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Title: The exchange of the fast substrate water in the S 2 state of photosystem II is limited by diffusion of bulk water through channels – implications for the water oxidation mechanism

Abstract

The molecular oxygen we breathe is produced from water-derived oxygen species bound to the Mn4CaO5 cluster in photosystem II (PSII). Present research points to the central oxo-bridge O5 as the ‘slow exchanging substrate water (Ws)’, while, in the S2 state, the terminal water ligands W2 and W3 are both discussed as the ‘fast exchanging substrate water (Wf)’. A critical point for the assignment of Wf is whether or not its exchange with bulk water is limited by barriers in the channels leading to the Mn4CaO5 cluster. In this study, we measured the rates of H216O/H218O substrate water exchange in the S2 and S3 states of PSII core complexes from wild-type (WT) Synechocystis sp. PCC 6803, and from two mutants, D1-D61A and D1-E189Q, that are expected to alter water access via the Cl1/O4 channels and the O1 channel, respectively. We found that the exchange rates of Wf and Ws were unaffected by the E189Q mutation (O1 channel), but strongly perturbed by the D61A mutation (Cl1/O4 channel). It is concluded that all channels have restrictions limiting the isotopic equilibration of the inner water pool near the Mn4CaO5 cluster, and that D61 participates in one such barrier. In the D61A mutant this barriermore » is lowered so that Wf exchange occurs more rapidly. This finding removes the main argument against Ca-bound W3 as fast substrate water in the S2 state, namely the indifference of the rate of Wf exchange towards Ca/Sr substitution.« less

Authors:
ORCiD logo [1];  [2]; ORCiD logo [3]; ORCiD logo [2]; ORCiD logo [1]
+ Show Author Affiliations
  1. Department of Chemistry, Umeå University, Linnaeus väg 6 (KBC huset), SE-901 87, Umeå, Sweden, Molecular Biomimetics, Department of Chemistry – Ångström Laboratory, Uppsala University, POB 523, SE-75120 Uppsala, Sweden
  2. Department of Biochemistry, University of California, Riverside, California 92521, USA
  3. Molecular Biomimetics, Department of Chemistry – Ångström Laboratory, Uppsala University, POB 523, SE-75120 Uppsala, Sweden
Publication Date:
Research Org.:
Univ. of California, Riverside, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC); ÅForsk; Vetenskapsrådet
OSTI Identifier:
1818794
Alternate Identifier(s):
OSTI ID: 1904513
Grant/Contract Number:  
SC0005291; 2016-051832020-03809
Resource Type:
Published Article
Journal Name:
Chemical Science
Additional Journal Information:
Journal Name: Chemical Science Journal Volume: 12 Journal Issue: 38; Journal ID: ISSN 2041-6520
Publisher:
Royal Society of Chemistry (RSC)
Country of Publication:
United Kingdom
Language:
English
Subject:
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY

Citation Formats

de Lichtenberg, Casper, Kim, Christopher J., Chernev, Petko, Debus, Richard J., and Messinger, Johannes. The exchange of the fast substrate water in the S 2 state of photosystem II is limited by diffusion of bulk water through channels – implications for the water oxidation mechanism. United Kingdom: N. p., 2021. Web. doi:10.1039/D1SC02265B.
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de Lichtenberg, Casper, Kim, Christopher J., Chernev, Petko, Debus, Richard J., & Messinger, Johannes. The exchange of the fast substrate water in the S 2 state of photosystem II is limited by diffusion of bulk water through channels – implications for the water oxidation mechanism. United Kingdom. https://doi.org/10.1039/D1SC02265B
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de Lichtenberg, Casper, Kim, Christopher J., Chernev, Petko, Debus, Richard J., and Messinger, Johannes. Wed . "The exchange of the fast substrate water in the S 2 state of photosystem II is limited by diffusion of bulk water through channels – implications for the water oxidation mechanism". United Kingdom. https://doi.org/10.1039/D1SC02265B.
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@article{osti_1818794,
title = {The exchange of the fast substrate water in the S 2 state of photosystem II is limited by diffusion of bulk water through channels – implications for the water oxidation mechanism},
author = {de Lichtenberg, Casper and Kim, Christopher J. and Chernev, Petko and Debus, Richard J. and Messinger, Johannes},
abstractNote = {The molecular oxygen we breathe is produced from water-derived oxygen species bound to the Mn4CaO5 cluster in photosystem II (PSII). Present research points to the central oxo-bridge O5 as the ‘slow exchanging substrate water (Ws)’, while, in the S2 state, the terminal water ligands W2 and W3 are both discussed as the ‘fast exchanging substrate water (Wf)’. A critical point for the assignment of Wf is whether or not its exchange with bulk water is limited by barriers in the channels leading to the Mn4CaO5 cluster. In this study, we measured the rates of H216O/H218O substrate water exchange in the S2 and S3 states of PSII core complexes from wild-type (WT) Synechocystis sp. PCC 6803, and from two mutants, D1-D61A and D1-E189Q, that are expected to alter water access via the Cl1/O4 channels and the O1 channel, respectively. We found that the exchange rates of Wf and Ws were unaffected by the E189Q mutation (O1 channel), but strongly perturbed by the D61A mutation (Cl1/O4 channel). It is concluded that all channels have restrictions limiting the isotopic equilibration of the inner water pool near the Mn4CaO5 cluster, and that D61 participates in one such barrier. In the D61A mutant this barrier is lowered so that Wf exchange occurs more rapidly. This finding removes the main argument against Ca-bound W3 as fast substrate water in the S2 state, namely the indifference of the rate of Wf exchange towards Ca/Sr substitution.},
doi = {10.1039/D1SC02265B},
journal = {Chemical Science},
number = 38,
volume = 12,
place = {United Kingdom},
year = {Wed Oct 06 00:00:00 EDT 2021},
month = {Wed Oct 06 00:00:00 EDT 2021}
}
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