thermophilum. United Kingdom. https://doi.org/10.1039/C9CP06556C
Charles, Philip, Kalendra, Vidmantas, He, Zhihui, Khatami, Mohammad Hassan, Golbeck, John H., van der Est, Art, Lakshmi, K. V., and Bryant, Donald A. Wed .
"Two-dimensional 67 Zn HYSCORE spectroscopy reveals that a Zn-bacteriochlorophyll a P ′ dimer is the primary donor (P 840 ) in the type-1 reaction centers of Chloracidobacterium thermophilum". United Kingdom. https://doi.org/10.1039/C9CP06556C.
@article{osti_1603806,
title = {Two-dimensional 67 Zn HYSCORE spectroscopy reveals that a Zn-bacteriochlorophyll a P ′ dimer is the primary donor (P 840 ) in the type-1 reaction centers of Chloracidobacterium thermophilum},
author = {Charles, Philip and Kalendra, Vidmantas and He, Zhihui and Khatami, Mohammad Hassan and Golbeck, John H. and van der Est, Art and Lakshmi, K. V. and Bryant, Donald A.},
abstractNote = {Using pulsed EPR spectroscopy and isotopic labeling we demonstrate that reaction centers of Chloracidobacterium thermophilum have an unusual primary donor that is a dimer of Zn-bacteriochlorophyll a P ′ molecules.},
doi = {10.1039/C9CP06556C},
journal = {Physical Chemistry Chemical Physics. PCCP (Print)},
number = 11,
volume = 22,
place = {United Kingdom},
year = {2020},
month = {3}
}
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https://doi.org/10.1039/C9CP06556C
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Works referenced in this record:
Determination of the Complete Spin Density Distribution in 13 C-Labeled Protein-Bound Radical Intermediates Using Advanced 2D Electron Paramagnetic Resonance Spectroscopy and Density Functional Theory
journal, October 2017
- Taguchi, Alexander T.; O’Malley, Patrick J.; Wraight, Colin A.
- The Journal of Physical Chemistry B, Vol. 121, Issue 44
Alteration of the H-Bond to the A 1A Phylloquinone in Photosystem I: Influence on the Kinetics and Energetics of Electron Transfer
journal, March 2011
- Srinivasan, Nithya; Santabarbara, Stefano; Rappaport, Fabrice
- The Journal of Physical Chemistry B, Vol. 115, Issue 8
Zinc-67 NMR study of tetrahedral and octahedral zinc sites with symmetrical oxygen, nitrogen, and sulfur ligands
journal, November 1999
- Sham, Simon; Wu, Gang
- Canadian Journal of Chemistry, Vol. 77, Issue 11
Discovery of Natural Photosynthesis using Zn-Containing Bacteriochlorophyll in an Aerobic Bacterium Acidiphilium rubrum
journal, September 1996
- Wakao, N.; Yokoi, N.; Isoyama, N.
- Plant and Cell Physiology, Vol. 37, Issue 6
Zinc Solid-State NMR Spectroscopy of Human Carbonic Anhydrase: Implications for the Enzymatic Mechanism
journal, April 2004
- Lipton, Andrew S.; Heck, Robert W.; Ellis, Paul D.
- Journal of the American Chemical Society, Vol. 126, Issue 14
Chloracidobacterium thermophilum gen. nov., sp. nov.: an anoxygenic microaerophilic chlorophotoheterotrophic acidobacterium
journal, February 2015
- Tank, M.; Bryant, D. A.
- INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 65, Issue Pt 5
EPR, ENDOR, and TRIPLE resonance studies of modified bacteriochlorophyll cation radicals
journal, January 1994
- Kaess, H.; Rautter, J.; Zweygart, W.
- The Journal of Physical Chemistry, Vol. 98, Issue 1
Structure of a symmetric photosynthetic reaction center–photosystem
journal, July 2017
- Gisriel, Christopher; Sarrou, Iosifina; Ferlez, Bryan
- Science, Vol. 357, Issue 6355
Monomeric Spin Density Distribution in the Primary Donor of Photosystem I as Determined by Electron Magnetic Resonance: Functional and Thermodynamic Implications
journal, December 1998
- Mac, Michelle; Bowlby, Neil R.; Babcock, Gerald T.
