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Title: Reactive oxygen species leave a damage trail that reveals water channels in Photosystem II

Abstract

Photosystem II (PSII), a unique membrane-bound oxidoreductase, catalyzes light-driven oxidation of water to molecular oxygen. Although high-resolution structures of PSII are known, the exact path of the substrate water molecules to the catalytic Mn 4CaO 5 center within the PSII complex remains poorly understood. PSII produces reactive oxygen species (ROS), responsible for the frequent damage and turnover of this megacomplex that occur under physiological conditions. Such ROS are known to specifically modify PSII proteins. Using high-resolution tandem mass spectrometry, we identified oxidative modifications on 36 amino acid residues on the lumenal side of PSII, in the core PSII proteins D1, D2, and CP43 of the cyanobacterium Synechocystis sp. PCC 6803. Remarkably, these oxidized residues clustered into three nearly continuous formations, tracking the pathways of ROS diffusion from the manganese center all the way out to the surface of PSII. We suggest that these profiles of oxidized residues reveal the locations of water channels within PSII. Our results provide the most comprehensive experimental evidence to date of physiologically relevant oxidized residues in PSII and illuminate three possible channels for water between the catalytic Mn cluster in the PSII complex and the bulk medium around it

Authors:
ORCiD logo [1]; ORCiD logo [1]; ORCiD logo [1]
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  1. Washington Univ., St. Louis, MO (United States)
Publication Date:
Research Org.:
Washington Univ., St. Louis, MO (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22). Chemical Sciences, Geosciences & Biosciences Division
OSTI Identifier:
1499939
Grant/Contract Number:  
FG02-99ER20350; SC0001035
Resource Type:
Accepted Manuscript
Journal Name:
Science Advances
Additional Journal Information:
Journal Volume: 3; Journal Issue: 11; Journal ID: ISSN 2375-2548
Publisher:
AAAS
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY

Citation Formats

Weisz, Daniel A., Gross, Michael L., and Pakrasi, Himadri B. Reactive oxygen species leave a damage trail that reveals water channels in Photosystem II. United States: N. p., 2017. Web. doi:10.1126/sciadv.aao3013.
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Weisz, Daniel A., Gross, Michael L., & Pakrasi, Himadri B. Reactive oxygen species leave a damage trail that reveals water channels in Photosystem II. United States. doi:10.1126/sciadv.aao3013.
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Weisz, Daniel A., Gross, Michael L., and Pakrasi, Himadri B. Fri . "Reactive oxygen species leave a damage trail that reveals water channels in Photosystem II". United States. doi:10.1126/sciadv.aao3013. https://www.osti.gov/servlets/purl/1499939.
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@article{osti_1499939,
title = {Reactive oxygen species leave a damage trail that reveals water channels in Photosystem II},
author = {Weisz, Daniel A. and Gross, Michael L. and Pakrasi, Himadri B.},
abstractNote = {Photosystem II (PSII), a unique membrane-bound oxidoreductase, catalyzes light-driven oxidation of water to molecular oxygen. Although high-resolution structures of PSII are known, the exact path of the substrate water molecules to the catalytic Mn4CaO5 center within the PSII complex remains poorly understood. PSII produces reactive oxygen species (ROS), responsible for the frequent damage and turnover of this megacomplex that occur under physiological conditions. Such ROS are known to specifically modify PSII proteins. Using high-resolution tandem mass spectrometry, we identified oxidative modifications on 36 amino acid residues on the lumenal side of PSII, in the core PSII proteins D1, D2, and CP43 of the cyanobacterium Synechocystis sp. PCC 6803. Remarkably, these oxidized residues clustered into three nearly continuous formations, tracking the pathways of ROS diffusion from the manganese center all the way out to the surface of PSII. We suggest that these profiles of oxidized residues reveal the locations of water channels within PSII. Our results provide the most comprehensive experimental evidence to date of physiologically relevant oxidized residues in PSII and illuminate three possible channels for water between the catalytic Mn cluster in the PSII complex and the bulk medium around it},
doi = {10.1126/sciadv.aao3013},
journal = {Science Advances},
number = 11,
volume = 3,
place = {United States},
year = {2017},
month = {11}
}
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DOI:  10.1126/sciadv.aao3013
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Figures / Tables:

Fig. 1. Fig. 1.: Example of product-ion (MS/MS) spectra that identify oxidative modifications of PSII residues. Product-ion (MS/MS) spectra of the oxidized CP43 peptide 362GPwLEPLRGPNGLDLD378K (top) and the unmodified form of the peptide (bottom). The oxidation (+15.9949 Da) was localized to 364W. Note that 372N contains the common deamidation modification (+0.9840 Da)more » according to both spectra. The fragment maps and corresponding labeled b- and y-ions show the convincing fragmentation series obtained at high mass accuracy (~0.02 Da), allowing highly confident peptide identification and unambiguous residue-level localization of the oxidative modification. Lowercase lettering in the amino acid sequence indicates the site of oxidation (see figs. S1 to S3 for additional example spectra). m/z, mass/charge ratio.« less
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