Ca Effects on Fe(II) Interactions with Mn-binding Sites in Mn-depleted Oxygen-evolving Complexes of Photosystem II and on Fe Replacement of Mn in Mn-containing, Ca-depleted Complexes

Overview

Journal Photosynth Res

Publisher Springer

Date 2021 Feb 3

PMID 33532973

Citations 2

Authors

B K Semin

L N Davletshina

S N Goryachev

M Seibert

Affiliations

Soon will be listed here.

Abstract

Fe(II) cations bind with high efficiency and specificity at the high-affinity (HA), Mn-binding site (termed the "blocking effect" since Fe blocks further electron donation to the site) of the oxygen-evolving complex (OEC) in Mn-depleted, photosystem II (PSII) membrane fragments (Semin et al. in Biochemistry 41:5854, 2002). Furthermore, Fe(II) cations can substitute for 1 or 2Mn cations (pH dependent) in Ca-depleted PSII membranes (Semin et al. in Journal of Bioenergetics and Biomembranes 48:227, 2016; Semin et al. in Journal of Photochemistry and Photobiology B 178:192, 2018). In the current study, we examined the effect of Ca cations on the interaction of Fe(II) ions with Mn-depleted [PSII(-Mn)] and Ca-depleted [PSII(-Ca)] photosystem II membranes. We found that Ca cations (about 50 mM) inhibit the light-dependent oxidation of Fe(II) (5 µM) by about 25% in PSII(-Mn) membranes, whereas inhibition of the blocking process is greater at about 40%. Blocking of the HA site by Fe cations also decreases the rate of charge recombination between Q and Y from t = 30 ms to 46 ms. However, Ca does not affect the rate during the blocking process. An Fe(II) cation (20 µM) replaces 1Mn cation in the MnCaO catalytic cluster of PSII(-Ca) membranes at pH 5.7 but 2 Mn cations at pH 6.5. In the presence of Ca (10 mM) during the substitution process, Fe(II) is not able to extract Mn at pH 5.7 and extracts only 1Mn at pH 6.5 (instead of two without Ca). Measurements of fluorescence induction kinetics support these observations. Inhibition of Mn substitution with Fe(II) cations in the OEC only occurs with Ca and Sr cations, which are also able to restore oxygen evolution in PSII(-Ca) samples. Nonactive cations like La, Ni, Cd, and Mg have no influence on the replacement of Mn with Fe. These results show that the location and/or ligand composition of one Mn cation in the MnCaO cluster is strongly affected by calcium depletion or rebinding and that bound calcium affects the redox potential of the extractable Mn4 cation in the OEC, making it resistant to reduction.

Citing Articles

Light increases resistance of thylakoid membranes to thermal inactivation.

Lovyagina E, Luneva O, Loktyushkin A, Semin B J Plant Res. 2024; 137(6):1189-1200.

PMID: 39356383 DOI: 10.1007/s10265-024-01584-7.

Current analysis of cations substitution in the oxygen-evolving complex of photosystem II.

Semin B, Loktyushkin A, Lovyagina E Biophys Rev. 2024; 16(2):237-247.

PMID: 38737202 PMC: 11078907. DOI: 10.1007/s12551-024-01186-6.

References

Ananyev G, Dismukes G . High-resolution kinetic studies of the reassembly of the tetra-manganese cluster of photosynthetic water oxidation: proton equilibrium, cations, and electrostatics. Biochemistry. 1996; 35(46):14608-17. DOI: 10.1021/bi960894t. View

Armstrong J . THE MOLAR EXTINCTION COEFFICIENT OF 2,6-DICHLOROPHENOL INDOPHENOL. Biochim Biophys Acta. 1964; 86:194-7. DOI: 10.1016/0304-4165(64)90180-1. View

Ghirardi M, Lutton T, Seibert M . Interactions between diphenylcarbazide, zinc, cobalt, and manganese on the oxidizing side of photosystem II. Biochemistry. 1996; 35(6):1820-8. DOI: 10.1021/bi951657d. View

