Chloride facilitates&nbsp;Mn(III) formation during photoassembly of the Photosystem II oxygen-evolving complex

Russell, Brandon P.; Vinyard, David J.

doi:10.1007/s11120-021-00886-4

Chloride facilitates Mn(III) formation during photoassembly of the Photosystem II oxygen-evolving complex

Journal Article · Wed Nov 24 00:00:00 EST 2021 · Photosynthesis Research

DOI:https://doi.org/10.1007/s11120-021-00886-4· OSTI ID:2283330

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Louisiana State University, Baton Rouge, LA (United States); Louisiana State University
Louisiana State University, Baton Rouge, LA (United States)

The Mn₄Ca oxygen-evolving complex (OEC) in Photosystem II (PSII) is assembled in situ from free Mn²⁺, Ca²⁺, and water. In an early light-driven step, Mn²⁺ in a protein high-affinity site is oxidized to Mn³⁺. Using dual-mode electron paramagnetic resonance spectroscopy, we observed that Mn³⁺ accumulation increases as chloride concentration increases in spinach PSII membranes depleted of all extrinsic subunits. At physiologically relevant pH values, this effect requires the presence of calcium. Here, when combined with pH studies, we conclude that the first Mn²⁺ oxidation event in OEC assembly requires a deprotonation that is facilitated by chloride.

View Accepted Manuscript (DOE)

Research Organization:: Louisiana State University, Baton Rouge, LA (United States)

Sponsoring Organization:: Herman Frasch Fund for Chemical Research; USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division (CSGB)

Grant/Contract Number:: SC0020119

OSTI ID:: 2283330

Alternate ID(s):: OSTI ID: 1909567

Journal Information:: Photosynthesis Research, Journal Name: Photosynthesis Research Journal Issue: 3 Vol. 152; ISSN 0166-8595

Publisher:: SpringerCopyright Statement

Country of Publication:: United States

Language:: English

References (27)

