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 Ca2+ cations on the interaction of Fe(II) ions with Mn-depleted [PSII(-Mn)] and Ca-depleted [PSII(-Ca)] photosystem II membranes. We found that Ca2+ 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 QA− and YZ•+ from t1/2 = 30 ms to 46 ms. However, Ca2+ does not affect the rate during the blocking process. An Fe(II) cation (20 µM) replaces 1Mn cation in the Mn4CaO5 catalytic cluster of PSII(-Ca) membranes at pH 5.7 but 2 Mn cations at pH 6.5. In the presence of Ca2+ (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 Ca2+). Measurements of fluorescence induction kinetics support these observations. Inhibition of Mn substitution with Fe(II) cations in the OEC only occurs with Ca2+ and Sr2+ cations, which are also able to restore oxygen evolution in PSII(-Ca) samples. Nonactive cations like La3+, Ni2+, Cd2+, and Mg2+ 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 Mn4CaO5 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.
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Abbreviations
- Chl:
-
Chlorophyll
- DCMU:
-
3-(3,4-Dichlorophenyl)-1,1-dimethylurea
- DCPIP:
-
2,6-Dichlorophenolindophenol
- HA:
-
High-affinity Mn-binding site [also known as the site where the “dangler” cation (Mn #4 of the Suga et al. 2015 structure) binds]
- F 0 :
-
Fluorescence emitted by a sample at low light levels prior to flash excitation
- (F − F 0)/F 0 :
-
Fluorescence yield
- F max :
-
Maximum fluorescence yield following actinic flash excitation
- F fin :
-
Final fluorescence yield detected after decay of the flash-induced fluorescence
- MES:
-
2-(N-Morpholino)-ethanesulfonic acid
- OEC:
-
Oxygen-evolving complex
- PSII:
-
Photosystem II
- PSII(-Ca):
-
Ca2+-depleted PSII membranes with 4 Mn cations in the OEC
- PSII(-Mn):
-
Mn-depleted PSII membranes
- PSII(-Mn,+Fe):
-
PSII(-Mn) membranes blocked by an iron cation at the high-affinity Mn-binding site
- RC:
-
Reaction center
- TMB:
-
3,3′,5,5′-Tetramethylbenzidine
- Tris:
-
Tris(hydroxymethyl)aminomethane
References
Ananyev GM, Dismukes GC (1996) High-resolution kinetic studies of the reassembly of the tetra-manganese cluster of photosynthetic water oxidation: proton equilibrium, cations, and electrostatics. Biochemistry 35:14608–14617. https://doi.org/10.1021/bi960894t
Armstrong JM (1964) The molar extinction coefficient of 2,6-dichlorophenolindophenol. Biochim Biophys Acta 86:194–197. https://doi.org/10.1016/0304-4165(64)90180-1
Dean JA (ed) (1985) Lange’s handbook of chemistry. McGraw-Hill Book Co, New York
Ghanotakis DF, Babcock GT (1983) Hydroxylamine as an inhibitor between Z and P680 in photosystem II. FEBS Lett 153:231–234. https://doi.org/10.1016/0014-5793(83)80154-9
Ghanotakis DF, Babcock GT, Yocum CF (1984a) Calcium reconstitutes high rates of oxygen evolution in polypeptide depleted photosystem II preparations. FEBS Lett 167:127–130. https://doi.org/10.1016/0014-5793(84)80846-7
Ghanotakis DF, Topper JN, Yocum CF (1984b) Exogenous reductants reduce and destroy the Mn-complex in photosystem II membranes depleted of the 17 and 23 kDa polypeptides. Biochim Biophys Acta 767:524–531. https://doi.org/10.1016/0005-2728(84)90051-3
Ghanotakis DF, Babcock GT, Yocum CF (1984c) Structural and catalytic properties of the oxygen-evolving complex. Correlation of polypeptide and manganese release with the behavior of Z+ in chloroplasts and a highly resolved preparation of the PSII complex. Biochim Biophys Acta 765:388–398. https://doi.org/10.1016/0005-2728(84)90180-4
Ghirardi ML, Lutton TM, Seibert M (1996) Interactions between diphenylcarbazide, zinc, cobalt, and manganese on the oxidizing side of photosystem II. Biochemistry 35:1820–1828. https://doi.org/10.1021/bi951657d
Gisriel CJ, Zhou K, Huang H-L, Debus RJ, Xiong Y, Brudvig GW (2020) Cryo-EM structure of monomeric photosystem II from Synechocystis sp. PCC 6803 lacking the water-oxidation complex. Joule 4(10):2131–2148. https://doi.org/10.1016/j.joule.2020.07.016
Kawakami K, Umena Y, Kamiya N, Shen J-R (2011) Structure of the catalytic, inorganic core of oxygen-evolving photosystem II at 1.9 Å resolution. J Photochem Photobiol B 104:9–18. https://doi.org/10.1016/j.jphotobiol.2011.03.017