Kawakami K, Umena Y, Kamiya N, Shen J . Structure of the catalytic, inorganic core of oxygen-evolving photosystem II at 1.9 Å resolution. J Photochem Photobiol B. 2011; 104(1-2):9-18. DOI: 10.1016/j.jphotobiol.2011.03.017. 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

Kim C, Debus R . Evidence from FTIR Difference Spectroscopy That a Substrate HO Molecule for O Formation in Photosystem II Is Provided by the Ca Ion of the Catalytic MnCaO Cluster. Biochemistry. 2017; 56(20):2558-2570. DOI: 10.1021/acs.biochem.6b01278. View

LAZAR . Chlorophyll a fluorescence induction1 . Biochim Biophys Acta. 1999; 1412(1):1-28. DOI: 10.1016/s0005-2728(99)00047-x. 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

Najafpour M, Renger G, Holynska M, Moghaddam A, Aro E, Carpentier R . Manganese Compounds as Water-Oxidizing Catalysts: From the Natural Water-Oxidizing Complex to Nanosized Manganese Oxide Structures. Chem Rev. 2016; 116(5):2886-936. DOI: 10.1021/acs.chemrev.5b00340. View

10.

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

11.

Preston C, Seibert M . The carboxyl modifier 1-ethyl-3-[3-(dimethylamino)propyl]carbodiimide (EDC) inhibits half of the high-affinity Mn-binding site in photosystem II membrane fragments. Biochemistry. 1991; 30(40):9615-24. DOI: 10.1021/bi00104a008. View

12.

Semin B, Ghirardi M, Seibert M . Blocking of electron donation by Mn(II) to Y(Z*) following incubation of Mn-depleted photosystem II membranes with Fe(II) in the light. Biochemistry. 2002; 41(18):5854-64. DOI: 10.1021/bi0200054. View

13.

Semin B, Seibert M . Iron bound to the high-affinity Mn-binding site of the oxygen-evolving complex shifts the pK of a component controlling electron transport via Y(Z). Biochemistry. 2004; 43(21):6772-82. DOI: 10.1021/bi036047p. View

14.

Semin B, Seibert M . A carboxylic residue at the high-affinity, Mn-binding site participates in the binding of iron cations that block the site. Biochim Biophys Acta. 2006; 1757(3):189-97. DOI: 10.1016/j.bbabio.2006.02.001. View

15.

Semin B, Davletshina L, Ivanov I, Rubin A, Seibert M . Decoupling of the processes of molecular oxygen synthesis and electron transport in Ca2+-depleted PSII membranes. Photosynth Res. 2008; 98(1-3):235-49. DOI: 10.1007/s11120-008-9347-5. View

16.

Semin B, Seibert M . A simple colorimetric determination of the manganese content in photosynthetic membranes. Photosynth Res. 2009; 100(1):45-8. DOI: 10.1007/s11120-009-9421-7. View

17.

Semin B, Davletshina L, Timofeev K, Ivanov I, Rubin A, Seibert M . Production of reactive oxygen species in decoupled, Ca(2+)-depleted PSII and their use in assigning a function to chloride on both sides of PSII. Photosynth Res. 2013; 117(1-3):385-99. DOI: 10.1007/s11120-013-9870-x. View

18.

Semin B, Seibert M . Substituting Fe for two of the four Mn ions in photosystem II-effects on water-oxidation. J Bioenerg Biomembr. 2016; 48(3):227-40. DOI: 10.1007/s10863-016-9651-2. View

19.

Suga M, Akita F, Hirata K, Ueno G, Murakami H, Nakajima Y . Native structure of photosystem II at 1.95 Å resolution viewed by femtosecond X-ray pulses. Nature. 2014; 517(7532):99-103. DOI: 10.1038/nature13991. View

20.

Suga M, Akita F, Sugahara M, Kubo M, Nakajima Y, Nakane T . Light-induced structural changes and the site of O=O bond formation in PSII caught by XFEL. Nature. 2017; 543(7643):131-135. DOI: 10.1038/nature21400. View