Skip to main content
Log in

Multiple copies of the PsbQ protein in a cyanobacterial photosystem II assembly intermediate complex

  • Regular Paper
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

Photosystem II (PSII) undergoes frequent damage owing to the demanding electron transfer chemistry it performs. To sustain photosynthetic activity, damaged PSII undergoes a complex repair cycle consisting of many transient intermediate complexes. By purifying PSII from the cyanobacterium Synechocystis sp. PCC 6803 using a histidine-tag on the PsbQ protein, a lumenal extrinsic subunit, a novel PSII assembly intermediate was isolated in addition to the mature PSII complex. This new complex, which we refer to as PSII-Q4, contained four copies of the PsbQ protein per PSII monomer, instead of the expected one copy. In addition, PSII-Q4 lacked two other lumenal extrinsic proteins, PsbU and PsbV, which are present in the mature PSII complex. We suggest that PSII-Q4 is a late PSII assembly intermediate that is formed just before the binding of PsbU and PsbV, and we incorporate these results into an updated model of PSII assembly.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Adir N, Zer H, Shochat S, Ohad I (2003) Photoinhibition-a historical perspective. Photosynth Res 76:343–370

    Article  CAS  PubMed  Google Scholar 

  • Aro E-M, Allahverdiyeva Y (2012) Photosynthetic responses of plants to excess light: mechanisms and conditions for photoinhibition, excess energy dissipation, and repair. In: Eaton JJ, Tripathy BC, Sharkey TD (eds) Photosynthesis: plastid biology, energy conversion and carbon assimilation. Advances in photosynthesis and respiration. Springer, Dordrecht, pp 275–297

    Google Scholar 

  • Becker K, Cormann KU, Nowaczyk MM (2011) Assembly of the water-oxidizing complex in photosystem II. J Photochem Photobiol B 104:204–211

    Article  CAS  PubMed  Google Scholar 

  • Boehm M, Yu J, Reisinger V, Beckova M, Eichacker LA, Schlodder E, Komenda J, Nixon PJ (2012) 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 B 367:3444–3454

    Article  CAS  Google Scholar 

  • Bricker T, Frankel L (2002) The structure and function of CP47 and CP43 in photosystem II. Photosynth Res 72:131–146

    Article  CAS  PubMed  Google Scholar 

  • Bricker TM, Morvant J, Masri N, Sutton HM, Frankel LK (1998) Isolation of a highly active photosystem II preparation from Synechocystis 6803 using a histidine-tagged mutant of CP47. Biochim Biophys Acta 1409:50–57

    Article  CAS  PubMed  Google Scholar 

  • Bricker TM, Roose JL, Fagerlund RD, Frankel LK, Eaton-Rye JJ (2012) The extrinsic proteins of photosystem II. Biochim Biophys Acta 1817:121–142

    Article  CAS  PubMed  Google Scholar 

  • Dasgupta J, Ananyev GM, Dismukes GC (2008) Photoassembly of the water-oxidizing complex in photosystem II. Coord Chem Rev 252:347–360

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ferreira KN, Iverson TM, Maghlaoui K, Barber J, Iwata S (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303:1831–1838

    Article  CAS  PubMed  Google Scholar 

  • Grasse N, Mamedov F, Becker K, Styrin S, Rögner M, Nowaczyk MM (2011) Role of novel dimeric photosystem II (PSII)-Psb27 protein complex in PSII repair. J Biol Chem 286:29548–29555

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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 16:334–342

    Article  CAS  PubMed  Google Scholar 

  • Kamiya N, Shen J-R (2003) Crystal structure of oxygen-evolving photosystem II from Thermosynechococcus vulcanus at 3.7-Å resolution. Proc Natl Acad Sci USA 100:98–103

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kashino Y, Koike H, Satoh K (2001) An improved sodium dodecyl sulfate-polyacrylamide gel electrophoresis system for the analysis of membrane protein complexes. Electrophoresis 22:1004–1007

    Article  CAS  PubMed  Google Scholar 

  • Kashino Y, Lauber WM, Carroll JA, Wang Q, Whitmarsh J, Satoh K, Pakrasi HB (2002) Proteomic analysis of a highly active photosystem II preparation from the cyanobacterium Synechocystis sp. PCC 6803 reveals the presence of novel polypeptides. Biochemistry 41:8004–8012

