Skip to main content
SpringerLink
Log in

Substituting Fe for two of the four Mn ions in photosystem II—effects on water-oxidation

  • Published:
Journal of Bioenergetics and Biomembranes Aims and scope Submit manuscript

Abstract

We have investigated the interaction of Fe(II) cations with Ca-depleted PSII membranes (PSII[-Ca,4Mn]) in the dark and found that Fe(II) incubation removes 2 of 4 Mn ions from the tetranuclear Mn cluster of the photosynthetic O2-evolving complex (OEC). The reduction of Mn ions in PSII(-Ca,4Mn) by Fe(II) and the concomitant release of two Mn(II) cations is accompanied by the binding of newly generated Fe(III) in at least one vacated Mn site. Flash-induced chlorophyll (Chl) fluorescence yield measurements of this new 2Mn/nFe cluster (PSII[-Ca,2Mn,nFe]) show that charge recombination in the presence of 3-(3,4-dichlorophenyl)-1,1-dimethylurea (DCMU) occurs between Qa - and the remaining Mn/Fe cluster (but not YZ ●) in the OEC, and extraction of 2 Mn occurs uniformly in all PSII complexes. No O2 evolution is observed, but the heteronuclear metal cluster in PSII(-Ca,2Mn,nFe) samples is still able to supply electrons for reduction of the exogenous electron acceptor, 2,6-dichlorophrenolindophenol, by photooxidizing water and producing H2O2 in the absence of an exogenous donor as seen previously with PSII(-Ca,4Mn). Selective extraction of Mn or Fe cations from the 2Mn/nFe heteronuclear cluster demonstrates that the high-affinity Mn-binding site is occupied by one of the iron cations. It is notable that partial water-oxidation function still occurs when only two Mn cations are present in the PSII OEC.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Ananyev GM, Wydrzynski T, Renger G, Klimov V (1992) Transient peroxide formation by the manganese-containing, redox-active donor side of photosystem II upon inhibition of O2 evolution with lauroylchloline chloride. Biochim Biophys Acta 1100:303–311

    Article  Google Scholar 

  • Armstrong JM (1964) The molar extinction coefficient of 2,6-dichlorophenolindophenol. Biochim Biophys Acta 86:194–197

    Article  CAS  Google Scholar 

  • Armstrong FA (2008) Why did Nature choose manganese to make oxygen? Phil Trans R Soc B 363:1263–1270

    Article  CAS  Google Scholar 

  • Asada K, Kiso K, Yoshikawa K (1974) Univalent reduction of molecular oxygen by spinach chloroplasts on illumination. J Biol Chem 249:2175–2181

    CAS  Google Scholar 

  • Atta M, Nordlund P, Åberg A, Eklund H, Fontecave M (1992) Substitution of manganese for iron in ribonucleotide reductase from Escherichia coli. spectroscopic and crystallographic characterization. J Biol Chem 267:20682–20688

    CAS  Google Scholar 

  • Blair D, Diehl H (1961) Bathophenanthrolinedisulphonic acid and bathocuproinedisulphonic acid, water soluble reagents for iron and copper. Talanta 7:163–174

    Article  CAS  Google Scholar 

  • Booth PJ, Rutherford AW, Boussac A (1996) Location of the calcium binding site in photosystem II: A Mn2+ substitution study. Biochim Biophys Acta 1277:127–134

    Article  Google Scholar 

  • Boussac A, Picaud M, Etienne A-L (1986) Effect of potassium iridic chloride on the electron donation by Mn2+ to photosystem II particles. Photochem Photobiophys 10:201–211

    CAS  Google Scholar 

  • Boussac A, Zimmermann J-L, Rutherford AW (1989) EPR signals from modified charge accumulation states of the oxygen evolving enzyme in Ca2 + -deficient photosystem II. Biochemistry 28:8984–8989

    Article  CAS  Google Scholar 

  • Boussac A, Zimmermann J-L, Rutherford AW (1990) Factors influencing the formation of modified S2 EPR signal and the S3 EPR signal in Ca(2+)-depleted photosystem II. FEBS Lett 277:69–74

    Article  CAS  Google Scholar 

  • Cardona T, Murray JW, Rutherford AW (2015) Origin and evolution of water oxidation before the last common ancestor of the cyanobacteria. Mol Biol Evol 32:1310–1328

    Article  Google Scholar 

  • Cox N, Pantazis DA, Nesee F, Lubitz W (2013) Biological water oxidation. Accounts Chem Res 46:1588–1596

