Skip to main content
SpringerLink
Log in

Membrane attachment of Slr0006 in Synechocystis sp. PCC 6803 is determined by divalent ions

  • Technical Communication
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

Slr0006 is one of the Synechocystis sp. PCC 6803 proteins strongly induced under carbon limiting conditions. Slr0006 has no predicted transmembrane helices or signal peptide sequence, yet it was exclusively recovered in the membrane fraction of Synechocystis, when the cells were broken in isolation buffers which contain divalent cations and are generally used for photosynthesis studies. Even subsequent washing of the membranes with high salt or various detergents did not release Slr0006, indicating strong binding of the Slr0006 protein to the membranes. Further, DNAse or RNAse treatment did not disturb the tight binding of Slr0006 protein to the membranes. Nevertheless, when the cells were broken in the absence of divalent cations, Slr0006 remained completely soluble. Binding of the Slr0006 to the membrane could not be properly reconstituted if the cations were added after breaking the cells in the absence of divalent ions. This unusual phenomenon has to be considered in identification and localization of other yet uncharacterized cyanobacterial proteins.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

References

  • Andersson B, Anderson JM (1980) Lateral heterogeneity in the distribution of chlorophyll–protein complexes of the thylakoid membranes of spinach chloroplasts. Biochim Biophy Acta 593:427–440

    Article  CAS  Google Scholar 

  • Battchikova N, Vainonen JP, Vorontsova N, Keranen M, Carmel D, Aro EM (2010) Dynamic changes in the proteome of Synechocystis 6803 in response to CO2 limitation revealed by quantitative proteomics. J Proteome Res 9:5896–5912

    Article  PubMed  CAS  Google Scholar 

  • Carmel D, Battchikova N, Holmström M, Mulo P, Aro EM (2010) Knock-out of low CO2-induced slr0006 gene in Synechocystis sp. PCC 6803: consequences on growth and proteome. In: Proceedings of the 15th International Congress on Photosynthesis, Beijing

  • Dühring U, Irrgang KD, Lunser K, Kehr J, Wilde A (2006) Analysis of photosynthetic complexes from a cyanobacterial ycf37 mutant. Biochim Biophys Acta 1757:3–11

    Article  PubMed  Google Scholar 

  • Gombos Z, Wada H, Murata N (1994) The recovery of photosynthesis from low-temperature photoinhibition is accelerated by the unsaturation of membrane lipids: a mechanism of chilling tolerance. PNAS 91:8787–8791

    Article  PubMed  CAS  Google Scholar 

  • Hung CH, Huang JY, Chiu YF, Chu HA (2007) Site-directed mutagenesis on the heme axial-ligands of cytochrome b559 in photosystem II by using cyanobacteria Synechocystis PCC 6803. Biochim Biophys Acta 1767:686–693

    Article  PubMed  CAS  Google Scholar 

  • Klinkert B, Ossenbühl F, Sikorski M, Berry S, Eichacker L, Nickelsen J (2004) PratA, a periplasmic tetratricopeptide repeat protein involved in biogenesis of photosystem II in Synechocystis sp. PCC 6803. J Biol Chem 279:44639–44644

    Article  PubMed  CAS  Google Scholar 

  • Komenda J, Tichy M, Prasil O, Knoppova J, Kuvikova S, de Vries R, Nixon PJ (2007) The exposed N-terminal tail of the D1 subunit is required for rapid D1 degradation during photosystem II repair in Synechocystis sp PCC 6803. Plant Cell 19:2839–2854

    Article  PubMed  CAS  Google Scholar 

  • Kubota H, Sakurai I, Katayama K, Mizusawa N, Ohashi S, Kobayashi M, Zhang P, Aro EM, Wada H (2010) Purification and characterization of photosystem I complex from Synechocystis sp. PCC 6803 by expressing histidine-tagged subunits. Biochim Biophys Acta 1797:98–105

    PubMed  CAS  Google Scholar 

  • Kwon J, Ohb J, Parka C, Chob K, Kimb SI, Kimb S, Leed S, Bhakd J, Norling B, Choib JS (2010) Systematic cyanobacterial membrane proteome analysis by combining acid hydrolysis and digestive enzymes with nano-liquid chromatography–Fourier transform mass spectrometry. J Chromatogr 1217:285–293

    Article  CAS  Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    Article  PubMed  CAS  Google Scholar 

  • Ma W, Mi H (2008) Effect of exogenous glucose on the expression and activity of NADPH dehydrogenase complexes in the cyanobacterium Synechocystis sp. strain PCC 6803. Plant Physiol Biochem 46:775–779

