The Photosystem II Assembly Factor Ycf48 from the Cyanobacterium Synechocystis sp. PCC 6803 Is Lipidated Using an Atypical Lipobox Sequence

. 2021 Apr 02 ; 22 (7) : . [epub] 20210402

Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid33918522

Grantová podpora
854126 European Research Council - International
19-29225X Grantová Agentura České Republiky
BB/L003260/1 Biotechnology and Biological Sciences Research Council - United Kingdom

Photochemical energy conversion during oxygenic photosynthesis is performed by membrane-embedded chlorophyll-binding protein complexes. The biogenesis and maintenance of these complexes requires auxiliary protein factors that optimize the assembly process and protect nascent complexes from photodamage. In cyanobacteria, several lipoproteins contribute to the biogenesis and function of the photosystem II (PSII) complex. They include CyanoP, CyanoQ, and Psb27, which are all attached to the lumenal side of PSII complexes. Here, we show that the lumenal Ycf48 assembly factor found in the cyanobacterium Synechocystis sp. PCC 6803 is also a lipoprotein. Detailed mass spectrometric analysis of the isolated protein supported by site-directed mutagenesis experiments indicates lipidation of the N-terminal C29 residue of Ycf48 and removal of three amino acids from the C-terminus. The lipobox sequence in Ycf48 contains a cysteine residue at the -3 position compared to Leu/Val/Ile residues found in the canonical lipobox sequence. The atypical Ycf48 lipobox sequence is present in most cyanobacteria but is absent in eukaryotes. A possible role for lipoproteins in the coordinated assembly of cyanobacterial PSII is discussed.

Zobrazit více v PubMed

Dühring U., Ossenbühl F., Wilde A. Late assembly steps and dynamics of the cyanobacterial photosystem I. J. Biol. Chem. 2007;282:10915–10921. doi: 10.1074/jbc.M609206200. PubMed DOI

Komenda J., Sobotka R., Nixon P.J. Assembling and maintaining the photosystem II complex in chloroplasts and cyanobacteria. Cur. Opin. Plant. Biol. 2012;15:245–251. doi: 10.1016/j.pbi.2012.01.017. PubMed DOI

Nickelsen J., Rengstl B. Photosystem II assembly: From cyanobacteria to plants. Annu. Rev. Plant. Biol. 2013;64:609–635. doi: 10.1146/annurev-arplant-050312-120124. PubMed DOI

Heinz S., Liauw P., Nickelsen J., Nowaczyk M. Analysis of photosystem II biogenesis in cyanobacteria. Biochim. Biophys. Acta. 2016;1857:274–287. doi: 10.1016/j.bbabio.2015.11.007. PubMed DOI

Nowaczyk M.M., Hebeler R., Schlodder E., Meyer H.E., Warscheid B., Rogner M. Psb27, a cyanobacterial lipoprotein, is involved in the repair cycle of photosystem II. Plant. Cell. 2006;18:3121–3131. doi: 10.1105/tpc.106.042671. PubMed DOI PMC

Cormann K.U., Bartsch M., Rogner M., Nowaczyk M.M. Localization of the CyanoP binding site on photosystem II by surface plasrnon resonance spectroscopy. Front. Plant. Sci. 2014;5 doi: 10.3389/fpls.2014.00595. PubMed DOI PMC

Knoppová J., Yu J.F., Konik P., Nixon P.J., Komenda J. CyanoP is involved in the early steps of photosystem II assembly in the cyanobacterium Synechocystis sp PCC 6803. Plant. and Cell Physiology. 2016;57:1921–1931. doi: 10.1093/pcp/pcw115. PubMed DOI

Summerfield T.C., Shand J.A., Bentley F.K., Eaton-Rye J.J. PsbQ (Sll1638) in Synechocystis sp. PCC 6803 is required for Photosystem II activity in specific mutants and in nutrient-limiting conditions. Biochemistry. 2005;44:805–815. doi: 10.1021/bi048394k. PubMed DOI

Kashino Y., Inoue-Kashino N., Roose J.L., Pakrasi H.B. 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;281:20834–20841. doi: 10.1074/jbc.M603188200. PubMed DOI

Fagerlund R.D., Eaton-Rye J.J. The lipoproteins of cyanobacterial photosystem II. J. Photochem. Photobiol. 2011;104:191–203. doi: 10.1016/j.jphotobiol.2011.01.022. PubMed DOI

