Skip to main content
SpringerLink
Log in

Effective binding of Tb3+ and La3+ cations on the donor side of Mn-depleted photosystem II

  • Original Paper
  • Published:
JBIC Journal of Biological Inorganic Chemistry Aims and scope Submit manuscript

Abstract

The interaction of Tb3+ and La3+ cations with different photosystem II (PSII) membranes (intact PSII, Ca-depleted PSII (PSII[-Ca]) and Mn-depleted PSII (PSII[-Mn]) membranes) was studied. Although both lanthanide cations (Ln3+) interact only with Ca2+-binding site of oxygen-evolving complex (OEC) in PSII and PSII(-Ca) membranes, we found that in PSII(-Mn) membranes both Ln3+ ions tightly bind to another site localized on the oxidizing side of PSII. Binding of Ln3+ cations to this site is not protected by Ca2+ and is accompanied by very effective inhibition of Mn2+ oxidation at the high-affinity (HA) Mn-binding site ([Mn2+  + H2O2] couple was used as a donor of electrons). The values of the constant for inhibition of electron transport Ki are equal to 2.10 ± 0.03 µM for Tb3+ and 8.3 ± 0.4 µM for La3+, whereas OEC inhibition constant in the native PSII membranes is 323 ± 7 µM for Tb3+. The value of Ki for Tb3+ corresponds to Ki for Mn2+ cations in the reaction of diphenylcarbazide oxidation via HA site (1.5 µM) presented in the literature. Our results suggest that Ln3+ cations bind to the HA Mn-binding site in PSII(-Mn) membranes like Mn2+ or Fe2+ cations. Taking into account the fact that Mn2+ and Fe2+ cations bind to the HA site as trivalent cations after light-induced oxidation and the fact that Mn cation bound to the HA site (Mn4) is also in trivalent state, we can suggest that valency may be important for the interaction of Ln3+ with the HA site.

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
Fig. 7
Fig. 8

Similar content being viewed by others

Abbreviations

Chl:

Chlorophyll

DCBQ:

2,6-Dichloro-p-benzoquinone

DCPIP:

2,6-Dichlorophenolindophenol

DPC:

Diphenylcarbazide

HA:

High-affinity Mn-binding site

MES:

2-(N-Morpholino)-ethanesulfonic acid

Ln3 + :

Lanthanide ions

OEC:

Oxygen-evolving complex

PSII:

Photosystem II

PSII(-Ca):

Ca2+-depleted PSII membranes

PSII(-Mn):

Mn-depleted PSII membranes

RC:

Reaction center

Tris:

Tris(hydroxymethyl)aminomethane

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. 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

    Article  CAS  PubMed  Google Scholar 

  3. 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

    Article  CAS  PubMed  Google Scholar 

  4. Young ID, Ibrahim M, Chatterjee R, Gul S, Fuller FD, Koroidov S, Brewster AS, Tran R, Alonso-Mori R, Kroll T, Michels-Clark T, Laksmono H, Sierra RG, Stan CA, Hussein R, Zhang M, Douthit L, Kubin M, de Lichtenberg C, Pham LV, Nilsson H, Cheah MH, Shevela D, Saracini C, Bean MA, Seuffert I, Sokaras D, Weng TC, Pastor E, Weninger C, Fransson T, Lassalle L, Brauer P, Aller P, Docker PT, Andi B, Orville AM, Glownia JM, Nelson S, Sikorski M, Zhu DL, Hunter MS, Lane TJ, Aquila A, Koglin JE, Robinson J, Liang MN, Boutet S, Lyubimov AY, Uervirojnangkoorn M, Moriarty NW, Liebschner D, Afonine PV, Waterman DG, Evans G, Wernet P, Dobbek H, Weis WI, Brunger AT, Zwart PH, Adams PD, Zouni A, Messinger J, Bergmann U, Sauter NK, Kern J, Yachandra VK, Yano J (2016) Structure of photosystem II and substrate binding at room temperature. Nature 540:453–457. https://doi.org/10.1038/nature20161

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. 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

  6. Wei X, Su X, Cao P, Liu X, Chang W, Li M, Zhang X, Liu Z (2016) Structure of spinach photosystem II–LHCII supercomplex at 3.2 Å resolution. Nature 534:69–74. https://doi.org/10.1038/nature18020

    Article  CAS  PubMed  Google Scholar 

  7. Yocum CF (1991) Calcium activation of photosynthetic water oxidation. Biochim Biophys Acta 1059:1–15. https://doi.org/10.1016/S0005-2728(05)80182-3

    Article  CAS  Google Scholar 

  8. Shamsipur M, Pashabadi A (2018) Latest advances in PSII features and mechanism of water oxidation. Coord Chem Rev 374:153–172. https://doi.org/10.1016/j.ccr.2018.07.006

    Article  CAS  Google Scholar 

  9. Bang S, Lee Y-M, Hong S, Cho K-B, Nishida Yu, Seo MS, Sarangi R, Fukuzumi S, Nam W (2014) Redox-inactive metal ions modulate the reactivity and oxygen release of mononuclear non-haem iron(III)–peroxo complexes. Nat Chem 6:934–940. https://doi.org/10.1038/nchem.2055

