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Evidence for the existence of trimeric and monomeric Photosystem I complexes in thylakoid membranes from cyanobacteria

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Abstract

In cyanobacteria, solubilization of thylakoid membranes by detergents yields both monomeric and trimeric Photosystem I (PS I) complexes in variable amounts. We present evidence for the existence of both monomeric and trimeric PS I in cyanobacterial thylakoid membranes with the oligomeric state depending ‘in vitro’ on the ion concentration. At low salt concentrations (i.e.≤10 mM MgSO4) PS I is mainly extracted as a trimer from these membranes and at high salt concentrations (i.e.≥150 mM MgSO4) nearly exclusively as a monomer, irrespective of the type of salt used (i.e. mono- or bivalent ions) and the temperature (i.e. 4°C or 20°C). Once solubilized, the PS I trimer is stable over a wide range of ion concentrations (i.e. beyond 0.5 M). A model is presented which suggests a monomer-oligomer equilibrium of PS I, but also of PS II and the cyt. b6/f-complex in the cyanobacterial thylakoid membrane. The possible physiological role of this equilibrium in the regulation of state transitions is discussed.

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Abbreviations

β-DM:

dodecyl-β-D-maltoside

Chl:

chlorophyll

cyt. b6f :

cytochrome b6f complex

EM:

electron microscopy

HPLC:

high performance liquid chromatography

LDAO:

N, N-dimethyl-N-dodecyl amine oxide

MES:

4-morpholino ethane sulfonic acid

PAGE:

polyacrylamide gel electrophoresis

PBS:

phycobilisome

PS:

photosystem

SDS:

sodium dodecyl sulfate

2D:

two dimensional

3D:

three dimensional

References

  • Allen JF, Sanders CE and Holmes NG (1985) Correlation of membrane protein phosphorylation with excitation energy distribution in the cyanobacterium Synechococcus 6301. FEBS Lett 193: 271–275

    Article  Google Scholar 

  • Allen JF (1992) Protein phosphorylation in regulation of photosynthesis. Biochim Biophys Acta 1098: 275–335

    PubMed  Google Scholar 

  • Almog O, Shoham G, Michaeli D and Nechushtai R (1991) Monomeric and trimeric forms of the Photosystem I reaction center of Mastigocladus laminosus: Crystallisation and preliminary characterization. Proc Natl Acad Sci USA 88: 5312–5316

    PubMed  Google Scholar 

  • Almog O, Shoham G and Nechushtal R (1992) Photosystem I: Composition, organization and structure. In: Barber J (ed) The Photosystems: Structure, Function and Molecular Biology Topics in Photosynthesis, Vol 11, pp 443–469 Elsevier, Amsterdam

    Google Scholar 

  • Arnon DI (1949) Copper enzymes in isolated chloroplasts: Polyphenoloxidase in Beta vulgaris. Plant Physiol 24: 1–15

    Google Scholar 

  • Bald D, Kruip J, Boekema EJ and Rögner M (1992) Structural investigations on Cyt.b6/f-complex and PS I-complex from the cyanobacterium Synechocystis PCC 6803. In: Murata N, (ed) Research in Photosynthesis, Vol I, pp 629–632. Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Boekema EJ, Dekker JP, van Heel MG, Rögner M, Saenger W, Witt I and Witt HT (1987) Evidence for a trimeric organization of the Photosystem I complex from the thermophilic cyanobacterium Synechococcus sp. FEBS Lett 217: 283–286

    Article  Google Scholar 

  • Boekema EJ, Boonstra AF, Dekker JP and Rögner M (1994) Electron microscopic structural analysis of Photosystem I, Photosystem II and the cytochrome b/6f complex from green plants and cyanobacteria. J Bioenerg Biomem 26: 17–29

    Google Scholar 

  • Böttcher B, Gräber P and Boekema EJ (1992) The structure of Photosystem I from the thermophilic cyanobacterium Synechococcus sp.determined by electron microscopy of two-dimensional crystals. Biochim Biophys Acta 1098: 131–143

