Phycobilisome Linker Proteins Are Phosphorylated in Synechocystis sp. PCC 6803

Abstract

The controversial issue of protein phosphorylation from the photosynthetic apparatus of Synechocystis sp. PCC 6803 has been reinvestigated using new detection tools that include various immunological and in vivo labeling approaches. The set of phosphoproteins detected with these methods includes ferredoxin-NADPH reductase and the linker proteins of the phycobilisome antenna. Using mutants that lack a specific set of linker proteins and are affected in phycobilisome assembly, we show that the phosphoproteins from the phycobilisomes correspond to the membrane, rod, and rod-core linkers. These proteins are in a phosphorylated state within the assembled phycobilisomes. Their dephosphorylation requires partial disassembly of the phycobilisomes and further contributes to their complete disassembly in vitro. In vivo we observed linker dephosphorylation upon long-term exposure to higher light intensities and under nitrogen limitation, two conditions that lead to remodeling and turnover of phycobilisomes. We conclude that this phosphorylation process is instrumental in the regulation of assembly/disassembly of phycobilisomes and should participate in signaling for their proteolytic cleavage and degradation. The controversial issue of protein phosphorylation from the photosynthetic apparatus of Synechocystis sp. PCC 6803 has been reinvestigated using new detection tools that include various immunological and in vivo labeling approaches. The set of phosphoproteins detected with these methods includes ferredoxin-NADPH reductase and the linker proteins of the phycobilisome antenna. Using mutants that lack a specific set of linker proteins and are affected in phycobilisome assembly, we show that the phosphoproteins from the phycobilisomes correspond to the membrane, rod, and rod-core linkers. These proteins are in a phosphorylated state within the assembled phycobilisomes. Their dephosphorylation requires partial disassembly of the phycobilisomes and further contributes to their complete disassembly in vitro. In vivo we observed linker dephosphorylation upon long-term exposure to higher light intensities and under nitrogen limitation, two conditions that lead to remodeling and turnover of phycobilisomes. We conclude that this phosphorylation process is instrumental in the regulation of assembly/disassembly of phycobilisomes and should participate in signaling for their proteolytic cleavage and degradation. Phycobilisomes (PBSs) 1The abbreviations used are: PBS, phycobilisome; APC, allophycocyanin; HL, high light; LL, low light; LCM, core-membrane linker; LR, rod linker; LRC, rod-core linker; μE, microeinstein; PC, phycocyanin. are large multimeric protein structures that function as an extrinsic light-harvesting antenna in cyanobacteria and red algae. They are located at the outer surface of thylakoid membranes where they transfer their excitation energy to the photosynthetic reaction centers that are embedded within the lipid bilayer. Our knowledge, generated over >30 years from biochemical and biophysical analysis, genetics, electron microscopy, and x-ray crystallography, led to improvement of the PBS structural model (1Sidler W.A. Bryant D.A. The Molecular Biology of Cyanobacteria. Kluwer Academic Publishers, Norwell, MA1994: 139-216Crossref Google Scholar). In Synechocystis sp. PCC 6803, PBSs are comprised of the bilin-containing proteins allophycocyanin (APC) and phycocyanin (PC) and colorless linker proteins that assemble PC and APC substructures and tune their properties to optimize energy transfer (2Glazer A.N. J. Biol. Chem. 1989; 264: 1-4Abstract Full Text PDF PubMed Google Scholar). Linker proteins can be divided into four groups: (i) rod-core linkers (LRC) that attach the peripheral rods to the PBS core; (ii) rod linkers ((LR10,LR33,LR35)) that associate PC substructures into rod segments; (iii) the small core linkers ((LC8)) that are associated with trimeric APC at the peripheries of the core cylinders; and (iv) the core-membrane linker ((LCM99)) that acts in the organization of the PBS core and is