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High-efficiency oxygen evolution by photosystem II oxygen-evolving complex containing 3Mn per reaction center

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Abstract

Ca-depleted photosystem II membranes obtained by treatment with acidic buffer do not contain Ca2+ in the Mn4CaO5 cluster but contain all extrinsic proteins protecting this cluster (PSII(-Ca/low pH)). However, unlike native photosystem II, Mn cluster in PSII(-Ca/low pH) samples is available for small-sized reductants. Using this property, we investigated the substitution possibility of Mn cation(s) with Fe cation(s) to obtain a chimeric cluster in PSII(-Ca/low pH) samples containing extrinsic proteins. We found that Fe(II) cation replaces Mn cation at pH 6.5, however, PSII(-Ca/low pH) membranes with the 3Mn1Fe chimeric cluster in the oxygen-evolving complex evolve O2 with high intensity in the presence of exogenous Ca2+. The O2 evolution rate is about 80% of the same rate in PSII(-Ca/low pH) membranes.

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Data availability

The data that support the findings of this study are available from the corresponding author, [BS], upon reasonable request.

Abbreviations

Chl:

Chlorophyll

DCBQ:

2,6-Dichloro-1,4-benzoquinone

HA:

High-affinity Mn-binding site

H2Q:

Hydroquinone

MES:

2-(N-morpholino)-ethanesulfonic acid

OEC:

Oxygen-evolving complex

PSII:

Photosystem II

PSII(-Ca):

Ca-depleted PSII

PSII(-Ca/low pH):

Ca-depleted PSII membranes using low pH treatment

PSII(-Ca/NaCl):

Ca-depleted PSII membranes using NaCl treatment

PSII(-Ca/low pH/3Mn1Fe):

Low pH-treated PSII(-Ca) membranes with chimeric cluster 3Mn1Fe

PSII(-Mn):

Mn-depleted PSII membranes

RC:

Reaction center

TMB:

3,3′,5,5′-Tetramethylbenzidine

References

  1. 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 473:55–60. https://doi.org/10.1038/nature09913

    Article  CAS  PubMed  Google Scholar 

  2. Ananyev GM, Dismukes GC (1996) Assembly of the tetra-Mn site of photosynthetic water oxidation by photoactivation: Mn stoichiometry and detection of a new intermediate. Biochemistry 35:4102–4109. https://doi.org/10.1021/bi952667h

    Article  CAS  PubMed  Google Scholar 

  3. Ono T-A, Mino H (1999) Unique binding site for Mn2+ ion responsible for reducing an oxidized YZ tyrosine in manganese-depleted photosystem II membranes. Biochemistry 38:8778–8785. https://doi.org/10.1021/bi982949s

    Article  CAS  PubMed  Google Scholar 

  4. Mino H, Asada M (2021) Location of two Mn2+ affinity sites in photosystem II detected by pulsed electron–electron double resonance. Photosynth Res. https://doi.org/10.1007/s11120-021-00885-5

    Article  PubMed  Google Scholar 

  5. Hoganson CW, Ghanotakis DF, Babcock GT, Yocum CF (1989) Mn2+ reduces Y+ in manganese-depleted photosystem II preparations. Photosynth Res 22:285–293. https://doi.org/10.1007/BF00048306

    Article  CAS  PubMed  Google Scholar 

  6. Becker K, Cormann KU, Nowaczyk MM (2011) Assembly of the water-oxidizing complex in photosystem II. J Photochem Photobiol B 104:204–211. https://doi.org/10.1016/j.jphotobiol.2011.02.005

    Article  CAS  PubMed  Google Scholar 

  7. Semin BK, Ivanov II, Rubin AB, Parak F (1995) High-specific binding of Fe(II) at the Mn-binding site in Mn-depleted PSII membranes from spinach. FEBS Lett 375:223–226. https://doi.org/10.1016/0014-5793(95)01215-Z

    Article  CAS  PubMed  Google Scholar 

  8. 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

    Article  CAS  PubMed  Google Scholar 

  9. 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

    Article  CAS  PubMed  Google Scholar 

  10. 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

    Article  CAS  PubMed  Google Scholar 

  11. Semin BK, Seibert M (2006) Flash-induced blocking of the high-affinity, Mn-binding site by iron cations: dependence on the dark interval between flashes and binary oscillations of fluorescence yield. J Phys Chem B 110:25532–25542. https://doi.org/10.1021/jp0652796

    Article  CAS  PubMed  Google Scholar 

  12. Semin BK, Lovyagina ER, Timofeev KN, Ivanov II, Rubin AB, Seibert M (2005) Iron-blocking the high-affinity Mn-binding site in photosystem II facilitates identification of the type of hydrogen bond participating in proton-coupled electron transport via YZ •. Biochemistry 44:9746–9757. https://doi.org/10.1021/bi047618w

    Article  CAS  PubMed  Google Scholar 

  13. Widdel F, Schnell S, Heising S, Ehrenreich A, Assmus B, Schink B (1993) Ferrous iron oxidation by anoxygenic phototrophic bacteria. Nature 362:834–836. https://doi.org/10.1038/362834a0

    Article  CAS  Google Scholar 

  14. 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

    Article  CAS  PubMed  Google Scholar 

  15. Semin BK, Davletshina LN, Rubin AB (2015) Correlation between pH dependence of O2 evolution and sensitivity of Mn cations in the oxygen-evolving complex to exogenous reductants. Photosynth Res 125:95–103. https://doi.org/10.1007/s11120-015-0155-4

    Article  CAS  PubMed  Google Scholar 

  16. 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

    Article  CAS  PubMed  Google Scholar 

  17. Ono T, Inoue Y (1988) Discrete extraction of the Ca atom functional for O2 evolution in higher plant photosystem II by a simple low pH treatment. FEBS Lett 227:147–152. https://doi.org/10.1016/0014-5793(88)80886-X