    PubMed  Google Scholar 

  • Chitnis VP, Xu Q, Yu L, Golbeck JH, Nakamoto H, Xie D-L and Chitnis PR (1993a) Targeted inactivation of the gene psaL encoding a subunit of Photosystem I of the cyanobacterium Synechocystis sp. PCC 6803. J Biol Chem 268: 11678–11684

    PubMed  Google Scholar 

  • Chitnis VP and Chitnis PR (1993b) PsaL subunit is required for the formation of Photosystem I trimers in the cyanobacterium Synechocystis sp. PCC 6803. FEBS Lett 336: 330–334

    Article  PubMed  Google Scholar 

  • Cramer WA, Everly RM, Furbacher PN, Huang D, Tae G-S, Szczepaniak A, Cherepanov DA and Krishtalik LI (1992) Structure-function-assembly of the cytochrome complexes in oxygenic photosynthesis. In: Murata N (ed) Research in Photosynthesis, Vol II, pp 447–454. Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Dekker JP, Boekema EJ, Witt HT and Rögner M (1988) Refined purification and further characterization of oxygen-evolving and tris-treated Photosystem II particles from the thermophilic cyanobacterium Synechococcus sp. Biochim Biophys Acta 936: 307–318

    Google Scholar 

  • Ford RC, and Holzenburg A (1988) Investigation of the structure of the Photosystem I reaction center. EMBO J 7: 2287–2293.

    Google Scholar 

  • Ford RC, Picot D and Garavito RM (1987) Crystallization of Photosystem I reaction center. EMBO J 6, 1581–1586

    Google Scholar 

  • Fork DC and Herbert SK (1993) Electron transport and photophosphorylation by Photosystem I in vivo in plants and cyanobacteria. Photosynth Res 36: 149–168

    Google Scholar 

  • Golbeck JH and Bryant DA (1991) Photosystem I. Curr Top Bioenerg 16: 83–177

    Google Scholar 

  • Hefti A, Ford RC, Miller M, Cox RP and Engel A (1992) Analysis of the structure of Photosystem I in cyanobacterial thylakoid membranes. FEBS Lett 296: 29–32

    Article  PubMed  Google Scholar 

  • Hladik J and Sofrova D (1991) Does the trimeric form of Photosystem I reaction center of cyanobacteria in vivo exist. Photosynth Res 29: 171–175

    Google Scholar 

  • Hladik J, Pospisilova L and Sofrova D (1990) Topograhy of Photosystem I in cyanobacteria. Baltscheffsky M (ed) Current Research in Photosynthesis, Vol II. pp 579–582

  • Krauß N, Hinrichs W, Witt I, Fromme P, Pritzkow W, Dauter Z, Betzel C, Wilson KS, Witt HT and Saenger W (1993) Three-dimensional structure of system I of photosynthesis at 6 Å resolution. Nature 361: 326–331

    Article  Google Scholar 

  • Krulp J, Boekema EI, Baid D, Boonstra AI and Bögner M (1992) Isolation and structural characterization of monomeric and trimeric Photosystem I complexes (P700-F A/F B and P700-F X ) from the cyanobacterium Synechocystis PCC 6803. J Biol Chem 268: 23353–23360

    Google Scholar 

  • Mörschel E and Schatz GH (1987) Correlation of Photosystem II complexes with exoplasmatic freeze-fracture particles of thylakoids of the cyanobacterium Synechococcus sp. Planta 172: 145–154

    Google Scholar 

  • Mullineaux CW (1992) Excitation energy transfer from phycobilisomes to Photosystem I and Photosystem II in a cyanobacterium. In: Murata N, (ed) Research in Photosynthesis, Vol I. pp 141–144, Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Mullineaux CW and Holzwarth AR (1991) Kinetics of excitation energy transfer in the cyanobacterial phycobilisome-photosystem II complex. Biochim Biophys Acta 1098: 68–78