the major terminal energy emitter to photosystem II (1Sidler W.A. Bryant D.A. The Molecular Biology of Cyanobacteria. Kluwer Academic Publishers, Norwell, MA1994: 139-216Crossref Google Scholar, 2Glazer A.N. J. Biol. Chem. 1989; 264: 1-4Abstract Full Text PDF PubMed Google Scholar, 3Capuano V. Braux A.S. Tandeau de Marsac N. Houmard J. J. Biol. Chem. 1991; 266: 7239-7247Abstract Full Text PDF PubMed Google Scholar). PBSs represent a major biosynthetic commitment of a cyanobacterial cell; apart from their light-harvesting function in photosynthesis, PBSs are recruited as a principal nutrient source under starvation conditions. This dual function implies specific regulation for assembling, disassembling, and remodeling the PBS structure according to changes in metabolic and energy requirements. Cyanobacteria have evolved several molecular mechanisms for acclimation of the PBS antenna that operates at the transcriptional (4Belknap W.R. Haselkorn R. EMBO J. 1987; 6: 871-884Crossref PubMed Scopus (81) Google Scholar, 5de Lorimier R.M. Smith R.L. Stevens Jr., S.E. Plant Physiol. 1991; 98: 1003-1010Crossref Scopus (37) Google Scholar), translational, and post-translational levels (6Grossman A.R. Schaefer M.R. Chiang G.G. Collier J.L. J. Bacteriol. 1993; 175: 575-582Crossref PubMed Google Scholar, 7Pojidaeva E. Zinchenko V. Shestakov S.V. Sokolenko A. J. Bacteriol. 2004; 186: 3991-3999Crossref PubMed Scopus (19) Google Scholar). Taken together, these regulatory mechanisms contribute to remodeling PBS composition, size, and number per thylakoid membrane when cells are exposed to environmental changes. It has been suggested that chaperones may be essential in the first steps of PBS assembly when the degradation of biliproteins competes with protein biosynthesis (8Anderson L.K. Toole C.M. Mol. Microbiol. 1998; 30: 467-474Crossref PubMed Scopus (65) Google Scholar). The subsequent modulation of PBS structures upon acclimation to various stresses leads in some cases to partial or full disassembly, degradation, and reutilization of phycobiliproteins. For instance, high rates of PBS degradation were observed for various cyanobacterial strains upon nutrient deprivation and high light stress (6Grossman A.R. Schaefer M.R. Chiang G.G. Collier J.L. J. Bacteriol. 1993; 175: 575-582Crossref PubMed Google Scholar, 9Duke C.S. Cezeaux A. Allen M.M. J. Bacteriol. 1989; 171: 1960-1966Crossref PubMed Google Scholar, 10Collier J.L. Grossman A.R. J. Bacteriol. 1992; 174: 4718-4726Crossref PubMed Scopus (235) Google Scholar, 11Garnier F. Dubacq J.P. Thomas J.C. Plant Physiol. 1994; 106: 747-754Crossref PubMed Scopus (37) Google Scholar). The nbl gene family encodes a major group of proteins that is involved in stress signaling and the control of PBS degradation. Two signaling components, a response regulator and a histidine kinase, are encoded by the nblR and nblS genes, respectively (12Schwarz R. Grossmann A.R. Proc. Natl. Acad. Sci. U. S. A. 1998; 95: 11008-11013Crossref PubMed Scopus (124) Google Scholar, 13van Waasbergen L.G. Dolganov N. Grossman A.R. J. Bacteriol. 2002; 184: 2481-2490Crossref PubMed Scopus (120) Google Scholar), whereas two other genes code for NblA and NblB, which are required for coordination of PBS degradation under nutrient deprivation (14Collier J.L. Grossman A.R. EMBO J. 1994; 13: 1039-1047Crossref PubMed Scopus (211) Google Scholar, 15Dolganov N. Grossmann A.R. J. Bacteriol. 1999; 181: 610-617Crossref PubMed Google Scholar, 16Baier K. Nicklisch S. Grundner C. Reinecke J. Lockau W. FEMS Microbiol. Lett. 2001; 195: 35-39Crossref PubMed Google Scholar, 17Baier K. Lehmann H. Stephan D.P. Lockau W. Microbiology (Read.). 2004; 150: 2739-2749Crossref PubMed Scopus (62) Google Scholar). The cleavage of linker proteins has been suggested to be a prerequisite for the complete degradation of phycobiliproteins (7Pojidaeva E. Zinchenko V. Shestakov S.V. Sokolenko A. J. Bacteriol. 2004; 186: 3991-3999Crossref PubMed Scopus (19) Google Scholar, 18Glazer A.N. Methods Enzymol. 1988; 167: 291-303Crossref PubMed Scopus (134) Google Scholar, 19Gottschalk L. Fisher R. Lottspeich F. Scheer H. Photochem. Photobiol. 