Cyanobacteria acclimate to high-light conditions by adjusting photosystem stoichiometry through a decrease of photosystem I (PSI) abundance in thylakoid membranes. As PSI complexes bind the majority of chlorophyll (Chl) in cyanobacterial cells, it is accepted that the mechanism controlling PSI level/synthesis is tightly associated with the Chl biosynthetic pathway. However, how Chl is distributed to photosystems under different light conditions remains unknown. Using radioactive labeling by (35)S and by (14)C combined with native/two-dimensional electrophoresis, we assessed the synthesis and accumulation of photosynthetic complexes in parallel with the synthesis of Chl in Synechocystis sp. PCC 6803 cells acclimated to different light intensities. Although cells acclimated to higher irradiances (150 and 300 μE m(-2)s(-1)) exhibited markedly reduced PSI content when compared with cells grown at lower irradiances (10 and 40 μE m(-2) s(-1)), they grew much faster and synthesized significantly more Chl, as well as both photosystems. Interestingly, even under high irradiance, almost all labeled de novo Chl was localized in the trimeric PSI, whereas only a weak Chl labeling in photosystem II (PSII) was accompanied by the intensive (35)S protein labeling, which was much stronger than in PSI. These results suggest that PSII subunits are mostly synthesized using recycled Chl molecules previously released during PSII repair-driven protein degradation. In contrast, most of the fresh Chl is utilized for synthesis of PSI complexes likely to maintain a constant level of PSI during cell proliferation.

Institute of Microbiology Department of Phototrophic Microorganisms Academy of Sciences 37981 Trebon Czech Republic

Zobrazit více v PubMed

Anderson JM, Chow WS, Park YI. (1995) The grand design of photosynthesis: Acclimation of the photosynthetic apparatus to environmental cues. Photosynth Res 46: 129–139 PubMed

Beisel KG, Jahnke S, Hofmann D, Köppchen S, Schurr U, Matsubara S. (2010) Continuous turnover of carotenes and chlorophyll a in mature leaves of Arabidopsis revealed by 14CO2 pulse-chase labeling. Plant Physiol 152: 2188–2199 PubMed PMC

Chow WS, Melis A, Anderson JM. (1990) Adjustments of photosystem stoichiometry in chloroplasts improve the quantum efficiency of photosynthesis. Proc Natl Acad Sci USA 87: 7502–7506 PubMed PMC

Czarnecki O, Grimm B. (2012) Post-translational control of tetrapyrrole biosynthesis in plants, algae, and cyanobacteria. J Exp Bot 63: 1675–1687 PubMed

Demmig-Adams B, Adams WW. (1992) Photoprotection and other responses of plants to high light stress. Annu Rev Plant Physiol Plant Mol Biol 43: 599–626

Eichacker LA, Helfrich M, Rüdiger W, Müller B. (1996) Stabilization of chlorophyll a-binding apoproteins P700, CP47, CP43, D2, and D1 by chlorophyll a or Zn-pheophytin a. J Biol Chem 271: 32174–32179 PubMed

El Bissati K, Delphin E, Murata N, Etienne AL, Kirilovsky D. (2000) Photosystem II fluorescence quenching in the cyanobacterium Synechocystis PCC 6803: involvement of two different mechanisms. Biochim Biophys Acta 1457: 229–242 PubMed

Feierabend J, Dehne S. (1996) Fate of the porphyrin cofactors during the light-dependent turnover of catalase and of the photosystem II reaction-center protein D1 in mature rye leaves. Planta 198: 413–422

Fujimori T, Higuchi M, Sato H, Aiba H, Muramatsu M, Hihara Y, Sonoike K. (2005) The mutant of sll1961, which encodes a putative transcriptional regulator, has a defect in regulation of photosystem stoichiometry in the cyanobacterium Synechocystis sp. PCC 6803. Plant Physiol 139: 408–416 PubMed PMC

Fujita Y, Murakami A, Ohki K. (1990) Regulation of the stoichiometry of thylakoid components in the photosynthetic system of cyanophytes: Model experiments showing that control of the synthesis or supply of Chl a can change the stoichiometric relationship between the two photosystems. Plant Cell Physiol 31: 145–153

He Q, Dolganov N, Bjorkman O, Grossman AR. (2001) The high light-inducible polypeptides in Synechocystis PCC6803. Expression and function in high light. J Biol Chem 276: 306–314 PubMed

Herranen M, Tyystjärvi T, Aro EM. (2005) Regulation of photosystem I reaction center genes in Synechocystis sp. strain PCC 6803 during light acclimation. Plant Cell Physiol 46: 1484–1493 PubMed

Hihara Y, Kamei A, Kanehisa M, Kaplan A, Ikeuchi M. (2001) DNA microarray analysis of cyanobacterial gene expression during acclimation to high light. Plant Cell 13: 793–806 PubMed PMC

