Skip to main content
Log in

Differential distribution of pigment-protein complexes in the Thylakoid membranes of Synechocystis 6803

  • Published:
Journal of Bioenergetics and Biomembranes Aims and scope Submit manuscript

Abstract

Thylakoids in Synechocystis 6803, though apparently uniform in appearance in ultrastructure, were found to consist of segments which were functionally dissimilar and had distinct proteomes. These thylakoid segments can be isolated from Synechocystis 6803 by successive ultracentrifugation of cell free extracts at 40,000×g (40 k segments), 90,000×g (90 k segments) and 150,000×g (150 k segments). Electron microscopy showed differences in their appearance. 40 k segments looked feathery and fluffy, whereas the 90 k and 150 k thylakoid membrane segments appeared tiny and less fluffy. The absorption spectra showed heterogeneous distribution of pigment-protein complexes in the three types of segments. The photochemical activities of Photosystem I (PSI) and Photosystem II (PSII) showed unequal distributions in 40 k, 90 k and 150 k segments which were substantiated with low temperature fluorescence measurements. The ratio of PSII/PSI fluorescence emission at 77 K (λex = 435 nm) was highest in 150 k segments indicating higher PSII per unit PSI in these segments. The chlorophyll fluorescence lifetimes in the membranes, determined with a time-correlated single-photon counting technique, could be resolved in three components: τ1= <40 ps, τ2= 425–900 ps and τ3= 2.4–3.2 ns. The percentage contribution of the fastest component (τ1) decreased in the order 40 k > 90 k > 150 k segments whereas that of the other two components showed a reversed trend. These studies indicated differential distribution of pigment-protein complexes in the three membrane segments suggesting heterogeneity in the thylakoids of Synechocystis 6803.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Agarwal R, Ortleb S, Sainis JK, Melzer M (2009) Immunoelectron microscopy for locating Calvin cycle enzymes in the thylakoids of Synechocystis 6803. Mol Plant 2(1):32–42

    Article  CAS  Google Scholar 

  • Agarwal R, Matros A, Melzer M, Mock HP, Sainis JK (2010) Heterogeneity in thylakoid membrane proteome of Synechocystis 6803. J Proteomics 73:976–991

    Article  CAS  Google Scholar 

  • Anderson JM, Aro EM (1994) Grana stacking and protection of photosystem II in thylakoid membranes of higher plant leaves under sustained irradiance: a hypothesis. Photosynth Res 41:315–326

    Article  CAS  Google Scholar 

  • Andreasson E, Svensson P, Weibull C, Albertsson P (1988) Separation and characterization of stroma and grana membranes-evidence for heterogeneity in antenna size of both Photosystem I and Photosystem II. Biochim Biophys Acta 936:339–350

    Article  CAS  Google Scholar 

  • Armond PA, Arntzen CJ (1977) Localization and characterization of photosystem II in grana and stroma lamellae. Plant Physiol 59:398–404

    Article  CAS  Google Scholar 

  • Bennett A, Bogorad L (1973) Complementary chromatic adaptation in a filamentous blue green alga. J Cell Biol 58:419–435

    Article  CAS  Google Scholar 

  • Bryant DA, Guglielmi G, Tandeau MN, Castets AM, Cohen-Bazire G (1979) The structure of cyanobacterial phycobilisome: a model. Arch Microbiol 123(2):113–127

    Article  CAS  Google Scholar 

  • Dani DN, Sainis JK (2005) Isolation and characterization of a thylakoid membrane module showing partial light and dark reactions. Biochim Biophys Acta 1669:43–52

    Article  CAS  Google Scholar 

  • Fuhrmann E, Gathmann S, Rupprecht E, Golecki J, Schneider D (2009) Thylakoid membrane reduction affects the photosystem stoichiometry in the cyaobacteriun Synechocystis sp. PCC 6803. Plant Physiol 149:735–744

    Article  CAS  Google Scholar 

  • Hill R, Bendall F (1960) Function of the two Cytochrome components in chloroplasts: a working hypothesis. Nature 186:136–137

    Article  CAS  Google Scholar 

  • Holzwarth AR (1990) The functional organization of the antenna systems in higher plants and green algae as studied by time-resolved fluorescence techniques. In: Baltscheffsky M (ed) Current research in photosynthesis, Vol 2. Kluwer, Dordrecht, pp 223–230

    Google Scholar 

  • Karukstis KK, Sauer K (1983) Fluorescence decay kinetics of chlorophyll in photosynthetic membranes. J Cell Biochem 23:131–158

    Article  CAS  Google Scholar 

  • Katoh T, Gantt E (1979) Photosynthetic vesicles with bound phycobilisomes from Anabaena variabilis. Biochim Biophys Acta 546:383–393

    Article  CAS  Google Scholar 

  • Keuper HJK, Sauer K (1989) Effect of photosystem II reaction center closure on nanosecond fluorescence relaxation kinetics. Photosynth Res 20:85–103