1991; 54: 283-288Crossref Scopus (18) Google Scholar, 20Li H. Sherman L.A. Arch. Microbiol. 2002; 178: 256-266Crossref PubMed Scopus (61) Google Scholar). Because PBSs represent tightly organized structures, it is not yet clear which protein determinants can trigger the initiation of the disassembly process and how such structural components as linker proteins, which are embedded in rod discs (21Yu M.-H. Glazer A.N. J. Biol. Chem. 1982; 257: 3429-3433Abstract Full Text PDF PubMed Google Scholar, 22Reuter W. Wiegand G. Huber R. Than M.E. Proc. Natl. Acad. Sci. U. S. A. 1999; 96: 1363-1368Crossref PubMed Scopus (126) Google Scholar, 23Stec B. Troxler R.F. Teeter M.M. Biophys. J. 1999; 76: 2912-2921Abstract Full Text Full Text PDF PubMed Scopus (80) Google Scholar), can become accessible to regulatory proteins and proteolytic enzymes. The facility by which phosphate groups can be added to a variety of amino acids within proteins and thereby induce changes in enzymatic activity, stability, or binding properties makes protein phosphorylation an attractive way of regulating cellular responses to the environment (24Pawson T. FASEB J. 1994; 8: 1112-1113Crossref PubMed Scopus (19) Google Scholar). In plant and algal chloroplasts, the light-harvesting antenna is a flexible structure that can accommodate changes in environmental conditions. Its post-translational modification by phosphorylation at some threonine residues triggers changes in protein conformation and redistribution of the antenna between the two photosystems in a process known as state transition (25Bonaventura C. Myers J. Biochim. Biophys. Acta. 1969; 189: 366-383Crossref PubMed Scopus (513) Google Scholar, 26Murata N. Biochim. Biophys. Acta. 1969; 172: 242-251Crossref PubMed Scopus (451) Google Scholar). Changes in protein phosphorylation also control the rate of proteolysis of the antenna proteins under excess illumination (27Yang D.H. Webster J. Adam Z. Lindahl M. Andersson B. Plant Physiol. 1998; 118: 827-834Crossref PubMed Scopus (106) Google Scholar). Phosphorylation changes had been suggested as contributing to some mechanisms for PBS modifications a decade ago, but the experimental support to this view remained controversial (28Bruce D. Brimble S. Bryant D.A. Biochim. Biophys. Acta. 1989; 974: 66-73Crossref PubMed Scopus (89) Google Scholar). Most attempts to detect phosphorylation within the PBS antenna in cyanobacteria were with in which the phosphorylation of in sp. PCC M. A. Molecular of in the of Scholar). In the we show that some linker proteins are phosphorylated within the assembled phycobilisomes in Synechocystis sp. PCC The phosphorylation of these proteins can be detected with as as by the of a that We show that strains that lack specific of linker proteins also these We in vivo and in that the dephosphorylation of linkers partial PBS disassembly and leads to their disassembly, a that may be a prerequisite for protein degradation. these we the of linker phosphorylation in the response to changes in levels and to nitrogen two environmental changes that remodeling and degradation of and sp. PCC 6803 and were in R. Methods Enzymol. 1988; 167: PubMed Scopus Google under a light of at For phosphorylation at a low light to and to high light or to nitrogen deprivation for For nitrogen cells were by at for and in The cells were under at for a further nitrogen were by and with and of and membrane proteins were as Shestakov S.V. Mol. Microbiol. 1992; 6: PubMed Scopus Google Scholar). For of and proteins from to cells were by with a from in a at with a of in PBSs were as A.N. Methods Enzymol. 1988; 167: 291-303Crossref PubMed Scopus (134) Google with some modifications (7Pojidaeva E. Zinchenko V. Shestakov S.V. Sokolenko A. J. Bacteriol. 