    Article  PubMed  CAS  Google Scholar 

  • Mann NH, Novac N, Mullineaux CW, Newman J, Bailey S, Robinson C (2000) Involvement of an FtsH homologue in the assembly of functional photosystem I in the cyanobacterium Synechocystis sp. PCC 6803. FEBS Lett 479:72–77

    Article  PubMed  CAS  Google Scholar 

  • Norling B (2000) Purification of cyanobacterial thylakoid, plasma, and outer membranes by two-phase partitioning. In: Hatti-Kaul R (ed) Aqueous two-phase systems. methods in biotechnology, vol 11. Humana Press Inc., Totowa, pp 185–192

    Chapter  Google Scholar 

  • Omata T, Murata N (1984) Isolation and characterisation of three types of membranes from cyanobacterium (blue green algae) Synechocystis PCC 6714. Arch Microbiol 139:113–116

    Article  CAS  Google Scholar 

  • Paulsen IT, Sliwinski MK, Saier MH (1998) Microbial genome analyses: global comparisons of transport capabilities based on phylogenies, bioenergetics and substrate specificities. J Mol Biol 277:573–592

    Article  PubMed  CAS  Google Scholar 

  • Rippka R (1988) Isolation and purification of cyanobacteria. Methods Enzymol 167:3–27

    Article  PubMed  CAS  Google Scholar 

  • Riviere ME, Arrio B, Steffan I, Molitor V, Kuntner O, Peschek GA (1990) Changes of some physical properties of isolated and purified plasma and thylakoid membrane vesicles from the freshwater cyanobacterium Synechococcus 6301 (Anacystis nidulans) during adaptation to salinity. Arch Biochem Biophys 280:159–166

    Article  PubMed  CAS  Google Scholar 

  • Rumak I, Gieczewska K, Kierdaszuk B, Gruszecki WI, Mostowska A, Mazur R, Garstka M (2010) 3-D modelling of chloroplast structure under (Mg(2+)) magnesium ion treatment. Relationship between thylakoid membrane arrangement and stacking. Biochim Biophys Acta 1797:1736–1748

    Article  PubMed  CAS  Google Scholar 

  • Speers AE, Wu CC (2007) Chem Rev 107:3687–3714

    Article  PubMed  CAS  Google Scholar 

  • Staehelin LA (2003) Chloroplast structure: from chlorophyll granules to supra-molecular architecture of thylakoid membranes. Photosynth Res 76:185–196

    Article  PubMed  CAS  Google Scholar 

  • van Thor JJ, Jeanjean R, Havaux M, Sjollema KA, Joset F, Hellingwerf KJ, Matthijs HC (2000) Salt shock-inducible photosystem I cyclic electron transfer in Synechocystis PCC6803 relies on binding of ferredoxin:NADP+ reductase to the thylakoid membranes via its CpcD phycobilisome-linker homologous N-terminal domain. Biochim Biophys Acta 1457:129–144

    Article  PubMed  Google Scholar 

  • Zhang P, Battchikova N, Jansen T, Appel J, Ogawa T, Aro EM (2004) Expression and functional roles of the two distinct NDH-1 complexes and the carbon acquisition complex NdhD3/NdhF3/CupA/Sll1735 in Synechocystis sp PCC 6803. Plant Cell 16:3326–3340

    Article  PubMed  CAS  Google Scholar 

  • Zhang P, Allahverdiyeva Y, Eisenhut M, Aro EM (2009) Flavodiiron proteins in oxygenic photosynthetic organisms: photoprotection of photosystem II by Flv2, Flv4 in Synechocystis sp. PCC 6803. PLoS ONE 4:e5331

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This study was financially supported by the Academy of Finland (Grants nos. 118637 and 130075) and the grant from the Maj and Tor Nessling Foundation. Maija Holmström MSc is thanked for technical assistance, and Dr Sari Sirpiö and Dr Saijaliisa Kangasjärvi for helpful discussions.

Author information

Authors and Affiliations

  1. Laboratory of Molecular Plant Biology, Department of Biochemistry and Food Chemistry, University of Turku, Tykistökatu 6A, Biocity 6th Floor, 20520, Turku, Finland

    Dalton Carmel, Paula Mulo, Natalia Battchikova & Eva-Mari Aro

Authors
  1. Dalton Carmel
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Paula Mulo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Natalia Battchikova
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Eva-Mari Aro
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Eva-Mari Aro.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Carmel, D., Mulo, P., Battchikova, N. et al. Membrane attachment of Slr0006 in Synechocystis sp. PCC 6803 is determined by divalent ions. Photosynth Res 108, 241–245 (2011). https://doi.org/10.1007/s11120-011-9662-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-011-9662-0

Keywords

Search

Navigation