    Article  CAS  Google Scholar 

  • Kumazaki S, Hasegawa M, Ghoneim M, Shimizu Y, Okamoto K, Nishiyama M, Ohoka H, Terazima M (2007) A line-scanning semi confocal multi-photon fluorescence microscope with a simultaneous broadband spectral acquisition and its application to the study of the thylakoid membrane of a cyanobacteriun Anabaena PCC 7120. J Microscopy 228(2):240–254

    Article  CAS  Google Scholar 

  • Lakowicz JR (2006) Principles of fluorescence spectroscopy, 3rd edn. Springer, New York

    Book  Google Scholar 

  • Li Y, Zhang J, Xie J, Zhao J, Jiang L (2001) Temperature-induced decoupling of phycobilisomes from reaction centers. Biochim Biophys Acta 1504:229–234

    Article  CAS  Google Scholar 

  • Magde D, Berens SJ, Butler WL (1982) Picosecond fluorescence in spinach chlorolasts. Proc Soc Photo-Opt Instrum Eng 322:80–86

    CAS  Google Scholar 

  • McCauley SW, Biltersmann E, Mueller M, Holzwarth AR (1990) Picosecond chlorophyll fluorescence from higher plants. In: Baltscheffsky M (ed) Current research in photosynthesis, Vol. 2. Kluwer, Dordrecht, pp 297–300

    Google Scholar 

  • Mullineaux CW (2008) Phycobilisome-reaction centre interaction in cyanobacteria. Photosynth Res 95:175–182

    Article  CAS  Google Scholar 

  • Murata N, Sato N, Omata T, Kuwabara T (1981) Separation and characterization of thylakoid and cell envelope of the blue-green alga (cyanobacterium) Anacystis nidulans. Plant Cell Physiol 22:855–866

    CAS  Google Scholar 

  • Nishiyama Y, Allakhverdiev SI, Murata NI (2005) Inhibition of the repair of Photosystem II by oxidative stress in cyanobacteria. Photosynth Res 84:1–7

    Article  CAS  Google Scholar 

  • Rexroth S, Mullineaux CW, Ellinger D, Sendtko E, Rögner M, Koenig F (2011) The plasma membrane of the cyanobacterium Gloeobacter violaceus contains segregated bioenergetic domains. Plant Cell 23:2379–2390

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Santhose I, Gnanadoss J, Ramganesh S, Elumalai S (2011) Enhanced carotenoid synthesis of Phormidium sp. in stressed conditions. J Exp Sci 2(3):38–44

    CAS  Google Scholar 

  • Sherman DM, Troyan TA, Sherman LA (1994) Localisation of membrane proteins in the cyanobacterium Synechococcus 7942: radial asymmetry in the photosynthetic complexes. Plant Physiol 138:1577–1585

    Google Scholar 

  • Staehelin LA, Arntzen CJ (1983) Regulation of chloroplast membrane function: protein phosphorylation changes the spatial organization of membrane components. J Cell Biol 97:1327–1337

    Article  CAS  Google Scholar 

  • Takahashi T, Inoue-Kashino N, Ozawa SI, Takahashi Y, Kashino Y, Satoh K (2009) Photosystem II complex in vivo is a monomer. J Biol Chem 284(23):15598–15606

    Article  CAS  Google Scholar 

  • Tandeau de Marsac N, Houmard J (1988) Complementary chromatic adaptation: physiological conditions and action spectra. In: Packer L, Glazer AN (eds) Methods in enzymology: cyanobacteria, Vol 167. Academic Press Inc, San Diego, pp 318–328

    Google Scholar 

  • Trissl HW, Wilhelm C (1993) Why do thylakoid membranes from higher plants form grana stacks? Trends Biochem Sci 18(11):415–419

    Article  CAS  Google Scholar 

  • Vermaas WFJ, Timlin JA, Jones HDT, Sinclair MB, Lieman LT, Hamad SW, Melgaard DK, Haaland DM (2008) In vivo hyperspectral confocal fluorescence imaging to determine pigment localization and distribution in cyanobacterial cells. Proc Natl Acad Sci, (USA) 105(10):4050–4055

    Article  CAS  Google Scholar 

  • Watanabe M, Iwai M, Narikawa R, Ikeuchi M (2009) Is the photosystem II complex a monomer or a dimer? Plant Cell Physiol 50(9):1674–1680

    Article  CAS  Google Scholar 

  • Wollman FA, Minai L, Nechushtai R (1999) The biogenesis and assembly of photosynthetic proteins in thylakoid membranes. Biochim Biophys Acta 1411:21–85

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jayashree Krishna Sainis.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM Fig. 1

(PDF 110 kb)

ESM Fig. 2

(PDF 64 kb)

ESM Fig. 3

(PDF 41 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Agarwal, R., Maralihalli, G., Sudarsan, V. et al. Differential distribution of pigment-protein complexes in the Thylakoid membranes of Synechocystis 6803. J Bioenerg Biomembr 44, 399–409 (2012). https://doi.org/10.1007/s10863-012-9437-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10863-012-9437-0

Keywords

Navigation