- Journal of the American Chemical Society, Vol. 120, Issue 50
Solid-State 67 Zn NMR Spectroscopic Studies and ab Initio Molecular Orbital Calculations on a Synthetic Analogue of Carbonic Anhydrase
journal, April 2003
- Lipton, Andrew S.; Bergquist, Catherine; Parkin, Gerard
- Journal of the American Chemical Society, Vol. 125, Issue 13
Characterization of the FMO protein from the aerobic chlorophototroph, Candidatus Chloracidobacterium thermophilum
journal, January 2010
- Tsukatani, Yusuke; Wen, Jianzhong; Blankenship, Robert E.
- Photosynthesis Research, Vol. 104, Issue 2-3
High-Field Solid-State 67 Zn NMR Spectroscopy of Several Zinc−Amino Acid Complexes
journal, January 2010
- Mroué, Kamal H.; Power, William P.
- The Journal of Physical Chemistry A, Vol. 114, Issue 1
Characterization of primary reactants in bacterial photosynthesis. I. Comparison of the light-induced EPR signal (g = 2.0026) with that of a bacteriochlorophyll radical
journal, May 1972
- McElroy, James D.; Feher, George; Mauzerall, David C.
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 267, Issue 2
One-electron photooxidation of porphyrins at low temperature
journal, May 1984
- Gasyna, Zbigniew; Browett, William R.; Stillman, Martin J.
- Inorganica Chimica Acta, Vol. 92, Issue 1
EPR, ENDOR, and Special TRIPLE measurements of P•+ in wild type and modified reaction centers from Rb. sphaeroides
journal, September 2008
- Allen, J. P.; Cordova, J. M.; Jolley, C. C.
- Photosynthesis Research, Vol. 99, Issue 1
Modulation effects from14N and15N nitrogen nuclei in the electron spin echo of imidazoline nitroxyl radicals containing the 2-oximinoalkyl group
journal, January 1984
- Astashkin, A. V.; Dikanov, S. A.; Tsvetkov, Yu. D.
- Journal of Structural Chemistry, Vol. 25, Issue 1
Three-dimensional structure of cyanobacterial photosystem I at 2.5 Å resolution
journal, June 2001
- Jordan, Patrick; Fromme, Petra; Witt, Horst Tobias
- Nature, Vol. 411, Issue 6840
Isolation and Characterization of Homodimeric Type-I Reaction Center Complex from Candidatus Chloracidobacterium thermophilum, an Aerobic Chlorophototroph
journal, December 2011
- Tsukatani, Yusuke; Romberger, Steven P.; Golbeck, John H.
- Journal of Biological Chemistry, Vol. 287, Issue 8
Candidatus Chloracidobacterium thermophilum: An Aerobic Phototrophic Acidobacterium
journal, July 2007
- Bryant, D. A.; Costas, A. M. G.; Maresca, J. A.
- Science, Vol. 317, Issue 5837
Identification of Histidine As an Axial Ligand to P 700 + †
journal, January 1996
- Mac, Michelle; Tang, Xiao-Song; Diner, Bruce A.
- Biochemistry, Vol. 35, Issue 41
Ultra-Wideline Solid-State NMR Spectroscopy
journal, June 2013
- Schurko, Robert W.
- Accounts of Chemical Research, Vol. 46, Issue 9
Solid-State 67 Zn NMR Spectroscopy in Bioinorganic Chemistry. Spectra of Four- and Six-Coordinate Zinc Pyrazolylborate Complexes Obtained by Management of Proton Relaxation Rates with a Paramagnetic Dopant
journal, May 2002
- Lipton, Andrew S.; Wright, Terri A.; Bowman, Michael K.
- Journal of the American Chemical Society, Vol. 124, Issue 20
The electronic structure of the primary donor cation radical in Rhodobacter sphaeroides R-26: ENDOR and TRIPLE resonance studies in single crystals of reaction centers
journal, November 1993
- Lendzian, F.; Huber, M.; Isaacson, R. A.