2004; 186: 3991-3999Crossref PubMed Scopus (19) Google Scholar). The PBS with by and subsequent of PBSs by using phosphate The of PBSs that the in the in phosphate and at for at The PBS in and at and per and PBS proteins were by according to PubMed Scopus Google Scholar). For PBS the of the at and an of biliproteins to per to and nitrogen deprivation were to and cells were into membrane and as For protein were with or the were detected by immunological with or with the For of the for residues were with membranes to the immunological PBS proteins were by A. The and were detected by the with and were by with at For detection of PBS bilin-containing proteins by were by red with excitation and at Phosphorylation of in phosphorylation of Synechocystis cellular proteins in vivo according to K. Tandeau de Marsac N. J. Bacteriol. 1994; PubMed Scopus Google Scholar). were in under to an of were by and in phosphate to an of For of to a small to The phosphorylation by the of of with subsequent under for cyanobacterial proteins were with with and in for the by and in dephosphorylation of thylakoid and PBS proteins, were with according to C. J.L. J. Biol. Chem. 1991; 266: Full Text PDF PubMed Google Scholar). proteins were with in a and for at The reaction by the of Phosphorylation of in the Synechocystis of photosynthetic proteins in Synechocystis by two immunological detection with phosphorylated amino residues or in vivo phosphorylation with For immunological protein were from cyanobacterial cells under conditions. protein were by and membrane for immunological detection of phosphorylated proteins The of and in not from of and residues or from the of or were the immunological Because these not the of phosphorylated proteins not we that phosphorylation at the threonine and the In subsequent we to the of phosphoproteins were detected in thylakoid with residues The phosphorylation were for proteins with molecular of and these proteins represent a set of phosphoproteins that are to be detected by an immunological detect phosphoproteins that phosphate we an in vivo labeling with This set of phosphoproteins in thylakoid membranes in the of and and a phosphorylated of of thylakoid membrane with of the immunological suggested that the major phosphorylated proteins in an of phycobilisome Because the phosphorylation of the PBS antenna has been a controversial issue for a we the immunological to a PBS PBS antenna proteins were from Synechocystis cells and by were by with or the The of PBSs two groups of proteins, proteins in the molecular of and proteins to the protein and linker the rod and the rod-core linkers as as the and the of the membrane respectively A.N. Methods Enzymol. 1988; 167: 291-303Crossref PubMed Scopus (134) Google Scholar). which is a and for protein of phycobiliproteins and proteins were with or the which with phosphorylated residues phosphorylated that to the linker proteins and and which were also in thylakoid membrane with the in of the between the and the and that is to changes in various and two phosphorylated in the molecular between and were also detected in thylakoid membrane and in the be in PBS at with the were with the it in the of the of the in proteins, the with PBS proteins with a red set at an for detection of bilin-containing We observed a with and from the PC and APC This that the from to the of proteins and not to the phosphorylation of Phosphorylation of in the phosphorylation from the PBS linkers from the immunological to strains that had a in PBS of a lack of rods or that PBS antenna The a in genes APC proteins in a G. C. Plant Mol. Biol. 1998; PubMed Scopus Google Scholar). The is in the and G. PBSs were in but APC and were in strains were for the of linker proteins by with various linker and bilin-containing to immunological analysis, of the PBS proteins in the In the the of PC rods and the rod the of LRC, which the core and the PC rods These rod-core linkers were in the but to a in the The APC in the PBS core and in a as in the The phosphorylation in thylakoid membranes of the and strains also with PBSs from the were as a control for the of linker The in the of the protein phosphorylation of thylakoid membranes as with the in from a exposure of to a with the protein in the of the phosphorylated in the of rod with the to PBS phosphorylated were detected at linker in the The core-membrane linker remained as a in the at the rate as in the whereas phosphorylated remained at the of the other linkers. Because the of linker in the mutants in the of the we that the rod linkers were phosphorylated in the PBSs of the in an of linker phosphorylation in PBSs were in by with an that is specific for of threonine or We observed partial dephosphorylation of the linker proteins Because linker proteins are embedded in PC we that the dephosphorylation not be accessible to the in the assembled PBSs are in or in phosphate of low they are M. Plant Physiol. 