Skip to main content
SpringerLink
Log in

Molecular mechanisms for interaction of glycine betaine with supra-molecular phycobiliprotein complexes

  • Published:
Science in China Series B: Chemistry Aims and scope Submit manuscript

Abstract

Glycine betaine (GB) is a biologically important small molecule protecting cells, proteins and enzymes in vivo and in vitro under environmental stresses. Recently, it was found that GB could also relax the structure and inactivate the function of phycobiliproteins and phycobilisome (PBS), a kind of supra-molecular complexes, in cyanobacterial cells. The molecular mechanisms for the opposite phenomena are quite ambiguous. Taking PBS and a trimeric or monomeric C-phycocyanin (C-PC) as models, the molecular mechanism for the interaction of GB with supra-molecular complexes or nuclear proteins was investigated. The energetic decoupling of PBS components induced by GB suggests that the PBS core-membrane linking polypeptide was the most sensitive site while the rod-core linker was the next. Biochemistry analysis proves that PBS structure was loosened but not dissociated into the components. On the basis of the results and structure knowledge, it was proposed that GB screened the electrostatic attraction of the opposite charges on a linker and a protein leading to a much looser structure. It was observed that GB induced a spectral blue shift for trimeric C-PC but a red shift for a monomeric C-PC (a nuclear protein), which were ascribed to GB’s screening of the electrostatic attraction of a linker to a protein and strengthening of the hydrophobic interaction between C-PC monomers. The trimers and monomers’ forming of the same products under high concentration of GB was ascribed to a compromise of the opposite interaction forces.

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

Similar content being viewed by others

Abbreviations

GB:

glycine betaine

PBS:

phycobilisome

C-PC:

C-phycocyanin

APC:

allophycocynin

LCM :

core-membrane linker

References

  1. Chattopadhyay M K. The cryoprotective effects of glycine betaine on bacteria. Trends Microbiol, 2002, 10(7): 311–311

    Article  CAS  Google Scholar 

  2. Caldas T, Demont-Caulet N, Ghazi A, Richarme G. Thermoprotection by glycine betaine and choline. Microbiology, 1999, 145: 2543–2548

    CAS  Google Scholar 

  3. Craig S A. Betaine in human nutrition. Am J Clin Nutr, 2004, 80: 539–549

    CAS  Google Scholar 

  4. Michael L, Sizeland P C M, Christopher M F, Chambers S T. Short and long-term variation of plasma glycine betaine concentrations in humans. Clin Biochem, 2004, 37: 184–190

    Article  Google Scholar 

  5. Parageorgiou G C, Murata N. The unusually strong stabilizing effects of glycine betaine on the structure function of the oxygen-evolving Photosystem II complex. Photosyn Res, 1995, 44: 243–252

    Article  Google Scholar 

  6. Li Y, Zhang J P, Xie J, Zhao J Q. Temperature-induced decoupling of phycobilisomes from reaction centers. Biochim Biophys Acta, 2001, 1504: 229–234

    Article  CAS  Google Scholar 

  7. Li D H, Xie J, Zhao Y W, Zhao J Q. Probing connection of PBS with the photosystems in intact cells of Spirulina platensis by temperature-induced fluorescence fluctuation. Biochim Biophys Acta, 2003, 1557: 35–40

    Article  CAS  Google Scholar 

  8. Yang S Z, Su Z Q, Li H, Feng J J, Xie J, Xia A D, Gong Y D, Zhao J Q. Demonstration of phycobilisome mobility by the time- and space- correlated fluorescence imaging of a cyanobacterial cell. Biochim Biophys Acta-Bioenerg, 2007, 1767: 15–21

    Article  CAS  Google Scholar 

  9. Li D H, Xie J, Zhao J Q. Light-induced excitation energy redistribution in Spirulina platensis cells: “spillover” or “mobile PBSs”? Biochim Biophys Acta, 2004, 1608: 114–121

    Article  CAS  Google Scholar 

  10. Li H, Li D H, Yang S Z, Xie J, Zhao J Q. The state transition mechanism — simply depending on light-on and off in Spirulina platensis. Biochim Biophys Acta, 2006, 1757: 1512–1519

    Article  CAS  Google Scholar 

  11. Li H, Yang S Z, Xie J, Zhao J Q. Probing the connection of PBSs to the photosystems in Spirulina platensis by artificially induced fluorescence fluctuations. J Lumin, 2007, 122: 294–296

    Article  Google Scholar 

  12. Sidler W A. Phycobilisome and phycobiliproteins structures. In: Bryant D A. ed. The molecular biology of cyanobacteria. Dordrecht: Kluwer, 1994. 139–216

    Google Scholar 

  13. Kruip B D, Rögner M. Supramolecular architecture of cyanobacterial thylakoid membranes: how is the phycobilisome connected with the photosystems? Photosyth Res, 1996, 49: 103–118

    Article  Google Scholar 

  14. MacColl R. Cyanobacterial phycobilisomes. J Struct Biol, 1998, 124: 311–334

    Article  CAS  Google Scholar 

  15. Zhao J Q, Li H. The excitation energy transfer in photosynthesis of cyanobacteria. In: Naohisa W, Mamoru M, eds. Recent Progress of Bio/chemiluminescence and Fluorescence Analysis in Photosynthesis. Kerala: Research Signpost, 2005. 175–192