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1183, Issue 1
Understanding heme proteins with hyperfine spectroscopy
journal, July 2017
- Van Doorslaer, Sabine
- Journal of Magnetic Resonance, Vol. 280
Structure of cyanobacterial Photosystem I
journal, July 2005
- Grotjohann, Ingo; Fromme, Petra
- Photosynthesis Research, Vol. 85, Issue 1
High-Resolution Two-Dimensional 1 H and 14 N Hyperfine Sublevel Correlation Spectroscopy of the Primary Quinone of Photosystem II
journal, February 2011
- Chatterjee, Ruchira; Milikisiyants, Sergey; Coates, Christopher S.
- Biochemistry, Vol. 50, Issue 4
1D- and 2D-ESEEM Study of the Semiquinone Radical Q A - of Photosystem II
journal, August 1999
- Deligiannakis, Yiannis; Hanley, Jonathan; Rutherford, A. William
- Journal of the American Chemical Society, Vol. 121, Issue 33
Endor Experiments on Chlorophyll and Bacteriochlorophyll in Vitro and in the Photosynthetic unit
journal, April 1975
- Feher, G.; Hoff, A. J.; Isaacson, R. A.
- Annals of the New York Academy of Sciences, Vol. 244, Issue 1 The Biologica
Electron Spin Resonance of Chlorophyll and the Origin of Signal I in Photosynthesis
journal, March 1971
- Norris, J. R.; Uphaus, R. A.; Crespi, H. L.
- Proceedings of the National Academy of Sciences, Vol. 68, Issue 3
Pulsed electron paramagnetic resonance methods for macromolecular structure determination
journal, September 2001
- Lakshmi, K. V.; Brudvig, Gary W.
- Current Opinion in Structural Biology, Vol. 11, Issue 5
Radicals, Radical Pairs and Triplet States in Photosynthesis
journal, May 2002
- Lubitz, Wolfgang; Lendzian, Friedhelm; Bittl, Robert
- Accounts of Chemical Research, Vol. 35, Issue 5
67 Zn QCPMG Solid-State NMR Studies of Zinc Complexes as Models for Metalloproteins
journal, April 1999
- Larsen, Flemming H.; Lipton, Andrew S.; Jakobsen, Hans J.
- Journal of the American Chemical Society, Vol. 121, Issue 15
Multifrequency Pulsed Electron Paramagnetic Resonance on Metalloproteins
journal, February 2010
- Lyubenova, Sevdalina; Maly, Thorsten; Zwicker, Klaus
- Accounts of Chemical Research, Vol. 43, Issue 2
Structure of the reaction center from Rhodobacter sphaeroides R-26 and 2.4.1: protein-cofactor (bacteriochlorophyll, bacteriopheophytin, and carotenoid) interactions.
journal, November 1988
- Yeates, T. O.; Komiya, H.; Chirino, A.
- Proceedings of the National Academy of Sciences, Vol. 85, Issue 21
Recent pulsed EPR studies of the Photosystem II oxygen-evolving complex: implications as to water oxidation mechanisms
journal, April 2004
- Britt, R. David; Campbell, Kristy A.; Peloquin, Jeffrey M.
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1655
Diversity of Chlorophototrophic Bacteria Revealed in the Omics Era
journal, April 2018
- Thiel, Vera; Tank, Marcus; Bryant, Donald A.
- Annual Review of Plant Biology, Vol. 69, Issue 1
Nuclear quadrupole double resonance
journal, February 1977
- Edmonds, D. T.
- Physics Reports, Vol. 29, Issue 4
Nuclear Magnetic Resonance in Solid Zinc
journal, January 1979
- Herberg, H.; Abart, J.; Voitländer, J.
