Dynamics of photosynthetic membranes in cyanobacteria

Conrad Mullineaux
Professor of Microbiology
School of Biological and Chemical Sciences
Queen Mary, University of London
Mile End Road,
London E1 4NS
UK

We use Fluorescence Recovery after Photobleaching to monitor the diffusion of protein complexes and lipids in the thylakoid membranes of live cells of cyanobacteria. Cyanobacteria come in different shapes and sizes. The technique can be applied to many species, but our favourite is Synechococcus 7942, which has elongated cells, and beautiful, regular thylakoid membrane conformation.

Thin-section electron micrographs of Synechococcus 7942. The thylakoid membranes can be seen as a series of concentric cylinders in the cytoplasm.

We have used FRAP to probe the mobility of lipids, photosynthetic pigment-protein complexes and other proteins tagged with GFP. Results for the photosynthetic complexes (light-harvesting phycobilisomes and Photosystem II reaction centres) are shown below.

Phycobilisomes diffuse rather rapidly on the membrane surface

Confocal FRAP image sequence showing phycobilisome diffusion in Synechococcus 7942. Time in seconds is shown top right. A line is bleached across the cell, and subsequent spread and recovery of the bleach shows phycobilisome diffusion.

In contrast to the phycobilisomes, the Photosystem II reaction centres are usually completely immobile. These results led a new model for membrane organisation and phycobilisome-reaction centre interaction.

Model for dynamic interaction of phycobilisomes and reaction centres

Photosystem II, Photosystem I and a phycobilisome (blue complex on the membrane surface) are shown. In reality, the phycobilisomes are packed much more densely than this. The reaction centres are normally slow-moving or immobile. Phycobilisomes are coupled only weakly to the reaction centres, and frequently detach, diffuse, and couple to another reaction centre. We have shown that this weak coupling of the phycobilisomes is essential for the rapid regulation of light-harvesting.

Some key publications on this topic:

Mullineaux, C.W., Tobin, M.J. and Jones, G.R. (1997) Mobility of photosynthetic complexes in thylakoid membranes. Nature 390, 421-424.

Sarcina, M., Tobin, M.J. and Mullineaux, C.W. (2001) Diffusion of phycobilisomes on the thylakoid membranes of the cyanobacterium Synechococcus 7942: effects of phycobilisome size, temperature and membrane lipid composition. J. Biol. Chem. 276: 46830-46834.

Mullineaux, C.W. and Sarcina, M. (2002) Probing the dynamics of photosynthetic membranes with Fluorescence Recovery after Photobleaching. Trends Plant Sci. 7, 237-240.

Sarcina, M., Murata, N., Tobin, M.J. and Mullineaux, C.W. (2003) Lipid diffusion in the thylakoid membranes of the cyanobacterium Synechococcus sp.: effect of fatty acid desaturation. FEBS Lett. 553, 295-298.

Sarcina, M. and Mullineaux, C.W. (2004) Mobility of the IsiA chlorophyll-binding protein in cyanobacterial thylakoid membranes. J. Biol. Chem. 279, 36514-36518

Mullineaux, C.W. (2004) FRAP analysis of photosynthetic membranes. J. Exp. Bot. 55, 1207-1211.

Joshua, S. and Mullineaux, C.W. (2004) Phycobilisome diffusion is required for light-state transitions in cyanobacteria. Plant Physiol. 135, 2112-2119.

Aspinwall, C.L., Sarcina, M. and Mullineaux, C.W. (2004) Phycobilisome mobility in the cyanobacterium Synechococcus sp. PCC7942 is influenced by the trimerisation of Photosystem I. Photosynthesis Research 79, 179-187.

Joshua, S. and Mullineaux, C.W. (2005) The rpaC gene product regulates phycobilisome-photosystem II interaction in cyanobacteria. BBA-Bioenergetics 1709, 58-68

Joshua, S., Bailey, S., Mann, N.H. and Mullineaux, C.W. (2005) Involvement of phycobilisome diffusion in energy quenching in cyanobacteria. Plant Physiology 138, 1577-1585.

Sarcina, M., Bouzovitis, N. and Mullineaux, C.W. (2006) Mobilization of Photosystem II induced by intense red light in the cyanobacterium Synechococcus sp. PCC7942. The Plant Cell 18, 457-464.

Mullineaux, C.W. (2008) Phycobilisome-reaction centre interaction in cyanobacteria. Photosynth. Res. 95, 175-182

Mullineaux, C.W. (2008) Factors controlling the mobility of photosynthetic proteins. Photochem. Photobiol. 84, 1310-1316

Kondo, K., Mullineaux, C.W. and Ikeuchi, M. (2009) Distinct roles of CpcG1 phycobilisome and CpcG2 phycobilisome in state transitions in a cyanobacterium Synechocystis sp. PCC6803. Photosynth. Res. 99, 217-225