Bicarbonate Coordinates to Mn3+ during Photo-Assembly of the Catalytic Mn4Ca Core of Photosynthetic Water Oxidation: EPR Characterization Dasgupta, Jyotishman; Tyryshkin, Alexei M.; Baranov, Sergei V. Applied Magnetic Resonance, Vol. 37, Issue 1-4 https://doi.org/10.1007/s00723-009-0053-z	journal	November 2009
Mn(III) species formed by the multi-copper oxidase MnxG investigated by electron paramagnetic resonance spectroscopy Tao, Lizhi; Stich, Troy A.; Soldatova, Alexandra V. JBIC Journal of Biological Inorganic Chemistry, Vol. 23, Issue 7 https://doi.org/10.1007/s00775-018-1587-z	journal	July 2018
Photoactivation of the manganese catalyst of O2 evolution. II. A two-quantum mechanism Radmer, Richard; Cheniae, George M. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 253, Issue 1 https://doi.org/10.1016/0005-2728(71)90243-X	journal	November 1971
The roles of the extrinsic subunits in Photosystem II as revealed by EPR Franzén, Lars-Gunnar; Hansson, Örjan; Andréasson, Lars-Erik Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 808, Issue 1 https://doi.org/10.1016/0005-2728(85)90040-4	journal	June 1985
Photoassembly of the water-oxidizing complex in photosystem II Dasgupta, J.; Ananyev, G.; Dismukes, G. Coordination Chemistry Reviews, Vol. 252, Issue 3-4 https://doi.org/10.1016/j.ccr.2007.08.022	journal	February 2008
EasySpin, a comprehensive software package for spectral simulation and analysis in EPR Stoll, Stefan; Schweiger, Arthur Journal of Magnetic Resonance, Vol. 178, Issue 1, p. 42-55 https://doi.org/10.1016/j.jmr.2005.08.013	journal	January 2006
Cryo-EM Structure of Monomeric Photosystem II from Synechocystis sp. PCC 6803 Lacking the Water-Oxidation Complex Gisriel, Christopher J.; Zhou, Kaifeng; Huang, Hao-Li Joule, Vol. 4, Issue 10 https://doi.org/10.1016/j.joule.2020.07.016	journal	October 2020
Rapid-Scan Time-Resolved ATR-FTIR Study on the Photoassembly of the Water-Oxidizing Mn ₄ CaO ₅ Cluster in Photosystem II Sato, Akihiko; Nakano, Yuki; Nakamura, Shin The Journal of Physical Chemistry B, Vol. 125, Issue 16 https://doi.org/10.1021/acs.jpcb.1c01624	journal	April 2021
Calcium Modulates the Photo-assembly of Photosystem II (Mn)4-Clusters by Preventing Ligation of Nonfunctional High-Valency States of Manganese Chen, Changguo; Kazimir, Janet; Cheniae, G. M. Biochemistry, Vol. 34, Issue 41 https://doi.org/10.1021/bi00041a031	journal	October 1995
Enhancement by chloride ions of photoactivation of oxygen evolution in manganese-depleted photosystem II membranes Miyao, Mitsue; Inoue, Yorinao Biochemistry, Vol. 30, Issue 22 https://doi.org/10.1021/bi00236a008	journal	June 1991
Manganese and calcium requirements for reconstitution of oxygen-evolution activity in manganese-depleted photosystem II membranes Miller, Anne Frances; Brudvig, Gary W. Biochemistry, Vol. 28, Issue 20 https://doi.org/10.1021/bi00446a033	journal	October 1989
Electron-transfer events leading to reconstitution of oxygen-evolution activity in manganese-depleted photosystem II membranes Miller, Anne Frances; Brudvig, Gary W. Biochemistry, Vol. 29, Issue 6 https://doi.org/10.1021/bi00458a007	journal	February 1990
Spectroscopic Evidence for Ca ²⁺ Involvement in the Assembly of the Mn ₄ Ca Cluster in the Photosynthetic Water-Oxidizing Complex ^† Tyryshkin, Alexei M.; Watt, Richard K.; Baranov, Sergei V. Biochemistry, Vol. 45, Issue 42 https://doi.org/10.1021/bi061495t	journal	October 2006
Chloride Regulation of Enzyme Turnover: Application to the Role of Chloride in Photosystem II Pokhrel, Ravi; McConnell, Iain L.; Brudvig, Gary W. Biochemistry, Vol. 50, Issue 14 https://doi.org/10.1021/bi2000388	journal	April 2011
The Manganese-Stabilizing Protein of Photosystem II Modifies the in Vivo Deactivation and Photoactivation Kinetics of the H ₂ O Oxidation Complex in Synechocystis sp. PCC6803 ^† Burnap, Robert L.; Qian, Ming; Pierce, Coy Biochemistry, Vol. 35, Issue 3 https://doi.org/10.1021/bi951964j	journal	January 1996
Dry-Ice Bath Based on Ethylene Glycol Mixtures Jensen, Craig M.; Lee, Do W. Journal of Chemical Education, Vol. 77, Issue 5 https://doi.org/10.1021/ed077p629	journal	May 2000
Dual-Mode EPR Detects the Initial Intermediate in Photoassembly of the Photosystem II Mn Cluster: The Influence of Amino Acid Residue 170 of the D1 Polypeptide on Mn Coordination Campbell, Kristy A.; Force, Dee Ann; Nixon, Peter J. Journal of the American Chemical Society, Vol. 122, Issue 15 https://doi.org/10.1021/ja000142t	journal	April 2000
How acidic is the lumen? Kramer, David M.; Sacksteder, Colette A.; Cruz, Jeffrey A. Photosynthesis Research, Vol. 60, Issue 2/3, p. 151-163 https://doi.org/10.1023/A:1006212014787	journal	May 1999
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
Structural insights into photosystem II assembly Zabret, Jure; Bohn, Stefan; Schuller, Sandra K. Nature Plants, Vol. 7, Issue 4 https://doi.org/10.1038/s41477-021-00895-0	journal	April 2021
Bicarbonate-induced redox tuning in Photosystem II for regulation and protection Brinkert, Katharina; De Causmaecker, Sven; Krieger-Liszkay, Anja Proceedings of the National Academy of Sciences, Vol. 113, Issue 43 https://doi.org/10.1073/pnas.1608862113	journal	October 2016
Photosystem II oxygen-evolving complex photoassembly displays an inverse H/D solvent isotope effect under chloride-limiting conditions Vinyard, David J.; Badshah, Syed Lal; Riggio, M. Rita Proceedings of the National Academy of Sciences, Vol. 116, Issue 38 https://doi.org/10.1073/pnas.1910231116	journal	September 2019
The role of Ca ²⁺ and protein scaffolding in the formation of nature’s water oxidizing complex Avramov, Anton P.; Hwang, Hong J.; Burnap, Robert L. Proceedings of the National Academy of Sciences, Vol. 117, Issue 45 https://doi.org/10.1073/pnas.2011315117	journal	October 2020
The Psb27 Protein Facilitates Manganese Cluster Assembly in Photosystem II Roose, Johnna L.; Pakrasi, Himadri B. Journal of Biological Chemistry, Vol. 283, Issue 7 https://doi.org/10.1074/jbc.M708960200	journal	December 2007
The Structure of Photosystem II and the Mechanism of Water Oxidation in Photosynthesis Shen, Jian-Ren Annual Review of Plant Biology, Vol. 66, Issue 1 https://doi.org/10.1146/annurev-arplant-050312-120129	journal	April 2015
Progress Toward a Molecular Mechanism of Water Oxidation in Photosystem II Vinyard, David J.; Brudvig, Gary W. Annual Review of Physical Chemistry, Vol. 68, Issue 1 https://doi.org/10.1146/annurev-physchem-052516-044820	journal	May 2017
Photoactivation: The Light-Driven Assembly of the Water Oxidation Complex of Photosystem II Bao, Han; Burnap, Robert L. Frontiers in Plant Science, Vol. 7 https://doi.org/10.3389/fpls.2016.00578	journal	May 2016

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59 BASIC BIOLOGICAL SCIENCES
Assembly
Electron paramagnetic resonance spectroscopy
Oxygen-evolving complex
Photosystem II

Chloride facilitates Mn(III) formation during photoassembly of the Photosystem II oxygen-evolving complex

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References (27)

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