- Zeitschrift für Naturforschung A, Vol. 34, Issue 8
67 Zn NMR Chemical Shifts and Electric Field Gradients in Zinc Complexes: A Quantum Chemical Investigation
journal, March 2005
- Zhang, Yong; Mukherjee, Sujoy; Oldfield, Eric
- Journal of the American Chemical Society, Vol. 127, Issue 8
Quinones in chlorosomes of green sulfur bacteria and their role in the redox-dependent fluorescence studied in chlorosome-like bacteriochlorophyll c aggregates
journal, May 1997
- Frigaard, N. -U.; Takaichi, Shinichi; Hirota, Masamitsu
- Archives of Microbiology, Vol. 167, Issue 6
Electron spin echo envelope modulation (ESEEM) spectroscopy as a tool to investigate the coordination environment of metal centers
journal, July 2000
- Deligiannakis, Yiannis; Louloudi, Maria; Hadjiliadis, Nick
- Coordination Chemistry Reviews, Vol. 204, Issue 1
Hyperfine sublevel correlation (hyscore) spectroscopy: a 2D ESR investigation of the squaric acid radical
journal, December 1986
- Höfer, P.; Grupp, A.; Nebenführ, H.
- Chemical Physics Letters, Vol. 132, Issue 3
P ULSED EPR S PECTROSCOPY : Biological Applications
journal, October 2001
- Prisner, Thomas; Rohrer, Martin; MacMillan, Fraser
- Annual Review of Physical Chemistry, Vol. 52, Issue 1
Reaction centers of the thermophilic microaerophile, Chloracidobacterium thermophilum (Acidobacteria) I: biochemical and biophysical characterization
journal, June 2019
- He, Zhihui; Ferlez, Bryan; Kurashov, Vasily
- Photosynthesis Research, Vol. 142, Issue 1
Recent developments in solid-state nuclear magnetic resonance of quadrupolar nuclei and applications to biological systems
journal, May 1998
- Wu, Gang
- Biochemistry and Cell Biology, Vol. 76, Issue 2-3
HYSCORE Spectroscopy in the Cytochrome b 559 of the Photosystem II Reaction Center
journal, December 2003
- García-Rubio, Inés; Martínez, Jesús I.; Picorel, Rafael
- Journal of the American Chemical Society, Vol. 125, Issue 51
Effect of Hydrogen Bond Strength on the Redox Properties of Phylloquinones: A Two-Dimensional Hyperfine Sublevel Correlation Spectroscopy Study of Photosystem I
journal, May 2011
- Srinivasan, Nithya; Chatterjee, Ruchira; Milikisiyants, Sergey
- Biochemistry, Vol. 50, Issue 17
Nutrient requirements and growth physiology of the photoheterotrophic Acidobacterium, Chloracidobacterium thermophilum
journal, March 2015
- Tank, Marcus; Bryant, Donald A.
- Frontiers in Microbiology, Vol. 06
Modeling the Metal Center of Cys 4 Zinc Proteins
journal, July 2007
- Lipton, Andrew S.; Ellis, Paul D.
- Journal of the American Chemical Society, Vol. 129, Issue 29
Natural abundance solid-state 67Zn NMR characterization of microporous zinc phosphites and zinc phosphates at ultrahigh magnetic field
journal, January 2011
- Sutrisno, Andre; Liu, Li; Xu, Jun
- Physical Chemistry Chemical Physics, Vol. 13, Issue 37
Electron spin echo envelope modulation spectroscopy in photosystem I
journal, October 2001
- Deligiannakis, Yiannis; Rutherford, A. W.
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1507, Issue 1-3
2D ESEEM of the 15N-Labeled Radical Cations of Bacteriochlorophyll a and of the Primary Donor in Reaction Centers of Rhodobacter sphaeroides
journal, January 1995
- Kaess, H.; Rautter, J.; Boenigk, B.
- The Journal of Physical Chemistry, Vol. 99, Issue 1
Two-Dimensional HYSCORE Spectroscopy of Superoxidized Manganese Catalase: A Model for the Oxygen-Evolving Complex of Photosystem II
journal, March 2015
- Coates, Christopher S.; Milikisiyants, Sergey; Chatterjee, Ruchira
- The Journal of Physical Chemistry B, Vol. 119, Issue 15
Ligand Environment of the S 2 State of Photosystem II: A Study of the Hyperfine Interactions of the Tetranuclear Manganese Cluster by 2D 14 N HYSCORE Spectroscopy
journal, August 2010
- Milikisiyants, Sergey; Chatterjee, Ruchira; Weyers, Amanda
- The Journal of Physical Chemistry B, Vol. 114, Issue 33
The bacteriochlorophylla cation radical revisited. An ENDOR and TRIPLE resonance study
journal, November 1997
- Lubitz, W.; Lendzian, F.; Plato, M.