1982; Google Scholar). the dephosphorylation of linker proteins is by the assembly state of the we the or PBS with in by the of the the proteins, this the PBSs at the of the in from or PBS at the of the in linker proteins in the of were detected with an and are in the of linker proteins were phosphorylated in but in where PBS proteins were detected by dephosphorylation by PBS phosphorylated linkers in PBSs but other phosphorylation observed over the the the phycobiliproteins were to the of the that they further This that linker proteins are to dephosphorylation in PBS structures and that their dephosphorylation disassembly of the PBS antenna. of PBS under or in higher plant chloroplasts, of light-harvesting antenna is involved in state and antenna degradation, two that are by changes in light and light We that the rate of linker not the acclimation to state not the cyanobacterial PBS antenna is and in upon light intensities as as in conditions (6Grossman A.R. Schaefer M.R. Chiang G.G. Collier J.L. J. Bacteriol. 1993; 175: 575-582Crossref PubMed Google Scholar). We for the of high light and nitrogen deprivation the in vivo phosphorylation of linker this the of Synechocystis to these conditions for from the other the protein were into membrane and These were with linker proteins and amino residues to the rates of phosphorylation of linker to in Our immunological PBS proteins in the membrane and the with the of which not detected in the We the degradation upon the PBS from the thylakoid The acclimation of cyanobacterial cells to and nitrogen deprivation leads to of PBS rods and degradation of PBS structures (6Grossman A.R. Schaefer M.R. Chiang G.G. Collier J.L. J. Bacteriol. 1993; 175: 575-582Crossref PubMed Google Scholar, 9Duke C.S. Cezeaux A. Allen M.M. J. Bacteriol. 1989; 171: 1960-1966Crossref PubMed Google Scholar, 10Collier J.L. Grossman A.R. J. Bacteriol. 1992; 174: 4718-4726Crossref PubMed Scopus (235) Google Scholar, 11Garnier F. 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In the the phosphoproteins of Synechocystis thylakoid membranes were by The first two are an immunological detection with phosphorylated amino residues and the of a phosphate groups to and threonine The of an in vivo of Synechocystis cells with phosphoproteins be detected using these in the thylakoid membranes of The of phosphoproteins detected by these were and and the detect proteins phosphorylated amino groups that may be whereas with proteins which are the in residues that are The and phosphorylated proteins to be and linker proteins and The with a molecular of detected with a S. E. E. Lett. 1998; PubMed Scopus Google correspond to of the rod linker We not phosphorylation of the major bilin-containing antenna proteins APC and PC, which with a M. A. Molecular of in the of Scholar). which to be associated to PBSs Bryant D.A. 1992; PubMed Scopus Google phosphorylated in antenna The phosphorylation of from higher plant at and threonine residues has been but the function of this process M. M. R. Biochim. Biophys. Acta. PubMed Scopus Google Scholar). The of phosphorylated proteins in and cyanobacterial strains in PBSs or rod linker proteins in these to the linkers in the This that the with to linker The detection of of linker proteins with with their phosphorylation by This that linker phosphorylation at threonine residues is a post-translational the rod linkers were to a dephosphorylation and their dephosphorylation in PBS by not This be by the of linker proteins PC in the of the W. Wiegand G. Huber R. Than M.E. Proc. Natl. Acad. Sci. U. S. A. 1999; 96: 1363-1368Crossref PubMed Scopus (126) Google Scholar, 23Stec B. Troxler R.F. Teeter M.M. Biophys. J. 1999; 76: 2912-2921Abstract Full Text Full Text PDF PubMed Scopus (80) Google Scholar). added have to the linkers within the assembled PBS The of PBSs that were with that or PBSs can be whereas linkers in a assembled PBSs are not we observed that dephosphorylation of linkers in assembled PBSs further their This suggested that dephosphorylation of linkers participate in the the remodeling and turnover of the PBSs in to higher light intensities as as nitrogen deprivation a of the PBS antenna that is in to changes in PBS gene (4Belknap W.R. Haselkorn R. EMBO J. 1987; 6: 871-884Crossref PubMed Scopus (81) Google Scholar, 5de Lorimier R.M. Smith R.L. Stevens Jr., S.E. Plant Physiol. 