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Photosynthesis Research

, Volume 117, Issue 1–3, pp 375–383 | Cite as

Crystal structure of the Psb28 accessory factor of Thermosynechococcus elongatus photosystem II at 2.3 Å

  • Wojciech Bialek
  • Songjia Wen
  • Franck Michoux
  • Martina Beckova
  • Josef Komenda
  • James W. Murray
  • Peter J. Nixon
Regular Paper

Abstract

Members of the Psb28 family of proteins are accessory factors implicated in the assembly and repair of the photosystem II complex. We present here the crystal structure of the Psb28 protein (Tlr0493) found in the thermophilic cyanobacterium Thermosynechococcus elongatus at a resolution of 2.3 Å. Overall the crystal structure of the Psb28 monomer is similar to the solution structures of C-terminally His-tagged Psb28-1 from Synechocystis sp. PCC 6803 obtained previously by nuclear magnetic resonance spectroscopy. One new aspect is that Escherichia coli-expressed T. elongatus Psb28 is able to form dimers in solution and packs as a dimer of dimers in the crystal. Analysis of wild type and mutant strains of Synechocystis 6803 by blue native-polyacrylamide gel electrophoresis suggests that Psb28-1, the closest homologue to T. elongatus Psb28 in this organism, also exists as an oligomer in vivo, most likely a dimer. In line with the prediction based on the crystal structure of T. elongatus Psb28, the addition of a 3× Flag-tag to the C-terminus of Synechocystis 6803 Psb28-1 interferes with the accumulation of the Psb28-1 oligomer in vivo. In contrast, the more distantly related Psb28-2 protein found in Synechocystis 6803 lacks the residues that stabilize dimer formation in the T. elongatus Psb28 crystal and is detected as a monomer in vivo. Overall our data suggest that the dimer interface in the Psb28 crystal might be physiologically relevant.

Keywords

Assembly factor Psb28 Psb28-2 X-ray crystallography Photosystem II Cyanobacteria 

Abbreviations

D1

Photosystem II reaction center subunit encoded by psbA

D2

Photosystem II reaction center subunit encoded by psbD

CP43 and CP47

Photosystem II proximal light-harvesting subunits encoded by psbC and psbB, respectively

RC47

Photosystem II complex lacking CP43

RCC1

Monomeric photosystem II

RCC2

Dimeric photosystem II

RMSD

Root mean square deviation

Notes

Acknowledgments

The authors would like to thank the Biotechnology and Biological Sciences Research Council (BBSRC) for financial support (Grant BB/I00937X/1). JWM holds a BBSRC David Phillips Fellowship (BB/F023308/1). JK and MB were supported by projects Algatech (CZ.1.05/2.1.00/03.0110), RVO61388971 and P501/11/0377 of the Grant Agency of the Czech Republic. The authors wish to thank the staff of the Diamond Light Source for their assistance.

Supplementary material

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Supplementary material 1 (DOC 176 kb)
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Supplementary material 7 (TIFF 644 kb)

