Assessment of the Manganese Cluster's Oxidation State Via Photoactivation of Photosystem II Microcrystals

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2019 Dec 19

PMID 31848244

Citations 13

Authors

Mun Hon Cheah

Miao Zhang

Dmitry Shevela

Fikret Mamedov

Athina Zouni

Johannes Messinger

Affiliations

Soon will be listed here.

Abstract

Knowledge of the manganese oxidation states of the oxygen-evolving MnCaO cluster in photosystem II (PSII) is crucial toward understanding the mechanism of biological water oxidation. There is a 4 decade long debate on this topic that historically originates from the observation of a multiline electron paramagnetic resonance (EPR) signal with effective total spin of S = 1/2 in the singly oxidized S state of this cluster. This signal implies an overall oxidation state of either Mn(III)Mn(IV) or Mn(III)Mn(IV) for the S state. These 2 competing assignments are commonly known as "low oxidation (LO)" and "high oxidation (HO)" models of the MnCaO cluster. Recent advanced EPR and Mn K-edge X-ray spectroscopy studies converge upon the HO model. However, doubts about these assignments have been voiced, fueled especially by studies counting the number of flash-driven electron removals required for the assembly of an active MnCaO cluster starting from Mn(II) and Mn-free PSII. This process, known as photoactivation, appeared to support the LO model since the first oxygen is reported to evolve already after 7 flashes. In this study, we improved the quantum yield and sensitivity of the photoactivation experiment by employing PSII microcrystals that retained all protein subunits after complete manganese removal and by oxygen detection via a custom built thin-layer cell connected to a membrane inlet mass spectrometer. We demonstrate that 9 flashes by a nanosecond laser are required for the production of the first oxygen, which proves that the HO model provides the correct description of the MnCaO cluster's oxidation states.

Citing Articles

Conformational Flexibility of D1-Glu189: A Crucial Determinant in Substrate Water Selection, Positioning, and Stabilization within the Oxygen-Evolving Complex of Photosystem II.

Isobe H, Suzuki T, Suga M, Shen J, Yamaguchi K ACS Omega. 2024; 9(50):50041-50048.

PMID: 39713658 PMC: 11656237. DOI: 10.1021/acsomega.4c09981.

Closing Kok's cycle of nature's water oxidation catalysis.

Guo Y, He L, Ding Y, Kloo L, Pantazis D, Messinger J Nat Commun. 2024; 15(1):5982.

PMID: 39013902 PMC: 11252165. DOI: 10.1038/s41467-024-50210-6.

On the simulation and interpretation of substrate-water exchange experiments in photosynthetic water oxidation.

Chernev P, Aydin A, Messinger J Photosynth Res. 2024; 162(2-3):413-426.

PMID: 38512410 PMC: 11639282. DOI: 10.1007/s11120-024-01084-8.

Assignment of the slowly exchanging substrate water of nature's water-splitting cofactor.

de Lichtenberg C, Rapatskiy L, Reus M, Heyno E, Schnegg A, Nowaczyk M Proc Natl Acad Sci U S A. 2024; 121(11):e2319374121.

PMID: 38437550 PMC: 10945779. DOI: 10.1073/pnas.2319374121.

Comprehensive Evaluation of Models for Ammonia Binding to the Oxygen Evolving Complex of Photosystem II.

Drosou M, Pantazis D J Phys Chem B. 2024; 128(6):1333-1349.

PMID: 38299511 PMC: 10875651. DOI: 10.1021/acs.jpcb.3c06304.

References

Cheniae G, Martin I . Photoactivation of the manganese catalyst of O 2 evolution. I. Biochemical and kinetic aspects. Biochim Biophys Acta. 1971; 253(1):167-81. DOI: 10.1016/0005-2728(71)90242-8. View

Nixon P, Diner B . Aspartate 170 of the photosystem II reaction center polypeptide D1 is involved in the assembly of the oxygen-evolving manganese cluster. Biochemistry. 1992; 31(3):942-8. DOI: 10.1021/bi00118a041. View

Krewald V, Retegan M, Cox N, Messinger J, Lubitz W, DeBeer S . Metal oxidation states in biological water splitting. Chem Sci. 2018; 6(3):1676-1695. PMC: 5639794. DOI: 10.1039/c4sc03720k. View

Inoue Y . Improvement by benzoquinones of the quantum yield of photoactivation of photosynthetic oxygen evolution: direct evidence for the two-quantum mechanism. Biochemistry. 1992; 31(2):526-32. DOI: 10.1021/bi00117a032. View

Radmer R, Cheniae G . Photoactivation of the manganese catalyst of 0 2 evolution II. A two-guantum mechanism. Biochim Biophys Acta. 1971; 253(1):182-6. DOI: 10.1016/0005-2728(71)90243-x. View

