Multiple Copies of the PsbQ Protein in a Cyanobacterial Photosystem II Assembly Intermediate Complex

Overview

Journal Photosynth Res

Publisher Springer

Date 2015 Mar 25

PMID 25800517

Citations 5

Authors

Haijun Liu

Daniel A Weisz

Himadri B Pakrasi

Affiliations

Soon will be listed here.

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.

Citing Articles

Comparison of PsbQ and Psb27 in photosystem II provides insight into their roles.

Gisriel C, Brudvig G Photosynth Res. 2022; 152(2):177-191.

PMID: 35001227 PMC: 9271139. DOI: 10.1007/s11120-021-00888-2.

N-Terminal Lipid Modification Is Required for the Stable Accumulation of CyanoQ in Synechocystis sp. PCC 6803.

Juneau A, Frankel L, Bricker T, Roose J PLoS One. 2016; 11(9):e0163646.

PMID: 27656895 PMC: 5033237. DOI: 10.1371/journal.pone.0163646.

The Use of Advanced Mass Spectrometry to Dissect the Life-Cycle of Photosystem II.

Weisz D, Gross M, Pakrasi H Front Plant Sci. 2016; 7:617.

PMID: 27242823 PMC: 4862242. DOI: 10.3389/fpls.2016.00617.

Structural Coupling of Extrinsic Proteins with the Oxygen-Evolving Center in Photosystem II.

Ifuku K, Noguchi T Front Plant Sci. 2016; 7:84.

PMID: 26904056 PMC: 4743485. DOI: 10.3389/fpls.2016.00084.

The extrinsic proteins of photosystem II: update.

Roose J, Frankel L, Mummadisetti M, Bricker T Planta. 2016; 243(4):889-908.

PMID: 26759350 DOI: 10.1007/s00425-015-2462-6.

References

Komenda J, Sobotka R, Nixon P . Assembling and maintaining the Photosystem II complex in chloroplasts and cyanobacteria. Curr Opin Plant Biol. 2012; 15(3):245-51. DOI: 10.1016/j.pbi.2012.01.017. View

Guskov A, Kern J, Gabdulkhakov A, Broser M, Zouni A, Saenger W . Cyanobacterial photosystem II at 2.9-A resolution and the role of quinones, lipids, channels and chloride. Nat Struct Mol Biol. 2009; 16(3):334-42. DOI: 10.1038/nsmb.1559. View

Kamiya N, Shen J . Crystal structure of oxygen-evolving photosystem II from Thermosynechococcus vulcanus at 3.7-A resolution. Proc Natl Acad Sci U S A. 2003; 100(1):98-103. PMC: 140893. DOI: 10.1073/pnas.0135651100. View

Shen J, Qian M, Inoue Y, Burnap R . Functional characterization of Synechocystis sp. PCC 6803 delta psbU and delta psbV mutants reveals important roles of cytochrome c-550 in cyanobacterial oxygen evolution. Biochemistry. 1998; 37(6):1551-8. DOI: 10.1021/bi971676i. View

Kashino Y, Inoue-Kashino N, Roose J, Pakrasi H . Absence of the PsbQ protein results in destabilization of the PsbV protein and decreased oxygen evolution activity in cyanobacterial photosystem II. J Biol Chem. 2006; 281(30):20834-20841. DOI: 10.1074/jbc.M603188200. View

Krupnik T, Kotabova E, van Bezouwen L, Mazur R, Garstka M, Nixon P . A reaction center-dependent photoprotection mechanism in a highly robust photosystem II from an extremophilic red alga, Cyanidioschyzon merolae. J Biol Chem. 2013; 288(32):23529-42. PMC: 5395030. DOI: 10.1074/jbc.M113.484659. View

Nowaczyk M, Hebeler R, Schlodder E, Meyer H, Warscheid B, Rogner M . Psb27, a cyanobacterial lipoprotein, is involved in the repair cycle of photosystem II. Plant Cell. 2006; 18(11):3121-31. PMC: 1693947. DOI: 10.1105/tpc.106.042671. View