1991; 98: 1003-1010Crossref Scopus (37) Google and in to proteolytic that some PBS (6Grossman A.R. Schaefer M.R. Chiang G.G. Collier J.L. J. Bacteriol. 1993; 175: 575-582Crossref PubMed Google Scholar, 7Pojidaeva E. Zinchenko V. Shestakov S.V. Sokolenko A. J. Bacteriol. 2004; 186: 3991-3999Crossref PubMed Scopus (19) Google Scholar). In the cleavage of linker proteins under acclimation to higher light with the subsequent of PC rod (7Pojidaeva E. Zinchenko V. Shestakov S.V. Sokolenko A. J. Bacteriol. 2004; 186: 3991-3999Crossref PubMed Scopus (19) Google Scholar). we observed that the rate of linker protein phosphorylation with environmental that disassembly, and degradation of The acclimation of cells for at to high light or nitrogen starvation conditions a in the rate of phosphorylation of the The dephosphorylation of these two as with that be to their degradation rate full This for a of linker dephosphorylation in vivo in PBS Linker dephosphorylation may as a for protein degradation PBS disassembly has whereas protein phosphorylation or the assembly of PBS The steps of biosynthesis include between protein biosynthesis and degradation. The with or can be to degradation in L.K. Toole C.M. Mol. Microbiol. 1998; 30: 467-474Crossref PubMed Scopus (65) Google Scholar). The mechanisms degradation are of the suggested is the binding of proteins that a degradation (8Anderson L.K. Toole C.M. Mol. Microbiol. 1998; 30: 467-474Crossref PubMed Scopus (65) Google Scholar). In that phosphorylation may an in the of linker in the PBS assembly whereas their state be signaling for their degradation. Changes in protein phosphorylation in changes their for proteolytic and assembly The of linker in cyanobacteria be to that of the of the light-harvesting II and the protein in higher plant that are to be to degradation upon dephosphorylation (27Yang D.H. Webster J. Adam Z. Lindahl M. Andersson B. Plant Physiol. 1998; 118: 827-834Crossref PubMed Scopus (106) Google Scholar, A. Andersson B. PubMed Scopus Google Scholar). of acclimation to higher light intensities of at is required for the detection of PBS protein a in the acclimation also observed for light-harvesting of higher (27Yang D.H. Webster J. Adam Z. Lindahl M. Andersson B. Plant Physiol. 1998; 118: 827-834Crossref PubMed Scopus (106) Google Scholar). This for an of some involved in the protein dephosphorylation it has not been clear how PBS structures can be nutrient deprivation or light conditions that a degradation of the cyanobacterial antenna J.L. Grossman A.R. J. Bacteriol. 1992; 174: 4718-4726Crossref PubMed Scopus (235) Google Scholar, G. Glazer A.N. Arch. Microbiol. Scopus Google Scholar, A.R. D. J. Biol. Chem. 2001; Full Text Full Text PDF PubMed Scopus Google Scholar). The major protein family known to be involved in the degradation of PBS is encoded by the nbl gene of the components, is involved in PBS degradation under nutrient deprivation (14Collier J.L. Grossman A.R. EMBO J. 1994; 13: 1039-1047Crossref PubMed Scopus (211) Google Scholar, 16Baier K. Nicklisch S. Grundner C. Reinecke J. Lockau W. FEMS Microbiol. Lett. 2001; 195: 35-39Crossref PubMed Google Scholar, 17Baier K. Lehmann H. Stephan D.P. Lockau W. Microbiology (Read.). 2004; 150: 2739-2749Crossref PubMed Scopus (62) Google Scholar). It is suggested that the binding of NblA to PC can proteins for their further by or can the PBS structure by the between PC It is that and higher to their These and other be by NblA and cyanobacterial We A. R. Grossman for the phycobiliproteins.