Hihara Y, Sonoike K, Ikeuchi M. (1998) A novel gene, pmgA, specifically regulates photosystem stoichiometry in the cyanobacterium Synechocystis species PCC 6803 in response to high light. Plant Physiol 117: 1205–1216 PubMed PMC

Jordan P, Fromme P, Witt HT, Klukas O, Saenger W, Krauss N. (2001) Three-dimensional structure of cyanobacterial photosystem I at 2.5 A resolution. Nature 411: 909–917 PubMed

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 PubMed

Melis A, Murakami A, Nemson JA, Aizawa K, Ohki K, Fujita Y. (1996) Chromatic regulation in Chlamydomonas reinhardtii alters photosystem stoichiometry and improves the quantum efficiency of photosynthesis. Photosynth Res 47: 253–265 PubMed

Miskiewicz E, Ivanov AG, Huner NPA. (2002) Stoichiometry of the photosynthetic apparatus and phycobilisome structure of the cyanobacterium Plectonema boryanum UTEX 485 are regulated by both light and temperature. Plant Physiol 130: 1414–1425 PubMed PMC

Müller P, Li XP, Niyogi KK. (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiol 125: 1558–1566 PubMed PMC

Mullineaux CW, Emlyn-Jones D. (2005) State transitions: an example of acclimation to low-light stress. J Exp Bot 56: 389–393 PubMed

Murakami A, Fujita Y. (1991) Regulation of photosystem stoichiometry in the photosynthetic system of the cyanophyte Synechocystis PCC 6714 in response to light-intensity. Plant Cell Physiol 32: 223–230 PubMed

Murakami A, Fujita Y. (1993) Regulation of stoichiometry between PSI and PSII in response to light regime for photosynthesis observed with Synechocystis PCC 6714: relationship between redox state of Cyt b6-f complex and regulation of PSI formation. Plant Cell Physiol 34: 1175–1180

Murakami A, Kim SJ, Fujita Y. (1997) Changes in photosystem stoichiometry in response to environmental conditions for cell growth observed with the cyanophyte Synechocystis PCC 6714. Plant Cell Physiol 38: 392–397 PubMed

Muramatsu M, Hihara Y. (2012) Acclimation to high-light conditions in cyanobacteria: from gene expression to physiological responses. J Plant Res 125: 11–39 PubMed

Muramatsu M, Sonoike K, Hihara Y. (2009) Mechanism of downregulation of photosystem I content under high-light conditions in the cyanobacterium Synechocystis sp. PCC 6803. Microbiology 155: 989–996 PubMed

Neale PJ, Melis A. (1986) Algal photosynthetic membrane complexes and the photosynthesis-irradiance curve: a comparison of light-adaptation responses in Chlamydomonas reinhardtii (Chlorophyta). J Phycol 22: 531–538

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

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 PubMed PMC

Porra RJ, Thompson WA, Kriedmann PE. (1989) 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 975: 384–394

Rippka R, Deruelles J, Waterbury JB, Herdman M, Stanier RY. (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111: 1–61

Shen G, Boussiba S, Vermaas WFJ. (1993) Synechocystis sp PCC 6803 strains lacking photosystem I and phycobilisome function. Plant Cell 5: 1853–1863 PubMed PMC

Shpilyov AV, Zinchenko VV, Shestakov SV, Grimm B, Lokstein H. (2005) Inactivation of the geranylgeranyl reductase (ChlP) gene in the cyanobacterium Synechocystis sp. PCC 6803. Biochim Biophys Acta 1706: 195–203 PubMed

Sobotka R, Dühring U, Komenda J, Peter E, Gardian Z, Tichý M, Grimm B, Wilde A. (2008) Importance of the cyanobacterial Gun4 protein for chlorophyll metabolism and assembly of photosynthetic complexes. J Biol Chem 283: 25794–25802 PubMed PMC

Sobotka R, Tichý M, Wilde A, Hunter CN. (2011) Functional assignments for the carboxyl-terminal domains of the ferrochelatase from Synechocystis PCC 6803: the CAB domain plays a regulatory role, and region II is essential for catalysis. Plant Physiol 155: 1735–1747 PubMed PMC

Sonoike K, Hihara Y, Ikeuchi M. (2001) Physiological significance of the regulation of photosystem stoichiometry upon high light acclimation of Synechocystis sp. PCC 6803. Plant Cell Physiol 42: 379–384 PubMed

Tanaka R, Rothbart M, Oka S, Takabayashi A, Takahashi K, Shibata M, Myouga F, Motohashi R, Shinozaki K, Grimm B, et al. (2010) LIL3, a light-harvesting-like protein, plays an essential role in chlorophyll and tocopherol biosynthesis. Proc Natl Acad Sci USA 107: 16721–16725 PubMed PMC