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. McEvoy JP, Brudvig GW (2006) Water-splitting chemistry of photosystem II. Chem Rev 106(11):4455–4483. https://doi.org/10.1021/cr0204294

    Article  CAS  PubMed  Google Scholar 

  11. Waggoner CM, Yocum CF (1990) Calcium activated oxygen evolution. In: Baltscheffsky M (ed) Current research in photosynthesis. Springer, Dordrecht. https://doi.org/10.1007/978-94-009-0511-5_167

  12. 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 

  13. Ghanotakis DF, Babcock GT, Yocum CF (1985) Structure of the oxygen-evolving complex of Photosystem II: calcium and lanthanum compete for sites on the oxidizing side of Photosystem II which control the binding of water-soluble polypeptides and regulate the activity of the manganese complex. Biochim Biophys Acta 809:173–180. https://doi.org/10.1016/0005-2728(85)90060-X

    Article  CAS  Google Scholar 

  14. Ono T (2000) Effects of lanthanide substitution at Ca2+-site on the properties of the oxygen evolving center of photosystem II. J Inorg Biochem 82:85–91. https://doi.org/10.1016/S0162-0134(00)00144-6

    Article  CAS  PubMed  Google Scholar 

  15. Kretsinger RH, Nelson DJ (1976) Calcium in biological systems. Coord Chem Rev 18:29–124. https://doi.org/10.1016/S0010-8545(00)82054-8

    Article  CAS  Google Scholar 

  16. Lee C-I, Lakshmi KV, Brudvig GW (2007) Probing the functional role of Ca2+ in the oxygen-evolving complex of photosystem II by metal ion inhibition. Biochemistry 46:3211–3223. https://doi.org/10.1021/bi062033i

    Article  CAS  PubMed  Google Scholar 

  17. Bakou A, Ghanotakis DF (1993) Substitution of lanthanides at the calcium site(s) in photosystem II affects electron transport from tyrosine Z to P680+. Biochim Biophys Acta 1141:303–308. https://doi.org/10.1016/0005-2728(93)90057-M

    Article  Google Scholar 

  18. Loktyushkin AV, Lovyagina ER, Semin BK (2019) Interaction of terbium cations with the donor side of photosystem II in higher plants. Moscow Univ Biol Sci Bull 74:81–85. https://doi.org/10.3103/S009639251902007X

    Article  Google Scholar 

  19. 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 

  20. Dunahay TG, Staechelin LA, Seibert M, Ogilvie PD, Berg SP (1984) Structural biochemical and biophysical characterization of four oxygen-evolving photosystem 2 preparations from spinach. Biochim Biophys Acta 764:179–193. https://doi.org/10.1016/0005-2728(84)90027-6

    Article  CAS  Google Scholar 

  21. 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. 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. Boussac A, Zimmermann J-L, Rutherford AW (1990) Factors influencing the formation of modified S2 EPR signal and the S3 EPR signal in Ca2+-depleted photosystem II. FEBS Lett 277:69–74. https://doi.org/10.1016/0014-5793(90)80811-V

    Article  CAS  PubMed  Google Scholar 

  24. Semin BK, Davletshina LN, Ivanov II, Rubin AB, Seibert M (2008) Decoupling of the processes of molecular oxygen synthesis and electron transport in Ca2+-depleted PSII membranes. Photosynth Res 98:235–249. https://doi.org/10.1007/s11120-008-9347-5

    Article  CAS  PubMed  Google Scholar 

  25. Armstrong JM (1964) The molar extinction coefficient of 2,6-dichlorophenol indophenol. Biochim Biophys Acta 86(1):194–197. https://doi.org/10.1016/0304-4165(64)90180-1

    Article  CAS  PubMed  Google Scholar 

  26. 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 

  27. Semin BK, Davletshina LN, Ivanov II, Seibert M, Rubin AB (2012) Rapid degradation of the tetrameric Mn cluster in iluminated, PsbO-depleted photosystem II preparations. Biochemistry (Moscow) 77:152–156. https://doi.org/10.1134/S0006297912020058

    Article  CAS  Google Scholar 

  28. 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 

  29. Lovyagina ER, Semin BK (2016) Mechanism of inhibition and decoupling of oxygen evolution from electron transfer in photosystem II by fluoride, ammonia and acetate. J Photochem Photobiol B 158:145–153. https://doi.org/10.1016/j.jphotobiol.2016.02.031

    Article  CAS  PubMed  Google Scholar 

  30. Lovyagina ER, Belevich NP, Semin BK (2016) Inhibition of photosystem II electron transport chain by ammonia and “decoupling effect”. Modern trends in biological physics and chemistry (BPPC) 1:95−98. https://pureportal.spbu.ru/files/9280949/Proceedings_BPPC_2016_Vol_1.pdf#page=96

  31. Bakou A, Buser C, Dandulakis G, Brudvig G, Ghanotakis DF (1992) Calcium binding site(s) of photosystem II as probed by lanthanides. Biochim Biophys Acta 1099:131–136. https://doi.org/10.1016/0005-2728(92)90209-K