Nakayama H., Kurokawa K., Lee B.L. Lipoproteins in bacteria: Structures and biosynthetic pathways. FEBS J. 2012;279:4247–4268. doi: 10.1111/febs.12041. PubMed DOI

Buddelmeijer N. The molecular mechanism of bacterial lipoprotein modification—How, when and why? FEMS Microbiol. Rev. 2015;39:246–261. doi: 10.1093/femsre/fuu006. PubMed DOI

Komenda J., Nickelsen J., Tichý M., Prášil O., Eichacker L.A., Nixon P.J. The cyanobacterial homologue of HCF136/YCF48 is a component of an early photosystem II assembly complex and is important for both the efficient assembly and repair of photosystem II in Synechocystis sp PCC 6803. J. Biol. Chem. 2008;283:22390–22399. doi: 10.1074/jbc.M801917200. PubMed DOI

Yu J., Knoppová J., Michoux F., Bialek W., Cota E., Shukla M.K., Strašková A., Pascual Aznar G., Sobotka R., Komenda J., et al. Ycf48 involved in the biogenesis of the oxygen-evolving photosystem II complex is a seven-bladed beta-propeller protein. Proc. Natl. Acad. Sci. U.S.A. 2018;115:E7824–E7833. doi: 10.1073/pnas.1800609115. PubMed DOI PMC

Komenda J., Reisinger V., Muller B.C., Dobáková M., Granvogl B., Eichacker L.A. 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. 2004;279:48620–48629. doi: 10.1074/jbc.M405725200. PubMed DOI

Hagio M., Gombos Z., Varkonyi Z., Masamoto K., Sato N., Tsuzuki M., Wada H. Direct evidence for requirement of phosphatidylglycerol in photosystem II of photosynthesis. Plant. Physiol. 2000;124:795–804. doi: 10.1104/pp.124.2.795. PubMed DOI PMC

Komenda J., Knoppová J., Kopečná J., Sobotka R., Halada P., Yu J.F., Nickelsen J., Boehm M., Nixon P.J. The Psb27 assembly factor binds to the CP43 complex of Photosystem II in the cyanobacterium Synechocystis sp. PCC 6803. Plant. Physiol. 2012;158:476–486. doi: 10.1104/pp.111.184184. PubMed DOI PMC

Knoppová J., Sobotka R., Tichý M., Yu J., Koník P., Halada P., Nixon P.J., Komenda J. Discovery of a chlorophyll binding protein complex involved in the early steps of photosystem II assembly in Synechocystis. Plant. Cell. 2014;26:1200–1212. doi: 10.1105/tpc.114.123919. PubMed DOI PMC

Frain K.M., Robinson C., van Dijl J.M. Transport of folded proteins by the Tat system. Prot. J. 2019;38:377–388. doi: 10.1007/s10930-019-09859-y. PubMed DOI PMC

Babu M.M., Priya M.L., Selvan A.T., Madera M., Gough J., Aravind L., Sankaran K. A database of bacterial lipoproteins (DOLOP) with functional assignments to predicted lipoproteins. J. Bacteriol. 2006;188:2761–2773. doi: 10.1128/JB.188.8.2761-2773.2006. PubMed DOI PMC

Huang G., Xiao Y., Pi X., Zhao L., Zhu Q., Wang W., Kuang T., Han G., Sui S.-F., Shen J.-R. Structural insights into a dimeric Psb27-photosystem II complex from a cyanobacterium Thermosynechococcus vulcanus. Proc. Natl. Acad. Sci. USA. 2021;118:e2018053118. doi: 10.1073/pnas.2018053118. PubMed DOI PMC

Mattoo A.K., Edelman M. Intramembrane translocation and posttranslational palmitoylation of the chloroplast 32-kDa herbicide-binding protein. Proc. Natl. Acad. Sci. USA. 1987;84:1497–1501. doi: 10.1073/pnas.84.6.1497. PubMed DOI PMC

Rengstl B., Knoppová J., Komenda J., Nickelsen J. Characterization of a Synechocystis double mutant lacking the photosystem II assembly factors YCF48 and Sll0933. Planta. 2013;237:471–480. doi: 10.1007/s00425-012-1720-0. PubMed DOI