References

  1. Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung LW, Kapral GJ, Grosse-Kunstleve RW, McCoy AJ, Moriarty NW, Oeffner R, Read RJ, Richardson DC, Richardson JS, Terwilliger TC, Zwart PH (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D 66:213–221PubMedCrossRefGoogle Scholar
  2. Adir N, Zer H, Shochat S, Ohad I (2003) Photoinhibition—a historical perspective. Photosynth Res 76:343–370PubMedCrossRefGoogle Scholar
  3. Ashkenazy H, Erez E, Martz E, Pupko T, Ben-Tal N (2010) ConSurf 2010: calculating evolutionary conservation in sequence and structure of proteins and nucleic acids. Nucleic Acids Res 38:W529–W533PubMedCrossRefGoogle Scholar
  4. Boehm M, Romero E, Reisinger V, Yu J, Komenda J, Eichacker LA, Dekker JP, Nixon PJ (2011) Investigating the early stages of photosystem II assembly in Synechocystis sp. PCC 6803: isolation of CP47 and CP43 complexes. J Biol Chem 286:14812–14819PubMedCrossRefGoogle Scholar
  5. Boehm M, Yu J, Krynicka V, Barker M, Tichy M, Komenda J, Nixon PJ, Nield J (2012a) Subunit organization of a Synechocystis hetero-oligomeric thylakoid FtsH complex involved in photosystem II repair. Plant Cell 24:3669–3683Google Scholar
  6. Boehm M, Yu J, Reisinger V, Beckova M, Eichacker LA, Schlodder E, Komenda J, Nixon PJ (2012b) Subunit composition of CP43-less photosystem II complexes of Synechocystis sp. PCC 6803: implications for the assembly and repair of photosystem II. Philos Trans R Soc Lond B Biol 367:3444–3454CrossRefGoogle Scholar
  7. Chi W, Ma J, Zhang L (2012) Regulatory factors for the assembly of thylakoid membrane protein complexes. Philos Trans R Soc Lond B Biol 367:3420–3429CrossRefGoogle Scholar
  8. Dobakova M, Tichy M, Komenda J (2007) Role of the PsbI protein in photosystem II assembly and repair in the cyanobacterium Synechocystis sp. PCC 6803. Plant Physiol 145:1681–1691PubMedCrossRefGoogle Scholar
  9. Dobakova M, Sobotka R, Tichy M, Komenda J (2009) Psb28 protein is involved in the biogenesis of the photosystem II inner antenna CP47 (PsbB) in the cyanobacterium Synechocystis sp. PCC 6803. Plant Physiol 149:1076–1086PubMedCrossRefGoogle Scholar
  10. Emsley P, Lohkamp B, Scott WG, Cowtan K (2010) Features and development of Coot. Acta Crystallogr D 66:486–501PubMedCrossRefGoogle Scholar
  11. Ferreira KN, Iverson TM, Maghlaoui K, Barber J, Iwata S (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303:1831–1838PubMedCrossRefGoogle Scholar
  12. Gouet P, Courcelle E, Stuart DI, Metoz F (1999) ESPript: analysis of multiple sequence alignments in postscript. Bioinformatics 15:305–308PubMedCrossRefGoogle Scholar
  13. Guskov A, Kern J, Gabdulkhakov A, Broser M, Zouni A, Saenger W (2009) Cyanobacterial photosystem II at 2.9-Å resolution and the role of quinones, lipids, channels and chloride. Nat Struct Mol Biol 16:334–342PubMedCrossRefGoogle Scholar
  14. Holm L, Rosenstrom P (2010) Dali server: conservation mapping in 3D. Nucl Acids Res 38:W545–W549PubMedCrossRefGoogle Scholar
  15. Hutchinson EG, Thornton JM (1996) PROMOTIF–a program to identify and analyze structural motifs in proteins. Protein Sci 5:212–220PubMedCrossRefGoogle Scholar
  16. Kamiya N, Shen JR (2003) Crystal structure of oxygen-evolving photosystem II from Thermosynechococcus vulcanus at 3.7-Å resolution. Proc Natl Acad Sci USA 100:98–103PubMedCrossRefGoogle Scholar
  17. Komenda J, Reisinger V, Muller BC, Dobakova M, Granvogl B, Eichacker LA (2004) Accumulation of the D2 protein is a key regulatory step for assembly of the photosystem II reaction center complex in Synechocystis PCC 6803. J Biol Chem 279:48620–48629PubMedCrossRefGoogle Scholar
  18. Komenda J, Kuvikova S, Granvogl B, Eichacker LA, Diner BA, Nixon PJ (2007) Cleavage after residue Ala352 in the C-terminal extension is an early step in the maturation of the D1 subunit of Photosystem II in Synechocystis PCC 6803. Biochim Biophys Acta 1767:829–837PubMedCrossRefGoogle Scholar
  19. Komenda J, Sobotka R, Nixon PJ (2012a) Assembling and maintaining the Photosystem II complex in chloroplasts and cyanobacteria. Curr Opin Plant Biol 15:245–251PubMedCrossRefGoogle Scholar
  20. Komenda J, Knoppova J, Kopecna J, Sobotka R, Halada P, Yu J, Nickelsen J, Boehm M, Nixon PJ (2012b) The Psb27 assembly factor binds to the CP43 complex of photosystem II in the cyanobacterium Synechocystis sp. PCC 6803. Plant Physiol 158:476–486PubMedCrossRefGoogle Scholar
  21. Krissinel E, Henrick K (2004) Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallogr D 60:2256–2268PubMedCrossRefGoogle Scholar
  22. Krissinel E, Henrick K (2007) Inference of macromolecular assemblies from crystalline state. J Mol Biol 372:774–797PubMedCrossRefGoogle Scholar
  23. Liu H, Roose JL, Cameron JC, Pakrasi HB (2011) A genetically tagged Psb27 protein allows purification of two consecutive photosystem II (PSII) assembly intermediates in Synechocystis 6803, a cyanobacterium. J Biol Chem 286:24865–24871PubMedCrossRefGoogle Scholar