    Article  CAS  Google Scholar 

  18. Vander Meulen KA, Hobson A, Yocum CF (2002) Calcium depletion modifies the structure of the photosystem II O2-evolving complex. Biochemistry 41:958–966. https://doi.org/10.1021/bi0109414

    Article  CAS  PubMed  Google Scholar 

  19. Vander Meulen KA, Hobson A, Yocum CF (2004) Reconstitution of the photosystem II Ca2+ binding site. Biochim Biophys Acta 1655:179–183. https://doi.org/10.1016/j.bbabio.2003.08.012

    Article  CAS  PubMed  Google Scholar 

  20. 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

    Article  CAS  Google Scholar 

  21. 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

    Article  CAS  Google Scholar 

  22. 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

    Article  CAS  Google Scholar 

  23. 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

    Article  CAS  PubMed  Google Scholar 

  24. 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

    Article  CAS  PubMed  Google Scholar 

  25. Serrat FB (1998) 3,3′,5,5′-Tetramethylbenzidme for the colorimetric determination of manganese in water. Microchim Acta 129:77–80. https://doi.org/10.1007/BF01246852

    Article  Google Scholar 

  26. Ghanotakis DF, Babcock GT, Yocum CF (1984) 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

    Article  CAS  Google Scholar 

  27. 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. https://doi.org/10.1016/S0021-9258(18)35683-7

    Article  CAS  PubMed  Google Scholar 

  28. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685. https://doi.org/10.1038/227680a0

    Article  CAS  PubMed  Google Scholar 

  29. Ghanotakis DF, Babcock GT, Yocum CF (1984) 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

    Article  CAS  Google Scholar 

  30. Miyao M, Murata N (1984) Calcium ions can be substituted for the 24-kDa polypeptide in photosynthetic oxygen evolution. FEBS Lett 168:118–120. https://doi.org/10.1016/0014-5793(84)80218-5

    Article  CAS  Google Scholar 

  31. Furia TE (1973) CRC handbook of food additives (Vol. 1), CRC press

  32. Kuntzleman T, Yocum CF (2005) 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 44:2129–2142. https://doi.org/10.1021/bi048460i

    Article  CAS  PubMed  Google Scholar 

  33. Roose JL, Frankel LK, Mummadisetti MP, Bricker TM (2016) The extrinsic proteins of photosystem II: update. Planta 243:889–908. https://doi.org/10.1007/s00425-015-2462-6

    Article  CAS  PubMed  Google Scholar 

  34. Nakatani HY (1984) Photosynthetic oxygen evolution does not require the participation of polypeptides of 16 and 24 kilodaltons. Biochem Biophys Res Commun 120:299–304. https://doi.org/10.1016/0006-291X(84)91448-7

    Article  CAS  PubMed  Google Scholar 

  35. Tomita M, Ifuku K, Sato F, Noguchi T (2009) FTIR evidence that the PsbP extrinsic protein induces protein conformational changes around the oxygen-evolving Mn cluster in photosystem II. Biochemistry 48:6318–6325. https://doi.org/10.1021/bi9006308

    Article  CAS  PubMed  Google Scholar 

  36. Zabret J, Bohn S, Schuller SK, Arnolds O, Möller M, Meier-Credo J et al (2021) Structural insights into photosystem II assembly. Nature plants 7:524–538. https://doi.org/10.1038/s41477-021-00895-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Avramov AP, Hwang HJ, Burnap RL (2020) The role of Ca2+ and protein scaffolding in the formation of nature’s water oxidizing complex. Proc Natl Acad Sci USA 117:28036–28045. https://doi.org/10.1073/pnas.2011315117

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Lubitz W, Cox CM, N, (2019) Water oxidation in photosystem II. Photosynth Res 142:105–125. https://doi.org/10.1007/s11120-019-00648-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Shen JR (2015) The structure of photosystem II and the mechanism of water oxidation in photosynthesis. Annu Rev Plant Biol 66:23–48. https://doi.org/10.1146/annurev-arplant-050312-120129

    Article  CAS  PubMed  Google Scholar 

  40. Vinyard DJ, Ananyev GM, Dismukes GC (2013) Photosystem II: the reaction center of oxygenic photosynthesis. Annu Rev Biochem 82:577–606. https://doi.org/10.1146/annurev-biochem-070511-100425

    Article  CAS  PubMed  Google Scholar 

  41. Gates C, Ananyev G, Roy-Chowdhury S, Cullinane B, Miller M, Fromme P, Dismukes GC (2022) Why did nature choose manganese over cobalt to make oxygen photosynthetically on the earth? J Phys Chem B 126:3257–3268. https://doi.org/10.1021/acs.jpcb.2c00749

    Article  CAS  PubMed  Google Scholar 

  42. Du P, Eisenberg R (2012) Catalysts made of earth-abundant elements (Co, Ni, Fe) for water splitting: Recent progress and future challenges. Energy Environ Sci 5:6012–6021. https://doi.org/10.1039/c2ee03250c

    Article  CAS  Google Scholar 

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Acknowledgements

The research was carried out as part of the Scientific Project of the State Order of the Government of Russian Federation to Lomonosov Moscow State University No. 121032500058-7

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  1. Department of Biophysics, Faculty of Biology, Moscow State University, Moscow, 119234, Russia

    Boris К. Semin & Lira N. Davletshina

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Semin, B.К., Davletshina, L.N. High-efficiency oxygen evolution by photosystem II oxygen-evolving complex containing 3Mn per reaction center. J Biol Inorg Chem 28, 393–401 (2023). https://doi.org/10.1007/s00775-023-01987-2

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