Baranov S, Tyryshkin A, Katz D, Dismukes G, Ananyev G, Klimov V . Bicarbonate is a native cofactor for assembly of the manganese cluster of the photosynthetic water oxidizing complex. Kinetics of reconstitution of O2 evolution by photoactivation. Biochemistry. 2004; 43(7):2070-9. DOI: 10.1021/bi034858n. View

Kern J, Chatterjee R, Young I, Fuller F, Lassalle L, Ibrahim M . Structures of the intermediates of Kok's photosynthetic water oxidation clock. Nature. 2018; 563(7731):421-425. PMC: 6485242. DOI: 10.1038/s41586-018-0681-2. View

Petrie S, Stranger R, Pace R . What Mn K spectroscopy reveals concerning the oxidation states of the Mn cluster in photosystem II. Phys Chem Chem Phys. 2017; 19(40):27682-27693. DOI: 10.1039/c7cp04797e. View

Kolling D, Cox N, Ananyev G, Pace R, Dismukes G . What are the oxidation states of manganese required to catalyze photosynthetic water oxidation?. Biophys J. 2012; 103(2):313-22. PMC: 3400770. DOI: 10.1016/j.bpj.2012.05.031. View

10.

Vermass W, Rutherford A, Hansson O . Site-directed mutagenesis in photosystem II of the cyanobacterium Synechocystis sp. PCC 6803: Donor D is a tyrosine residue in the D2 protein. Proc Natl Acad Sci U S A. 1988; 85(22):8477-81. PMC: 282481. DOI: 10.1073/pnas.85.22.8477. View

11.

Ananyev G, Dismukes G . Assembly of the tetra-Mn site of photosynthetic water oxidation by photoactivation: Mn stoichiometry and detection of a new intermediate. Biochemistry. 1996; 35(13):4102-9. DOI: 10.1021/bi952667h. View

12.

Messinger J, Robblee J, Bergmann U, Fernandez C, Glatzel P, Visser H . Absence of Mn-centered oxidation in the S(2) --> S(3) transition: implications for the mechanism of photosynthetic water oxidation. J Am Chem Soc. 2001; 123(32):7804-20. PMC: 3965774. DOI: 10.1021/ja004307+. View

13.

Ibrahim M, Chatterjee R, Hellmich J, Tran R, Bommer M, Yachandra V . Improvements in serial femtosecond crystallography of photosystem II by optimizing crystal uniformity using microseeding procedures. Struct Dyn. 2016; 2(4). PMC: 4697744. DOI: 10.1063/1.4919741. View

14.

Kok B, Forbush B, McGloin M . Cooperation of charges in photosynthetic O2 evolution-I. A linear four step mechanism. Photochem Photobiol. 1970; 11(6):457-75. DOI: 10.1111/j.1751-1097.1970.tb06017.x. View

15.

Cox N, Retegan M, Neese F, Pantazis D, Boussac A, Lubitz W . Photosynthesis. Electronic structure of the oxygen-evolving complex in photosystem II prior to O-O bond formation. Science. 2014; 345(6198):804-8. DOI: 10.1126/science.1254910. View

16.

Beckmann K, Messinger J, Badger M, Wydrzynski T, Hillier W . On-line mass spectrometry: membrane inlet sampling. Photosynth Res. 2009; 102(2-3):511-22. PMC: 2847165. DOI: 10.1007/s11120-009-9474-7. View

17.

Zhang M, Bommer M, Chatterjee R, Hussein R, Yano J, Dau H . Structural insights into the light-driven auto-assembly process of the water-oxidizing MnCaO-cluster in photosystem II. Elife. 2017; 6. PMC: 5542773. DOI: 10.7554/eLife.26933. View

18.

Cheniae G, Martin I . Effects of Hydroxylamine on Photosystem II: II. Photoreversal of the NH(2)OH Destruction of O(2) Evolution. Plant Physiol. 1972; 50(1):87-94. PMC: 367321. DOI: 10.1104/pp.50.1.87. View

19.

Kuntzleman T, Yocum C . Reduction-induced inhibition and Mn(II) release from the photosystem II oxygen-evolving complex by hydroquinone or NH2OH are consistent with a Mn(III)/Mn(III)/Mn(IV)/Mn(IV) oxidation state for the dark-adapted enzyme. Biochemistry. 2005; 44(6):2129-42. DOI: 10.1021/bi048460i. View

20.

Zheng M, Dismukes G . Orbital Configuration of the Valence Electrons, Ligand Field Symmetry, and Manganese Oxidation States of the Photosynthetic Water Oxidizing Complex: Analysis of the S(2) State Multiline EPR Signals. Inorg Chem. 1996; 35(11):3307-3319. DOI: 10.1021/ic9512340. View