- Applied Magnetic Resonance, Vol. 13, Issue 3-4
Nitrogen-14 nuclear quadrupole resonance spectra of the coordinated amino group and of coordinated imidazole. Crystal and molecular structures of chloroglycylglycinato(imidazole)cadmium
journal, April 1980
- Ashby, Carol I. H.; Paton, William F.; Brown, Theodore I.
- Journal of the American Chemical Society, Vol. 102, Issue 9
A QM/MM Approach to Interpreting 67 Zn Solid-State NMR Data in Zinc Proteins
journal, May 2008
- Lipton, Andrew S.; Heck, Robert W.; Staeheli, Greg R.
- Journal of the American Chemical Society, Vol. 130, Issue 19
15N photo-CIDNP MAS NMR analysis of reaction centers of Chloracidobacterium thermophilum
journal, March 2018
- Zill, Jeremias C.; He, Zhihui; Tank, Marcus
- Photosynthesis Research, Vol. 137, Issue 2
Avogadro: an advanced semantic chemical editor, visualization, and analysis platform
journal, August 2012
- Hanwell, Marcus D.; Curtis, Donald E.; Lonie, David C.
- Journal of Cheminformatics, Vol. 4, Issue 1
EasySpin, a comprehensive software package for spectral simulation and analysis in EPR
journal, January 2006
- Stoll, Stefan; Schweiger, Arthur
- Journal of Magnetic Resonance, Vol. 178, Issue 1, p. 42-55
Theoretical Study of the 67 Zn Electric-Field-Gradient Tensors in Zinc(II) Coordination Complexes
journal, November 2002
- Ida, Ramsey; Wu, Gang
- The Journal of Physical Chemistry A, Vol. 106, Issue 46
67 Zn Solid-State NMR Spectroscopy of the Minimal DNA Binding Domain of Human Nucleotide Excision Repair Protein XPA
journal, February 2001
- Lipton, A. S.; Buchko, G. W.; Sears, J. A.
- Journal of the American Chemical Society, Vol. 123, Issue 5
Nitrogen-14 nuclear quadrupole resonance spectra of coordinated imidazole
journal, September 1978
- Ashby, Carol I. H.; Cheng, C. P.; Brown, Theodore L.
- Journal of the American Chemical Society, Vol. 100, Issue 19
Structural model and spectroscopic characteristics of the FMO antenna protein from the aerobic chlorophototroph, Candidatus Chloracidobacterium thermophilum
journal, January 2011
- Wen, Jianzhong; Tsukatani, Yusuke; Cui, Weidong
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1807, Issue 1
Ultrastructural Analysis and Identification of Envelope Proteins of "Candidatus Chloracidobacterium thermophilum" Chlorosomes
journal, September 2011
- Garcia Costas, A. M.; Tsukatani, Y.; Romberger, S. P.
- Journal of Bacteriology, Vol. 193, Issue 23
Energy and electron transfer in the photosynthetic reaction center complex of Acidiphilium rubrum containing Zn-bacteriochlorophyll a studied by femtosecond up-conversion spectroscopy
journal, January 2007
- Tomi, Tetsuo; Shibata, Yutaka; Ikeda, Yuki
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1767, Issue 1
Zinc-67 nuclear magnetic resonance spectroscopy of solids
journal, December 1998
- Wu, Gang
- Chemical Physics Letters, Vol. 298, Issue 4-6
Models for Antenna and Reaction Center Chlorophylls
journal, April 1975
- Norris, James R.; Scheer, Hugo; Katz, Joseph J.
- Annals of the New York Academy of Sciences, Vol. 244, Issue 1 The Biologica
Ligation of D1-His332 and D1-Asp170 to the Manganese Cluster of Photosystem II from Synechocystis Assessed by Multifrequency Pulse EPR Spectroscopy †
journal, August 2011
- Stich, Troy A.; Yeagle, Gregory J.; Service, Rachel J.
- Biochemistry, Vol. 50, Issue 34