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Title: Binding of the substrate analog methanol in the oxygen-evolving complex of photosystem II in the D1-N87A genetic variant of cyanobacteria

Abstract

The solar water-splitting protein complex, photosystem II (PSII), catalyzes one of the most energetically demanding reactions in nature by using light energy to drive a catalyst capable of oxidizing water. The water oxidation reaction is catalyzed at the Mn4Ca-oxo cluster in the oxygen-evolving complex (OEC), which cycles through five light-driven S-state intermediates (S0–S4). A detailed mechanism of the reaction remains elusive as it requires knowledge of the delivery and binding of substrate water in the higher S-state intermediates. In this paper, we use two-dimensional (2D) hyperfine sublevel correlation spectroscopy, in conjunction with quantum mechanics/molecular mechanics (QM/MM) and density functional theory (DFT), to probe the binding of the substrate analog, methanol, in the S2 state of the D1-N87A variant of PSII from Synechocystis sp. PCC 6803. The results indicate that the size and specificity of the “narrow” channel is altered in D1-N87A PSII, allowing for the binding of deprotonated 13C-labeled methanol at the Mn4(IV) ion of the catalytic cluster in the S2 state. This has important implications on the mechanistic models for water oxidation in PSII.

Authors:
 [1];  [2];  [2];  [2];  [1];  [2]; ORCiD logo [2]; ORCiD logo [1]
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  1. Rensselaer Polytechnic Inst., Troy, NY (United States)
  2. Yale Univ., New Haven, CT (United States)
Publication Date:
Research Org.:
Yale Univ., New Haven, CT (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1860619
Alternate Identifier(s):
OSTI ID: 1844805
Grant/Contract Number:  
FG02-05ER15646; FG02-07ER15903; FG0205ER15646; SC0001423
Resource Type:
Accepted Manuscript
Journal Name:
Faraday Discussions
Additional Journal Information:
Journal Volume: 234; Journal ID: ISSN 1359-6640
Publisher:
Royal Society of Chemistry
Country of Publication:
United States
Language:
English
Subject:
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; Photosystem II; oxygen-evolving complex; oxygen evolution; S2 state; substrate binding; methanol; EPR spectroscopy; HYSCORE spectroscopy

Citation Formats

Kalendra, Vidmantas, Reiss, Krystle M., Banerjee, Gourab, Ghosh, Ipsita, Baldansuren, Amgalanbaatar, Batista, Victor S., Brudvig, Gary W., and Lakshmi, K. V. Binding of the substrate analog methanol in the oxygen-evolving complex of photosystem II in the D1-N87A genetic variant of cyanobacteria. United States: N. p., 2022. Web. doi:10.1039/d1fd00094b.
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Kalendra, Vidmantas, Reiss, Krystle M., Banerjee, Gourab, Ghosh, Ipsita, Baldansuren, Amgalanbaatar, Batista, Victor S., Brudvig, Gary W., & Lakshmi, K. V. Binding of the substrate analog methanol in the oxygen-evolving complex of photosystem II in the D1-N87A genetic variant of cyanobacteria. United States. https://doi.org/10.1039/d1fd00094b
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Kalendra, Vidmantas, Reiss, Krystle M., Banerjee, Gourab, Ghosh, Ipsita, Baldansuren, Amgalanbaatar, Batista, Victor S., Brudvig, Gary W., and Lakshmi, K. V. Fri . "Binding of the substrate analog methanol in the oxygen-evolving complex of photosystem II in the D1-N87A genetic variant of cyanobacteria". United States. https://doi.org/10.1039/d1fd00094b. https://www.osti.gov/servlets/purl/1860619.
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@article{osti_1860619,
title = {Binding of the substrate analog methanol in the oxygen-evolving complex of photosystem II in the D1-N87A genetic variant of cyanobacteria},
author = {Kalendra, Vidmantas and Reiss, Krystle M. and Banerjee, Gourab and Ghosh, Ipsita and Baldansuren, Amgalanbaatar and Batista, Victor S. and Brudvig, Gary W. and Lakshmi, K. V.},
abstractNote = {The solar water-splitting protein complex, photosystem II (PSII), catalyzes one of the most energetically demanding reactions in nature by using light energy to drive a catalyst capable of oxidizing water. The water oxidation reaction is catalyzed at the Mn4Ca-oxo cluster in the oxygen-evolving complex (OEC), which cycles through five light-driven S-state intermediates (S0–S4). A detailed mechanism of the reaction remains elusive as it requires knowledge of the delivery and binding of substrate water in the higher S-state intermediates. In this paper, we use two-dimensional (2D) hyperfine sublevel correlation spectroscopy, in conjunction with quantum mechanics/molecular mechanics (QM/MM) and density functional theory (DFT), to probe the binding of the substrate analog, methanol, in the S2 state of the D1-N87A variant of PSII from Synechocystis sp. PCC 6803. The results indicate that the size and specificity of the “narrow” channel is altered in D1-N87A PSII, allowing for the binding of deprotonated 13C-labeled methanol at the Mn4(IV) ion of the catalytic cluster in the S2 state. This has important implications on the mechanistic models for water oxidation in PSII.},
doi = {10.1039/d1fd00094b},
journal = {Faraday Discussions},
number = ,
volume = 234,
place = {United States},
year = {Fri Feb 11 00:00:00 EST 2022},
month = {Fri Feb 11 00:00:00 EST 2022}
}
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