  24. Loll B, Kern J, Saenger W, Zouni A, Biesiadka J (2005) Towards complete cofactor arrangement in the 3.0 Å resolution structure of photosystem II. Nature 438:1040–1044PubMedCrossRefGoogle Scholar
  25. Mayes SR, Dubbs JM, Vass I, Hideg E, Nagy L, Barber J (1993) Further characterization of the psbH locus of Synechocystis sp. PCC 6803: inactivation of psbH impairs QA to QB electron transport in photosystem 2. Biochemistry 32:1454–1465CrossRefGoogle Scholar
  26. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ (2007) Phaser crystallographic software. J Appl Crystalogr 40:658–674CrossRefGoogle Scholar
  27. Michoux F, Takasaka K, Boehm M, Nixon PJ, Murray JW (2010) Structure of CyanoP at 2.8 Å: implications for the evolution and function of the PsbP subunit of photosystem II. Biochemistry 49:7411–7413PubMedCrossRefGoogle Scholar
  28. Michoux F, Takasaka K, Boehm M, Komenda J, Nixon PJ, Murray JW (2012) Crystal structure of the Psb27 assembly factor at 1.6 Å: implications for binding to Photosystem II. Photosynth Res 110:169–175PubMedCrossRefGoogle Scholar
  29. Murshudov GN, Skubak P, Lebedev AA, Pannu NS, Steiner RA, Nicholls RA, Winn MD, Long F, Vagin AA (2011) REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallogr D 67:355–367PubMedCrossRefGoogle Scholar
  30. Nixon PJ, Trost JT, Diner BA (1992) Role of the carboxy terminus of polypeptide D1 in the assembly of a functional water-oxidizing manganese cluster in photosystem II of the cyanobacterium Synechocystis sp. PCC 6803: assembly requires a free carboxyl group at C-terminal position 344. Biochemistry 31:10859–10871PubMedCrossRefGoogle Scholar
  31. Nixon PJ, Michoux F, Yu J, Boehm M, Komenda J (2010) Recent advances in understanding the assembly and repair of photosystem II. Ann Bot 106:1–16PubMedCrossRefGoogle Scholar
  32. Nowaczyk MM, Krause K, Mieseler M, Sczibilanski A, Ikeuchi M, Rogner M (2012) Deletion of psbJ leads to accumulation of Psb27-Psb28 photosystem II complexes in Thermosynechococcus elongatus. Biochim Biophys Acta 1817:1339–1345PubMedCrossRefGoogle Scholar
  33. Promnares K, Komenda J, Bumba L, Nebesarova J, Vacha F, Tichy M (2006) Cyanobacterial small chlorophyll-binding protein ScpD (HliB) is located on the periphery of photosystem II in the vicinity of PsbH and CP47 subunits. J Biol Chem 281:32705–32713PubMedCrossRefGoogle Scholar
  34. Sakata S, Mizusawa N, Kubota-Kawai H, Sakurai I, Wada H (2013) Psb28 is involved in recovery of photosystem II at high temperature in Synechocystis sp. PCC 6803. Biochim Biophys Acta 1827:50–59PubMedCrossRefGoogle Scholar
  35. Shen G, Boussiba S, Vermaas WFJ (1993) Synechocystis sp. PCC 6803 strains lacking photosystem I and phycobilisome function. Plant Cell 5:1856–1863Google Scholar
  36. Umena Y, Kawakami K, Shen JR, Kamiya N (2011) Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å. Nature 473:55–60PubMedCrossRefGoogle Scholar
  37. Vavilin D, Yao D, Vermaas W (2007) Small Cab-like proteins retard degradation of photosystem II-associated chlorophyll in Synechocystis sp. PCC 6803: kinetic analysis of pigment labeling with 15N and 13C. J Biol Chem 282:37660–37668PubMedCrossRefGoogle Scholar
  38. Vermaas WFJ, Ikeuchi M, Inoue Y (1988) Protein composition of the photosystem II core complex in genetically engineered mutants of the cyanobacterium Synechocystis sp. PCC 6803. Photosynth Res 17:97–113CrossRefGoogle Scholar
  39. Williams JGK (1988) Construction of specific mutations in PSII photosynthetic reaction center by genetic engineering methods in Synechocystis 6803. Methods Enzymol 167:766–778CrossRefGoogle Scholar
  40. Xu H, Vavilin D, Funk C, Vermaas W (2002) Small Cab-like proteins regulating tetrapyrrole biosynthesis in the cyanobacterium Synechocystis sp. PCC 6803. Plant Mol Biol 49:149–160PubMedCrossRefGoogle Scholar
  41. Yang Y, Ramelot TA, Cort JR, Wang D, Ciccosanti C, Hamilton K, Nair R, Rost B, Acton TB, Xiao R, Everett JK, Montelione GT, Kennedy MA (2011) Solution NMR structure of photosystem II reaction center protein Psb28 from Synechocystis sp. Strain PCC 6803. Proteins 79:340–344PubMedCrossRefGoogle Scholar
  42. Yao D, Kieselbach T, Komenda J, Promnares K, Prieto MA, Tichy M, Vermaas W, Funk C (2007) Localization of the small CAB-like proteins in photosystem II. J Biol Chem 282:267–276PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Wojciech Bialek
    • 1
  • Songjia Wen
    • 1
    • 4
  • Franck Michoux
    • 1
    • 5
  • Martina Beckova
    • 2
  • Josef Komenda
    • 3
  • James W. Murray
    • 1
  • Peter J. Nixon
    • 1
  1. 1.Sir Ernst Chain Building–Wolfson Laboratories, Department of Life SciencesImperial College LondonLondonUK
  2. 2.Faculty of ScienceUniversity of South BohemiaCeske BudejoviceCzech Republic
  3. 3.Institute of MicrobiologyAcademy of SciencesTrebonCzech Republic
  4. 4.Department of Biochemistry, LKS Faculty of MedicineThe University of Hong KongPokfulamHong Kong, China
  5. 5.Alkion BiopharmaEvryFrance

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