    Google Scholar 

  16. Yu M H, Glazer A N. Cyanobacterial phycobilisomes. Role of the linker polypeptides in the assembly of phycocyanin. J Biol Chem, 1982, 257: 3429–3433

    CAS  Google Scholar 

  17. Zilinskas B A, Howell D A. Immunological conservation of phycobilisome rod linker polypeptides. Plant Physiol, 1987, 85: 322–326

    Article  CAS  Google Scholar 

  18. Capuano V, Braux A, Marsac N T, Houmard J. The ‘anchor polypeptide’ of cyanobacterial phycobilisomes. Molecular characterization of the Synechococcus sp. PCC 6301 apcE gene. J Biol Chem, 1993, 268: 8277–8283

    CAS  Google Scholar 

  19. Zhao K H, Su P, Boehm S, Song B, Zhou M, Bubenzer C, Scheer H. Reconstitution of phycobilisome core-membrane linker, LCM, by autocatalytic chromophore binding to ApcE. Biochim Biophys Acta, 2005, 1706: 81–87

    Article  CAS  Google Scholar 

  20. Zilinskas B A, Glick R E. Noncovalent intermolecular forces in phycobilisomes of porphyridium cruentum. Plant Physiol, 1981, 68: 447–452

    Article  CAS  Google Scholar 

  21. Schirmer T, Huber R, Schneider M, Bode W, Miller M, Hackert M L. Crystal structure analysis and refinement at 2.5Å of hexameric C-phycocyanin from the cyanobacterium Agmenellum quadruplicatum. J Mol Biol, 1986, 188: 651–676

    Article  CAS  Google Scholar 

  22. Reuter W, Wiegand G, Huber R, Than M E. Structural analysis at 2.2 Å of orthorhombic crystals presents the asymmetry of the allophycocyanin-linker complex, AP.LC7.8, from phycobilisomes of Mastigocladus laminosus. Proc Natl Acad Sci, 1999, 96: 1363–1368

    Article  CAS  Google Scholar 

  23. Padyana A K, Bhat V B, Madyastha K M, Rajashankar K R, Ramakumar S. Crystal structure of a light-harvesting protein C-phycocyanin from Spirulina Platensis. Biochem Biophys Res Commun, 2001, 282: 893–898

    Article  CAS  Google Scholar 

  24. Gantt E, Lipschultz C A, Grabowski J, Zimmerman B K. Phycobilisomes from blue-green and red algae. Plant Physiol, 1979, 63: 615–620

    Article  CAS  Google Scholar 

  25. Glazer A N, Fang S. Chromophore content of blue-green algal phycobiliproteins. J Biol Chem, 1973, 248: 659–662

    CAS  Google Scholar 

  26. Gantt E, Lipschultz C A, Zilinskas B. Further evidence for a phycobilisome model from selective dissociation, fluorescence emission, immunoprecipitation and electron microscopy. Biochim Biophys Acta, 1976, 430: 375–388

    Article  CAS  Google Scholar 

  27. Debreczeny M P, Sauer K. Comparison of calculated and experimentally resolved rate constants for excitation energy transfer in C-phycocyanin. 2. Trimers. J Phys Chem, 1995, 99: 8420–8431

    Article  CAS  Google Scholar 

  28. Pizarro S A, Sauer K. Spectroscopic study of the light-harvesting protein C-phycocyanin associated with colorless linker peptides. Photochem Photobiol, 2001, 73: 556–563

    Article  CAS  Google Scholar 

  29. Viskari P J, Colyer C L. Separation and quantitation of phycobiliproteins using phytic acid in capillary electrophoresis with laser-induced fluorescence detection. J Chromatography A, 2002, 972: 269–276

    Article  CAS  Google Scholar 

  30. Wang X Q, Li L N, Chang W R, Zhang J P, Gui L L, Guo B J, Liang D C. Structure of C-phycocynin from spirulina platensis at 2.2 Å resolution: a novel crystal from for phycobiliproteins in phycobilisomes. Acta Crytallogr. Sect. D, 2001, 57: 784–792

    Article  CAS  Google Scholar 

  31. Mao H B, Li G, Li D, Wu Q, Gong Y D, Zhang X, Zhao N M. Effects of glycerol and high temperatures on structure and function of phycobilisomes in Synechocystis sp. PCC 6803. FEBS Lett, 2003, 553: 68–72

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Beijing National Laboratory for Molecular Sciences (BNLMS), Photochemistry Laboratory, Institute of Chemistry, Chinese Academy of Sciences, Beijing, 100190, China

    XiuLing Xu, Heng Li, Jie Xie & JingQuan Zhao

Authors
  1. XiuLing Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Heng Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jie Xie
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. JingQuan Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to JingQuan Zhao.

Additional information

Supported by the National Natural Science Foundation of China (Grant No. 20872144)

Equal contribution has been made by the authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Xu, X., Li, H., Xie, J. et al. Molecular mechanisms for interaction of glycine betaine with supra-molecular phycobiliprotein complexes. Sci. China Ser. B-Chem. 52, 1865–1870 (2009). https://doi.org/10.1007/s11426-009-0254-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11426-009-0254-1

Keywords

Search

Navigation