Bučinská L., Kiss E., Konik P., Knoppová J., Komenda J., Sobotka R. The ribosome-bound protein Pam68 promotes insertion of chlorophyll into the CP47 subunit of Photosystem II. Plant. Physiol. 2018;176:2931–2942. doi: 10.1104/pp.18.00061. PubMed DOI PMC

Juneau A.D., Frankel L.K., Bricker T.M., Roose J.L. N-Terminal Lipid Modification Is Required for the Stable Accumulation of CyanoQ in Synechocystis sp. PCC 6803. PLoS ONE. 2016;11:e0163646. doi: 10.1371/journal.pone.0163646. PubMed DOI PMC

Liu H., Zhang H., Weisz D.A., Vidavsky I., Gross M.L., Pakrasi H.B. MS-based cross-linking analysis reveals the location of the PsbQ protein in cyanobacterial photosystem II. Proc. Natl. Acad. Sci. USA. 2014;111:4638–4643. doi: 10.1073/pnas.1323063111. PubMed DOI PMC

Tang X.S., Chisholm D.A., Dismukes G.C., Brudvig G.W., Diner B.A. Spectroscopic evidence from site-directed mutants of Synechocystis PCC6803 in favor of a close interaction between histidine-189 and redox-active tyrosine-160 both of polypeptide D2 of the photosystem II reaction center. Biochemistry. 1993;32:13742–13748. doi: 10.1021/bi00212a045. PubMed DOI

Suzuki H., Yu J.F., Kobayashi T., Nakanishi H., Nixon P.J., Noguchi T. Functional roles of D2-Lys317 and the interacting chloride ion in the water oxidation reaction of photosystem II as revealed by Fourier transform infrared analysis. Biochemistry. 2013;52:4748–4757. doi: 10.1021/bi301699h. PubMed DOI PMC

Porra R.J., Thompson W.A., Kriedemann P.E. Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: Verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim. Biophys. Acta. 1989;975:384–394. doi: 10.1016/S0005-2728(89)80347-0. DOI

Schägger H., von Jagow G. Blue native electrophoresis for isolation of membrane protein complexes in enzymatically active form. Anal. Biochem. 1991;199:223–231. doi: 10.1016/0003-2697(91)90094-A. PubMed DOI

Wittig I., Karas M., Schagger H. High resolution clear native electrophoresis for in-gel functional assays and fluorescence studies of membrane protein complexes. Mol. Cell. Proteomics. 2007;6:1215–1225. doi: 10.1074/mcp.M700076-MCP200. PubMed DOI

Dobáková M., Sobotka R., Tichý M., Komenda J. Psb28 protein is involved in the biogenesis of the photosystem II inner antenna CP47 (PsbB) in the cyanobacterium Synechocystis sp. PCC 6803. Plant. Physiol. 2009;149:1076–1086. doi: 10.1104/pp.108.130039. PubMed DOI PMC

Kiss E., Knoppová J., Aznar G.P., Pilný J., Yu J., Halada P., Nixon P.J., Sobotka R., Komenda J. A photosynthesis-specific rubredoxin-like protein is required for efficient association of the D1 and D2 proteins during the initial steps of photosystem II assembly. Plant. Cell. 2019;31:2241–2258. doi: 10.1105/tpc.19.00155. PubMed DOI PMC

Whitelegge J.P., Gundersen C.B., Faull K.F. Electrospray-ionization mass spectrometry of intact intrinsic membrane proteins. Protein Sci. 1998;7:1423–1430. doi: 10.1002/pro.5560070619. PubMed DOI PMC

Zhang Z., Marshall A.G. A universal algorithm for fast and automated charge state deconvolution of electrospray mass-to-charge ratio spectra. J. Am. Soc. Mass Spectr. 1998;9:225–233. doi: 10.1016/S1044-0305(97)00284-5. PubMed DOI

Katoh K., Standley D.M. MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Mol. Biol. Evol. 2013;30:772–780. doi: 10.1093/molbev/mst010. PubMed DOI PMC

Ponce-Toledo R.I., Deschamps P., López-García P., Zivanovic Y., Benzerara K., Moreira D. An early-branching freshwater cyanobacterium at the origin of plastids. Curr. Biol. 2017;27:386–391. doi: 10.1016/j.cub.2016.11.056. PubMed DOI PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...