    Google Scholar 

  • Nußberger S, Dörr K, Wand DN and Kühlbrandt W 1993 Lipid-protein interactions in crystals of plant light-harvesting complex. J Mol Biol. 232 (in press)

  • Olive J, M'Bina I, Vernotte C, Astier C and Wollman FA (1986) Randomization of the EF particles in thylakoid membranes of Synechocystis 6714 upon transition from state I to state II. FEBS Lett 208: 308–312

    Article  Google Scholar 

  • Reed RH, Warr SRC, Richardson DL, Moore DJ and Stewart WDP (1985) Multiphasic osmotic adjustment in a euryhaline cyanobacterium. FEMS Microbiol Lett 28: 225–229

    Article  Google Scholar 

  • Richardson DL, Reed RH and Stewart WDP (1984) Glucosylglycerol accumulation in Synechocystis PCC 6803 in response to osmotic stress. Br Phycol J 18: 209

    Google Scholar 

  • Rögner M, Dekker JP, Boekema EJ and 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 

  • Rögner M, Mühlenhoff U, Boekema EJ and Witt HT (1990a) Mono-, di- and trimeric PS I reaction center complexes isolated from the thermophilic cyanobacterium Synechococcus sp. Size, shape and activity. Biochim Biophys Acta 1015: 415–424

    Google Scholar 

  • Rögner M, Nixon PJ and Diner B (1990b) Purification and characterization of Photosystem I and Photosystem II core complexes from wild-type and phycocyanin-deficient strains of the cyanobacterium Synechocystis PCC 6803. J Biol Chem 265: 6189–6196

    PubMed  Google Scholar 

  • Sprague SG, Camm EL, Green BR and Staehelin LA (1985) Reconstitution of light-harvesting complexes and Photosystem II cores into galactolipid and phospholipid liposomes. J Cell Biol 100: 552–557

    Article  PubMed  Google Scholar 

  • Van der Lee J, Bald D, Kwa SLS, van Grondelle R, Rögner M and Dekker JP (1993) Steady-state polarized light spectroscopy of isolated Photosystem I complexes. Photosynth Res 35: 311–321

    Article  Google Scholar 

  • Van der Staay GWM, Boekema EJ, Dekker JP and Matthys HCP (1993) Characterization of trimeric Photosystem I particles from the prochlorophyte Prochlorothrix hollandica by electron microscopy and image analysis. Biochim Biophys Acta 1142:189–193

    Google Scholar 

  • Vernotte C, Astier C and Olive J (1990) State 1-state 2 adaptation in the cyanobacteria Synechocystis PCC 6714 wild type and Synechocystis PCC 6803 wild type and phycocyanin-less mutant. Photosynth Res 26: 203–212

    Google Scholar 

  • Witt I, Witt HT, Gerken S, Saenger W, Dekker JP and Rögner M (1987) Crystallisation of reaction center I of photosynthesis. Low-concentration crystallization of photoactive protein complexes from the cyanobacterium Synechococcus sp. FEBS Lett 221: 260–264

    Article  Google Scholar 

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Authors and Affiliations

  1. Institute of Botany, University of Münster, Schlossgarten 3, D-48149, Münster, Germany

    Jochen Kruip, Dirk Bald & Matthias Rögner

  2. Bioson Research Institute, Biophysical Chemistry, University of Groningen, Nijenborgh 4, 9747 AG, Groningen, The Netherlands

    Egbert Boekema

Authors
  1. Jochen Kruip
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  2. Dirk Bald
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  3. Egbert Boekema
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  4. Matthias Rögner
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Kruip, J., Bald, D., Boekema, E. et al. Evidence for the existence of trimeric and monomeric Photosystem I complexes in thylakoid membranes from cyanobacteria. Photosynth Res 40, 279–286 (1994). https://doi.org/10.1007/BF00034777

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  • DOI: https://doi.org/10.1007/BF00034777

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