Kern J, Chatterjee R, Young ID, Fuller FD, Lassalle L, Ibrahim M, Gul S, Fransson T, Brewster AS, Alonso-Mori R, Hussein R, Zhang M, Douthit L, de Lichtenberg C, Cheah MH, Shevela D, Wersig J, Seuffert I, Sokaras D, Pastor E, Weninger C, Kroll T, Sierra RG, Aller P, Butryn A, Orville AM, Liang M, Batyuk A, Koglin JE, Carbajo S, Boutet S, Moriarty NW, Holton JM, Dobbek H, Adams PD, Bergmann U, Sauter NK, Zouni A, Messinger J, Yano J, Yachandra VK (2018) Structures of the intermediates of Kok’s photosynthetic water oxidation clock. Nature 563:421–425. https://doi.org/10.1038/s41586-018-0681-2
Kim CJ, Debus RJ (2017) Evidence from FTIR difference spectroscopy that a substrate H2O molecule for O2 formation in photosystem II is provided by the Ca ion of the catalytic Mn4CaO5 cluster. Biochemistry 56:2558–2570. https://doi.org/10.1021/acs.biochem.6b01278
Lazar D (1999) Chlorophyll a fluorescence induction. Biochim Biophys Acta 1412:1–28. https://doi.org/10.1016/S0005-2728(99)00047-X
Miyao-Tokutomi M, Inoue Y (1992) Improvement by benzoquinones of the quantum yield of photoactivation of photosynthetic oxygen evolution: direct evidence for the two-quantum mechanism. Biochemistry 31:526–532. https://doi.org/10.1021/bi00117a032
Najafpour MM, Renger G, Hołyńska M, Moghaddam AN, Aro EM, Carpentier R, Nishihara H, Eaton-Rye JJ, Shen J-R, Allakhverdiev SI (2016) Manganese compounds as water-oxidizing catalysts: from the natural water-oxidizing complex to nanosized manganese oxide structures. Chem Rev 116:2886–2936. https://doi.org/10.1021/acs.chemrev.5b00340
Nixon PJ, Diner BA (1992) Aspartate 170 of the photosystem II reaction center polypeptide D1 is involved in the assembly of the oxygen-evolving manganese cluster. Biochemistry 31:942–948. https://doi.org/10.1021/bi00118a041
Ono T, Inoue Y (1990) Abnormal redox reactions in photosynthetic O2-evolving centers in NaCl/EDTA-washed PS II A dark-stable EPR multiline signal and an unknown positive charge accumulator. Biochim Biophys Acta 1020:269–277. https://doi.org/10.1016/0005-2728(90)90157-Y
Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous-equations for assaying chlorophyll-A and chlorophyll-B extracted with 4 different solvents: verification of the concentration of chlorophyll standards by atomic-absorption spectroscopy. Biochim Biophys Acta 975:384–394. https://doi.org/10.1016/S0005-2728(89)80347-0
Preston C, Seibert M (1991) The carboxyl modifier 1-ethyl-3-[3-(dimethylamino)propyl] carbodiimide (EDC) inhibits half of the high-affinity manganese-binding site in photosystem II membrane fragments. Biochemistry 30:9615–9624. https://doi.org/10.1021/bi00104a008
Semin BK, Ghirardi ML, Seibert M (2002) Blocking of electron donation by Mn(II) to YZ• following incubation of Mn-depleted photosystem II membranes with Fe(II) in the light. Biochemistry 41:5854–5864. https://doi.org/10.1021/bi0200054
Semin BK, Seibert M (2004) 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 43:6772–6782. https://doi.org/10.1021/bi036047p
Semin BK, Seibert M (2006) A carboxylic residue at the high-affinity, Mn-binding site participates in the binding of iron cations that block the site. Biochim Biophys Acta 1757:189–197. https://doi.org/10.1016/j.bbabio.2006.02.001
Semin BK, Davletshina LN, Ivanov II, Rubin AB, Seibert M (2008) Uncoupling of processes of molecular synthesis and electron transport in the Ca2+-depleted PSII membranes. Photosynth Res 98:235–249. https://doi.org/10.1007/s11120-008-9347-5
Semin BK, Seibert M (2009) A simple colorimetric determination of the manganese content in photosynthetic membranes. Photosynth Res 100:45–48. https://doi.org/10.1007/s11120-009-9421-7
Semin BK, Davletshina LN, Timofeev KN, Ivanov II, Rubin AB, Seibert M (2013) Production of reactive oxygen species in decoupled, Ca2+-depleted PSII and their use in assigning a function to chloride on both sides of PSII. Photosynth Res 117:385–399. https://doi.org/10.1007/s11120-013-9870-x
Semin BK, Seibert M (2016) Substituting Fe for two of the four Mn ions in photosystem II: effects on water-oxidation. J Bioenerg Biomembr 48:227–240. https://doi.org/10.1007/s10863-016-9651-2