    Article  CAS  Google Scholar 

  • Debus RJ, Aznar K, Campbell KA, Gregor W, Diner BA, Britt RD (2003) Does aspartate 170 of the D1 polypeptide ligate the manganese cluster in photosystem II? an EPR and ESEEM study. Biochemistry 42:10600–10608

    Article  CAS  Google Scholar 

  • Debus RJ, Strickler MA, Walker LM, Hillier W (2005) No evidence from FTIR difference spectroscopy that aspartate-170 of the D1 polypeptide ligates a manganese ion that undergoes oxidation during the S0 to S1, S1 to S2, or S2 to S3 transitions in photosystem II. Biochemistry 44:1367–1374

    Article  CAS  Google Scholar 

  • Diner BA, Nixon PJ (1992) The rate of reduction of oxidized redox-active tyrosine, Z+, by exogenous Mn2+ is slowed in a site-directed mutant, at aspartate 170 of polypeptide D1 of photosystem II, inactive for photosynthetic oxygen evolution. Biochim Biophys Acta 1101:123–138

    Google Scholar 

  • Fillol JL, Codola Z, Garcia-Bosch I, Goґmez L, Pla JJ, Costas M (2011) Efficient water oxidation catalysts based on readily available iron coordination complexes. Nat Chem 3:807–813

    Article  CAS  Google Scholar 

  • Ghanotakis DF, Babcock GT (1983) Hydroxylamine as an inhibitor between Z and P680 in photosystem II. FEBS Lett 153:231–234

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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 Aсta 767:524–531

    Article  CAS  Google Scholar 

  • Ghirardi ML, Lutton TW, Seibert M (1996) Interactions between diphenylcarbazide, zinc, cobalt, and manganese on the oxidizing side of photosystem II. Biochemistry 35:1820–1828

    Article  CAS  Google Scholar 

  • Herbert DE, Lionetti D, Rittle J, Agapie T (2013) Heterometallic Triiron-Oxo/Hydroxo clusters: effect of redox-inactive metals. J Am Chem Soc 135:19075–19078

    Article  CAS  Google Scholar 

  • Hillier W, Wydrzynski T (1993) Increases in peroxide formation by the photosystem II oxygen evolving reactions upon removal of the extrinsic 16, 22 and 33 kDa proteins are reversed by CaCl2 addition. Photosynth Res 38:417–423

    Article  CAS  Google Scholar 

  • Hoganson CW, Ghanotakis DF, Babcock GT, Yocum CF (1989) Mn2+ reduces YZ + in manganese-depleted photosystem II preparations. Photosynth Res 22:285–293

    Article  CAS  Google Scholar 

  • Högbom M (2010) The manganese/iron-carboxylate proteins: what is what, where are they, and what can the sequences tell us? J Biol Inorg Chem 15:339–349

    Article  Google Scholar 

  • Hohmann-Marriott MF, Blankenship RE (2011) Evolution of photosynthesis. Ann Rev Plant Biol 62:515–548

    Article  CAS  Google Scholar 

  • Inoue H, Wada T (1987) Requirement of manganese for electron donation of hydrogen peroxide in photosystem II reaction center complex. Plant Cell Physiol 28:767–773

    CAS  Google Scholar 

  • Jiang W, Yun D, Saleh L, Barr EW, Xing G, Hoffart LM, Maslak M-A, Krebs C, Bollinger JM Jr (2007) A manganese(IV)/iron(III) cofactor in Chlamydia trachomatis ribonucleotide reductase. Science 316:1188–1191

    Article  CAS  Google Scholar 

  • Kálmán L, LoBrutto R, Williams JC, Allen JP (2006) Iron as a bound secondary electron donor in modified bacterial reaction center. Biochemistry 45:13869–13874

    Article  Google Scholar 

  • Khorobrych SA, Ivanov BN (2002) Oxygen reduction in a plastoquinone pool of isolated pea thylakoids. Photosynth Res 71:209–219

    Article  Google Scholar 

  • Kolbeck RC, She ZW, Callahan LA, Nosek TM (1997) Increased superoxide production during fatigue in the perfused rat diaphragm. Am J Respir Crit Care Med 156:140–145

    Article  CAS  Google Scholar 

  • Kruck J, Jemiola-Rzemi’nska M, Strzalka K (2003) Cytochrome c is reduced mainly by plastoquinol and not by superoxide in thylakoid membranes at low and medium light intensities: its specific interaction with thylakoid membrane lipids. Biochem J 375:215–220

    Article  Google Scholar 

  • Kuntzleman T, Yocum C (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

    Article  CAS  Google Scholar 

  • Mano J, Kawamoto K, Dismukes GC, Asada K (1993) Inhibition of the catalase reaction of photosystem II by anions. Photosynth Res 38:433–440