    Article  CAS  PubMed  Google Scholar 

  • Kashino Y, Inoue-Kashino N, Roose JL, Pakrasi HB (2006) Absence of the PsbQ protein results in destabilization of the PsbV protein and decreased oxygen evolution activity in cyanobacterial photosystem II. J Biol Chem 281:20834–20841

    Article  CAS  PubMed  Google Scholar 

  • Komenda J, Reisinger V, Müller BC, Dobáková 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 279:48620–48629

    Article  CAS  PubMed  Google Scholar 

  • Komenda J, Sobotka R, Nixon PJ (2012) Assembling and maintaining the photosystem II complex in chloroplasts and cyanobacteria. Curr Opin Plant Biol 15:245–251

    Article  CAS  PubMed  Google Scholar 

  • Krieger-Liszkay A, Fufezan C, Trebst A (2008) Singlet oxygen production in photosystem II and related protection mechanism. Photosynth Res 98:551–564

    Article  CAS  PubMed  Google Scholar 

  • Krupnik T, Kotabova E, van Bezouwen LS, Mazur R, Garstka M, Nixon PJ, Barber J, Kana R, Boekema EJ, Kargul J (2013) A reaction center-dependent photoprotection mechanism in a highly robust Photosystem II from an extremophilic Red alga, Cyanidioschyzon merolae. J Biol Chem 288:23529–23542

    Article  CAS  PubMed  Google Scholar 

  • 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 286:24865–24871

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Liu H, Chen J, Huang RY-C, Weisz D, Gross ML, Pakrasi HB (2013) Mass spectrometry-based footprinting reveals structural dynamics of loop E of the chlorophyll-binding protein CP43 during photosystem II assembly in the cyanobacterium Synechocystis 6803. J Biol Chem 288:14212–14220

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Liu H, Zhang H, Weisz DA, Vidavsky I, Gross ML, Pakrasi HB (2014) MS-based cross-linking analysis reveals the location of the PsbQ protein in cyanobacterial photosystem II. Proc Natl Acad Sci USA 111:4638–4643

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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 438:1040–1044

    Article  CAS  PubMed  Google Scholar 

  • Nagao R, Moriguchi A, Tomo T, Niikura A, Nakajima S, Suzuki T, Okumura A, Iwai M, Shen J-R, Ikeuchi M, Enami I (2010) Binding and functional properties of five extrinsic proteins in oxygen-evolving photosystem II from a marine centric diatom, Chaetoceros gracilis. J Biol Chem 285:29191–29199

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nagao R, Suga M, Niikura A, Okumura A, Koua FHM, Suzuki T, Tomo T, Enami I, Shen J-R (2013) Crystal structure of Psb31, a novel extrinsic protein of photosystem II from a marine centric diatom and implications for its binding and function. Biochemistry 52:6646–6652

    Article  CAS  PubMed  Google Scholar 

  • Nickelsen J, Rengstl B (2013) Photosystem II assembly: from cyanobacteria to plants. Annu Rev Plant Biol 64:609–635

    Article  CAS  PubMed  Google Scholar 

  • Nixon PJ, Michoux F, Yu J, Boehm M, Komenda J (2010) Recent advances in understanding the assembly and repair of photosystem II. Ann Bot 106:1–16

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nowaczyk MM, Hebeler R, Schlodder E, Meyer HE, Warscheid B, Rögner M (2006) Psb27, a cyanobacterial lipoprotein, is involved in the repair cycle of photosystem II. Plant Cell 18:3121–3131

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nowaczyk MM, Krause K, Mieseler M, Sczibilanski A, Ikeuchi M, Rögner M (2012) Deletion of psbJ leads to accumulation of Psb27–Psb28 photosystem II complexes in Thermosynechococcus elongatus. Biochim Biophys Acta 1817:1339–1345

    Article  CAS  PubMed  Google Scholar 

  • Rappaport F, Diner BA (2008) Primary photochemistry and energetic leading to the oxidation of the (Mn)4Ca cluster and to the evolution of molecular oxygen in photosystem II. Coord Chem Rev 252:259–272

    Article  CAS  Google Scholar 

  • Rögner M, Dekker JP, Boekema EJ, Witt HT (1987) Size, shape, and mass of the oxygen-evolving photosystem II complex from the thermophilic cyanobacterium Synechococcus sp. FEBS Lett 219:207–211

    Article  Google Scholar 

  • Roose JL, Pakrasi HB (2008) The Psb27 protein facilitates manganese cluster assembly in photosystem II. J Biol Chem 283:4044–4050