Nagao R, Suga M, Niikura A, Okumura A, Koua F, Suzuki T . Crystal structure of Psb31, a novel extrinsic protein of photosystem II from a marine centric diatom and implications for its binding and function. Biochemistry. 2013; 52(38):6646-52. DOI: 10.1021/bi400770d. View

Grasse N, Mamedov F, Becker K, Styring S, Rogner M, Nowaczyk M . Role of novel dimeric Photosystem II (PSII)-Psb27 protein complex in PSII repair. J Biol Chem. 2011; 286(34):29548-55. PMC: 3190995. DOI: 10.1074/jbc.M111.238394. View

10.

Kashino Y, Lauber W, Carroll J, Wang Q, Whitmarsh J, Satoh K . Proteomic analysis of a highly active photosystem II preparation from the cyanobacterium Synechocystis sp. PCC 6803 reveals the presence of novel polypeptides. Biochemistry. 2002; 41(25):8004-12. DOI: 10.1021/bi026012+. View

11.

Nickelsen J, Rengstl B . Photosystem II assembly: from cyanobacteria to plants. Annu Rev Plant Biol. 2013; 64:609-35. DOI: 10.1146/annurev-arplant-050312-120124. View

12.

Suga M, Akita F, Hirata K, Ueno G, Murakami H, Nakajima Y . Native structure of photosystem II at 1.95 Å resolution viewed by femtosecond X-ray pulses. Nature. 2014; 517(7532):99-103. DOI: 10.1038/nature13991. View

13.

Umena Y, Kawakami K, Shen J, Kamiya N . Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å. Nature. 2011; 473(7345):55-60. DOI: 10.1038/nature09913. View

14.

Liu H, Roose J, Cameron J, Pakrasi H . A genetically tagged Psb27 protein allows purification of two consecutive photosystem II (PSII) assembly intermediates in Synechocystis 6803, a cyanobacterium. J Biol Chem. 2011; 286(28):24865-71. PMC: 3137061. DOI: 10.1074/jbc.M111.246231. View

15.

Shi L, Schroder W . The low molecular mass subunits of the photosynthetic supracomplex, photosystem II. Biochim Biophys Acta. 2004; 1608(2-3):75-96. DOI: 10.1016/j.bbabio.2003.12.004. View

16.

Vinyard D, Ananyev G, Dismukes G . Photosystem II: the reaction center of oxygenic photosynthesis. Annu Rev Biochem. 2013; 82:577-606. DOI: 10.1146/annurev-biochem-070511-100425. View

17.

Nagao R, Moriguchi A, Tomo T, Niikura A, Nakajima S, Suzuki T . Binding and functional properties of five extrinsic proteins in oxygen-evolving photosystem II from a marine centric diatom, Chaetoceros gracilis. J Biol Chem. 2010; 285(38):29191-9. PMC: 2937949. DOI: 10.1074/jbc.M110.146092. View

18.

Nowaczyk M, Krause K, Mieseler M, Sczibilanski A, Ikeuchi M, Rogner M . Deletion of psbJ leads to accumulation of Psb27-Psb28 photosystem II complexes in Thermosynechococcus elongatus. Biochim Biophys Acta. 2012; 1817(8):1339-45. DOI: 10.1016/j.bbabio.2012.02.017. View

19.

Krieger-Liszkay A, Fufezan C, Trebst A . Singlet oxygen production in photosystem II and related protection mechanism. Photosynth Res. 2008; 98(1-3):551-64. DOI: 10.1007/s11120-008-9349-3. View

20.

Boehm M, Yu J, Reisinger V, Beckova M, Eichacker L, Schlodder E . 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 Sci. 2012; 367(1608):3444-54. PMC: 3497071. DOI: 10.1098/rstb.2012.0066. View