Semin BK, Davletshina LN, Seibert M, Rubin AB (2018) Creation of a 3Mn/1Fe cluster in the oxygen-evolving complex of photosystem II and investigation of its functional activity. J Photochem Photobiol B 178:192–200. https://doi.org/10.1016/j.jphotobiol.2017.11.016
Serrat FB (1998) 3,3′,5,5′-Tetramethylbenzidine for the colorimetric determination of manganese in water. Mikrochim Acta 129:77–80. https://doi.org/10.1007/BF01246852
Suga M, Akita F, Hirata K, Ueno G, Murakami H, Nakajima Y, Shimizu T, Yamashita K, Yamamoto M, Ago H, Shen J-R (2015) Native structure of photosystem II at 1.95 Å resolution viewed by femtosecond X-ray pulses. Nature 517:99–103. https://doi.org/10.1038/nature13991
Suga M, Akita F, Sugahara M, Kubo M, Nakajima Y, Nakane T, Yamashita K, Umena Y, Nakabayashi M, Yamane T, Nakano T, Suzuki M, Masuda T, Inoue S, Kimura T, Nomura T, Yonekura S, Yu L-J, Sakamoto T, Motomura T, Chen J-H, Kato Y, Noguchi T, Tono K, Joti Y, Kameshima T, Hatsui T, Nango E, Tanaka R, Naitow H, Matsuura Y, Yamashita A, Yamamoto M, Nureki O, Yabashi M, Ishikawa T, Iwata S, Shen J-R (2017) Light-induced structural changes and the site of O=O bond formation in PSII caught by XFEL. Nature 543:131–135. https://doi.org/10.1038/nature21400
Tamura N, Cheniae GM (1987) Photoactivation of the water-oxidizing complex in photosystem II membranes depleted of Mn and extrinsic proteins. I. Biochemical and kinetic characterization. Biochim Biophys Acta 890:179–194. https://doi.org/10.1016/0005-2728(87)90019-3
Tamura N, Inoue Y, Cheniae GM (1989) Photoactivation of the water-oxidizing complex in photosystem II membranes depleted of Mn, Ca and extrinsic proteins: II. Studies on the functions of Ca2+. Biochim Biophys Acta 976:173–181. https://doi.org/10.1016/S0005-2728(89)80227-0
Tokano T, Kato Y, Sugiyama S, Uchihashi T, Noguchi T (2020) Structural dynamics of a protein domain relevant to the water-oxidizing complex in photosystem II as visualized by high-speed atomic force microscopy. J Phys Chem B 124(28):5847–5857. https://doi.org/10.1021/acs.jpcb.0c03892
Tsui EY, Agapie T (2013) Reduction potentials of heterometallic manganese–oxido cubane complexes modulated by redox-inactive metals. Proc Natl Acad Sci USA 110:10084–10088. https://doi.org/10.1073/pnas.1302677110
Umena Y, Kawakami K, Shen J-R, Kamiya N (2011) Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å. Nature 473:55–65. https://doi.org/10.1038/nature09913
Vrettos JS, Limburg J, Brudvig GW (2001a) Mechanism of photosynthetic water oxidation: combining biophysical studies of photosystem II with inorganic model chemistry. Biochim Biophys Acta 1503:229–245. https://doi.org/10.1016/S0005-2728(00)00214-0
Vrettos JS, Stone DA, Brudvig GW (2001b) Quantifying the ion selectivity of the Ca2+ site in photosystem II. Evidence for direct involvement of Ca2+ in O2 formation. Biochemistry 40:7937–7945. https://doi.org/10.1021/bi010679z
Xu Q, Bricker TM (1992) Structural organization of proteins on the oxidizing side of photosystem I. Two molecules of the 33-kDa manganese-stabilizing proteins per reaction center. J Biol Chem 267:25816–25821
Zabret J, Bohn S, Schuller SK, Arnolds O, Möller M, Meier-Credo J, Liauw P, Chan A, Tajkhorshid E, Langer JD, Stoll R, Krieger-Liszkay A, Engel BD, Rudack T, Schuller JM, Nowaczyk MM (2020) How to build a water-splitting machine: structural insights into photosystem II assembly. bioRxiv. https://doi.org/10.1101/2020.09.14.294884
Zhang M, Bommer M, Chatterjee R, Hussein R, Yano J, Dau H, Kern J, Dobbek H, Zouni A (2017) Structural insights into the light-driven auto-assembly process of the water-oxidizing Mn4CaO5-cluster in photosystem II. eLife 6:e26933. https://doi.org/10.7554/eLife.26933
Acknowledgements
The work (MS) at the National Renewable Energy Laboratory (NREL) was carried out under US Department of Energy contract number DE-AC36-08-GO28308. MS also acknowledges the support of the NREL Emeritus Program.
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Semin, B.К., Davletshina, L.N., Goryachev, S.N. et al. Ca2+ 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. Photosynth Res 147, 229–237 (2021). https://doi.org/10.1007/s11120-020-00813-z
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DOI: https://doi.org/10.1007/s11120-020-00813-z