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: 55–60 PubMed

Vavilin D, Brune DC, Vermaas WFJ. (2005) 15N-labeling to determine chlorophyll synthesis and degradation in Synechocystis sp. PCC 6803 strains lacking one or both photosystems. Biochim Biophys Acta 1708: 91–101 PubMed

Vavilin D, Vermaas WFJ. (2007) Continuous chlorophyll degradation accompanied by chlorophyllide and phytol reutilization for chlorophyll synthesis in Synechocystis sp. PCC 6803. Biochim Biophys Acta 1767: 920–929 PubMed

Vavilin D, Yao D, Vermaas WFJ. (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: 37660–37668 PubMed

Wallner T, Hagiwara Y, Bernát G, Sobotka R, Reijerse EJ, Frankenberg-Dinkel N, Wilde A. (2012) Inactivation of the conserved open reading frame ycf34 of Synechocystis sp. PCC 6803 interferes with the photosynthetic electron transport chain. Biochim Biophys Acta 1817: 2016–2026 PubMed

Walters RG. (2005) Towards an understanding of photosynthetic acclimation. J Exp Bot 56: 435–447 PubMed

Walters RG, Horton P. (1994) Acclimation of Arabidopsis thaliana to the light environment: changes in composition of the photosynthetic apparatus. Planta 195: 248–256 PubMed

Williams JGK. (1988) Construction of specific mutations in photosystem II photosynthetic reaction center by genetic engineering methods in Synechocystis 6803. Methods Enzymol 167: 766–778

Wittig I, Schägger H. (2008) Features and applications of blue-native and clear-native electrophoresis. Proteomics 8: 3974–3990 PubMed

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: 149–160 PubMed

Xu H, Vavilin D, Funk C, Vermaas W. (2004) Multiple deletions of small Cab-like proteins in the cyanobacterium Synechocystis sp. PCC 6803: consequences for pigment biosynthesis and accumulation. J Biol Chem 279: 27971–27979 PubMed

Yao DC, Brune DC, Vavilin D, Vermaas WF. (2012a) Photosystem II component lifetimes in the cyanobacterium Synechocystis sp. strain PCC 6803: small Cab-like proteins stabilize biosynthesis intermediates and affect early steps in chlorophyll synthesis. J Biol Chem 287: 682–692 PubMed PMC

Yao DC, Brune DC, Vermaas WF. (2012b) Lifetimes of photosystem I and II proteins in the cyanobacterium Synechocystis sp. PCC 6803. FEBS Lett 586: 169–173 PubMed

The biogenesis and maintenance of PSII: Recent advances and current challenges

The Role of FtsH Complexes in the Response to Abiotic Stress in Cyanobacteria

FtsH4 protease controls biogenesis of the PSII complex by dual regulation of high light-inducible proteins

Assembly of D1/D2 complexes of photosystem II: Binding of pigments and a network of auxiliary proteins

Psb34 protein modulates binding of high-light-inducible proteins to CP47-containing photosystem II assembly intermediates in the cyanobacterium Synechocystis sp. PCC 6803

Plant LHC-like proteins show robust folding and static non-photochemical quenching

Gradual Response of Cyanobacterial Thylakoids to Acute High-Light Stress-Importance of Carotenoid Accumulation

Photomorphogenesis in the Picocyanobacterium Cyanobium gracile Includes Increased Phycobilisome Abundance Under Blue Light, Phycobilisome Decoupling Under Near Far-Red Light, and Wavelength-Specific Photoprotective Strategies

Evolution of Ycf54-independent chlorophyll biosynthesis in cyanobacteria

Reconstruction of the absorption spectrum of Synechocystis sp. PCC 6803 optical mutants from the in vivo signature of individual pigments

Plasticity of Cyanobacterial Thylakoid Microdomains Under Variable Light Conditions

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

Ycf48 involved in the biogenesis of the oxygen-evolving photosystem II complex is a seven-bladed beta-propeller protein

Binding of pigments to the cyanobacterial high-light-inducible protein HliC

The Ribosome-Bound Protein Pam68 Promotes Insertion of Chlorophyll into the CP47 Subunit of Photosystem II

Strain of Synechocystis PCC 6803 with Aberrant Assembly of Photosystem II Contains Tandem Duplication of a Large Chromosomal Region

Porphyrin Binding to Gun4 Protein, Facilitated by a Flexible Loop, Controls Metabolite Flow through the Chlorophyll Biosynthetic Pathway

Lack of Phosphatidylglycerol Inhibits Chlorophyll Biosynthesis at Multiple Sites and Limits Chlorophyllide Reutilization in Synechocystis sp. Strain PCC 6803

Presence of state transitions in the cryptophyte alga Guillardia theta

Discovery of a chlorophyll binding protein complex involved in the early steps of photosystem II assembly in Synechocystis