    Article  CAS  Google Scholar 

  32. Riggs-Gelasco PJ, Mei R, Ghanotakis DF, Yocum CF, Penner-Hahn JE (1996) X-ray absorption spectroscopy of calcium-substituted derivatives of the oxygen-evolving complex of photosystem II. J Am Chem Soc 118:2400–2410. https://doi.org/10.1021/ja9504505

    Article  CAS  Google Scholar 

  33. 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 

  34. Ghanotakis DF, Topper JN, Youcum CF (1984) Structural organization of the oxidizing side of photosystem II. Exogenous reductants reduce and destroy the Mn-complex in photosystems II membranes depleted of the 17 and 23 kDa polypeptides. Biochim Biophys Acta 767(3):524−531. https://doi.org/https://doi.org/10.1016/0005-2728(84)90051-3

  35. 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 

  36. Segel IW (1993) Enzyme kinetics behavior and analysis of rapid equilibrium and steady-state enzyme systems. Wiley, New York

    Google Scholar 

  37. 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. https://doi.org/10.1093/oxfordjournals.pcp.a077357

    Article  CAS  Google Scholar 

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

    CAS  Google Scholar 

  39. Semin BK, Davletschina LN, Aleksandrov AYu, Lanchinskaya VYu, Novakova AA, Ivanov II (2004) pH-dependence of iron binding to the donor side of photosystem II. Biochemistry (Moscow) 69:410–419. https://doi.org/10.1023/B:BIRY.0000022066.38297.8a

    Article  Google Scholar 

  40. 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 

  41. Pospíšil P, Dau H (2000) Chlorophyll fluorescence transients of photosystem II membrane particles as a tool for studying photosynthetic oxygen evolution. Photosynth Res 65:41–52. https://doi.org/10.1023/A:1006469809812

    Article  PubMed  Google Scholar 

  42. Strasser BJ (1997) Donor side capacity of photosystem II probed by chlorophyll a fluorescence transients. Photosynth Res 52:147–155. https://doi.org/10.1023/A:1005896029778

    Article  CAS  Google Scholar 

  43. Hsu B-D, Lee J-Y, Pan R-L (1987) The high-affinity binding site for manganese on the oxidizing side of Photosystem II. Biochim Biophys Acta 890:89–96. https://doi.org/10.1016/0005-2728(87)90072-7

    Article  CAS  Google Scholar 

  44. 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

    Article  CAS  PubMed  Google Scholar 

  45. Seibert M, Tamura N, Inoue Y (1989) Lack of photoactivation capacity in Scenedesmus obliquus LF-1 results from loss of half the high-affinity manganese-binding site: relationship to the unprocessed D1 protein. Biochim Biophys Acta 974:185–191. https://doi.org/10.1016/S0005-2728(89)80371-8

    Article  CAS  Google Scholar 

  46. 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. https://doi.org/10.1021/bi951657d

    Article  CAS  PubMed  Google Scholar 

  47. 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 

  48. 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 

  49. 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 

  50. Boggon TJ, Shapiro L (2000) Screening for phasing atoms in protein crystallography. Structure 8:R143–R149. https://doi.org/10.1016/s0969-2126(00)00168-4

    Article  CAS  PubMed  Google Scholar 

  51. Kawakami K, Umena Y, Kamiya N, Shen J-R (2009) Location of chloride and its possible functions in oxygen-evolving photosystem II revealed by X-ray crystallography. PNAS 106:8567–8572. https://doi.org/10.1073/pnas.0812797106

    Article  PubMed  Google Scholar 

  52. Asada M, Mino H (2015) Location of the high-affinity Mn2+ site in photosystem II detected by PELDOR. J Phys Chem B 119:10139–10144. https://doi.org/10.1021/acs.jpcb.5b03994

    Article  CAS  PubMed  Google Scholar 

  53. Shannon RD (1976) Revised effective ionic radii and systematic studies of interatomic distances in halides and chalcogenides. Acta Cryst A32:751–767. https://doi.org/10.1107/S0567739476001551

    Article  CAS  Google Scholar 

  54. Semin BK, Davletshina LN, Rubin AB (2019) Effect of sucrose-bound polynuclear iron oxyhydroxide nanoparticles on the efficiency of electron transport in the photosystem II membranes. Photosynth Res 142:57–67. https://doi.org/10.1007/s11120-019-00647-4

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We are grateful to Dr. S. Vassiliev (University of New Brunswick, Canada) for technical comments and editorial advice.

Author information

Authors and Affiliations

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

    Elena R. Lovyagina, Aleksey V. Loktyushkin & Boris K. Semin

Authors
  1. Elena R. Lovyagina
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Aleksey V. Loktyushkin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Boris K. Semin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Boris K. Semin.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 81 kb)

Supplementary material 2 (TIF 81 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lovyagina, E.R., Loktyushkin, A.V. & Semin, B.K. Effective binding of Tb3+ and La3+ cations on the donor side of Mn-depleted photosystem II. J Biol Inorg Chem 26, 1–11 (2021). https://doi.org/10.1007/s00775-020-01832-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00775-020-01832-w

Keywords

Search

Navigation