    Article  CAS  PubMed  Google Scholar 

  • Roose JL, Kashino Y, Pakrasi HB (2007a) The PsbQ protein defines cyanobacterial photosystem II complexes with highest activity and stability. Proc Natl Acad Sci USA 104:2548–2553

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Roose JL, Wegener KM, Pakrasi HB (2007b) The extrinsic proteins of photosystem II. Photosynth Res 92:369–387

    Article  CAS  PubMed  Google Scholar 

  • Satoh K (1980) F-695 emission from the purified photosystem II chlorophyll a-protein complex. FEBS Lett 110:53–56

    Article  CAS  Google Scholar 

  • Schägger H, von Jagow G (1991) Blue native electrophoresis for isolation of membrane protein complexes in enzymatically active form. Anal Biochem 199:223–231

    Article  PubMed  Google Scholar 

  • Shen J-R, Qian M, Inoue Y, Burnap RL (1998) Functional characterization of Synechocystis sp. PCC 6803 ΔpsbU and ΔpsbV mutants reveals important roles of cytochrome c-550 in cyanobacterial oxygen evolution. Biochemistry 37:1551–1558

    Article  CAS  PubMed  Google Scholar 

  • Shi L-X, Schröder WP (2004) The low molecular mass subunits of the photosynthetic supracomplex, photosystem II. Biochim Biophys Acta 1608:75–96

    Article  CAS  PubMed  Google Scholar 

  • Shi L-X, Hall M, Funk C, Schröder WP (2012) Photosystem II, a growing complex: updates on newly discovered components and low molecular mass proteins. Biochim Biophys Acta 1817:13–25

    Article  CAS  PubMed  Google Scholar 

  • Suga M, Akita F, Hirata K, Ueno G, Murakami H, Nakajima Y, Shimizu T, Yamashita K, Yamamoto M, Ago H, Shen JR (2015) Native structure of photosystem II at 1.95 Å resolution viewed by femtosecond X-ray pulses. Nature 517:99–103

    Article  CAS  PubMed  Google Scholar 

  • Summerfield TC, Shand JA, Bentley FK, Eaton-Rye JJ (2005) PsbQ (Sll1638) in Synechocystis sp. PCC 6803 is required for photosystem II activity in specific mutants and in nutrient-limiting conditions. Biochemistry 44:805–815

    Article  CAS  PubMed  Google Scholar 

  • Thornton LE, Ohkawa H, Roose JL, Kashino Y, Keren N, Pakrasi HB (2004) Homologs of plant PsbP and PsbQ proteins are necessary for regulation of photosystem II activity in the cyanobacterium Synechocystis 6803. Plant Cell 16:2164–2175

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tyystjärvi E (2013) Photoinhibition of photosystem II. Int Rev Cell Mol Biol 300:243–303

    Article  PubMed  Google Scholar 

  • Umena Y, Kawakami K, Shen JR, Kamiya N (2011) Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å. Nature 473:55–61

    Article  CAS  PubMed  Google Scholar 

  • Vinyard DJ, Ananyev GM, Dismukes GC (2013) Photosystem II: the reaction center of oxygenic photosynthesis. Annu Rev Biochem 82:577–606

    Article  CAS  PubMed  Google Scholar 

  • Watanabe M, Iwai M, Narikawa R, Ikeuchi M (2009) Is the photosystem II complex a monomer or a dimer? Plant Cell Physiol 50:1674–1680

    Article  CAS  PubMed  Google Scholar 

  • Zouni A, Witt HT, Kern J, Fromme P, Krauss N, Saenger W, Orth P (2001) Crystal structure of photosystem II from Synechococcus elongatus at 3.8 Å resolution. Nature 409:739–743

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Dr. Terry Bricker for the kind gift of the HT3 strain of Synechocystis 6803, and all members of the Pakrasi lab for collegial discussions. This work was supported by funding from the National Science Foundation (NSF-MCB0745611) to H.B.P.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Himadri B. Pakrasi.

Additional information

Haijun Liu and Daniel A. Weisz have contributed equally to this study.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, H., Weisz, D.A. & Pakrasi, H.B. Multiple copies of the PsbQ protein in a cyanobacterial photosystem II assembly intermediate complex. Photosynth Res 126, 375–383 (2015). https://doi.org/10.1007/s11120-015-0123-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-015-0123-z

Keywords

Navigation