    Article  CAS  Google Scholar 

  • Nagata T, Zharmukhamedov SK, Khorobrykh AA, Klimov VV, Allakhverdiev SI (2008) Reconstitution of the water-oxidizing complex in manganese-depleted photosystem II preparations using synthetic Mn-complexes: a fluorine-19 NMR study of the reconstitution process. Photosynth Res 98:277–284

    Article  CAS  Google Scholar 

  • Najafpour MM, Moghaddam AN, Allakhverdiev SI, Govindjee (2012) Biological water oxidation: lessons from nature. Biochim Biophys Acta 1817:1110–1121

    Article  CAS  Google Scholar 

  • Ngo TT, Lenhoff HM (1980) A sensitive and versatile chromogenic assay for peroxidase and peroxidase-coupled reactions. Anal Biochem 105:389–397

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Ono T, 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

    Article  CAS  Google Scholar 

  • Pace RJ, Stranger R, Petrie S (2012) Why nature chose Mn for the water oxidase in photosystem II. Dalton Trans 41:7179–7189

    Article  CAS  Google Scholar 

  • Peloquin JM, Campbell KA, Randall DW, Evanchik MA, Pecoraro VL, Armstrong WH, Britt RD (2000) 55Mn ENDOR of the S2-state multiline EPR signal of photosystem II: implications on the structure of the tetranuclear Mn cluster. J Am Chem Soc 122:10926–10942

    Article  CAS  Google Scholar 

  • Porra RJ, Tompson 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Semin BK, Parak F (1997) Coordination sphere and structure of the Mn cluster of the oxygen-evolving complex in photosynthetic organisms. FEBS Lett 400:259–262

    Article  CAS  Google Scholar 

  • Semin BK, Seibert M (2006a) 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

    Article  CAS  Google Scholar 

  • Semin BK, Seibert M (2006b) 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

    Article  CAS  Google Scholar 

  • Semin BK, Seibert M (2009) A simple colorimetric determination of the manganese content in photosynthetic membranes. Photosynth Res 100:45–48

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Semin BK, Davletshina LN, Ivanov II, Seibert M, Rubin AB (2012) Rapid degradation of the tetrameric Mn cluster in illuminated, PsbO-depleted PSII preparations. Biochem Mosc 77:152–156

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Serrat FB (1998) Colorimetric method for determination of chlorine with 3,3′,5,5′-tetramethyl benzidine. Mikrochim Acta 129:77–80

    Article  Google Scholar 

  • Sheptovitsky YG, Brudvig GW (1996) Isolation and characterization of spinach photosystem II membranes-associated catalase and polyphenoloxydase. Biochemistry 35:16255–16263

    Article  CAS  Google Scholar 

  • Singh A, Spiccia L (2013) Water oxidation catalysts based on abundant 1st row transition metals. Coordinat Chem Rev 257:2607–2622

    Article  CAS  Google Scholar 

  • 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 1.95A° resolution viewed by femtosecond X-ray pulses. Nature 517:99–103

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Vass I, Styring S (1991) pH-Dependent charge equilibria between tyrosine-D and the S states in photosystem II. estimation of relative midpoint redox potentials. Biochemistry 30:830–839

    Article  CAS  Google Scholar 

  • Widdel F, Schnell S, Heising S, Enrenreich A (1993) Ferrous iron oxidation by anoxygenic phototrophic bacteria. Nature 362:834–836

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors acknowledge the contribution of Drs. Paul King and Michael Himmel for their critical reading of an earlier version of the manuscript and valuable suggestions for its improvement. The work at the National Renewable Energy Laboratory (NREL) was carried out under US Department of Energy contract number DE-AC36-08-GO28308. This study was supported by the US Department of Energy, Office of Science, Office of Basic Energy Sciences (MS). MS also acknowledges the NREL Emeritus Program.

Author information

Authors and Affiliations

  1. BioEnergy Sciences & Technology Directorate, National Renewable Energy Laboratory, Golden, CO, 80401, USA

    Boris K. Semin & Michael Seibert

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

    Boris K. Semin

Authors
  1. Boris K. Semin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Michael Seibert
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Boris K. Semin.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOC 383 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Semin, B.K., Seibert, M. Substituting Fe for two of the four Mn ions in photosystem II—effects on water-oxidation. J Bioenerg Biomembr 48, 227–240 (2016). https://doi.org/10.1007/s10863-016-9651-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10863-016-9651-2

Keywords

Search

Navigation