Presence of heterogeneous microdomains in thylakoids of cyanobacteria

Adela Strašková, Gábor Steinbach, Eva Kotabová, Josef Komenda, Martin Tichý, Radek Kaňa
Institute of Microbiology, CAS, Centrum ALGATECH, Třeboň, Czech Republic

Primary photochemical reactions in oxygenic photosynthesis require two different photosystems, Photosystem I (PSI) and Photosystem II (PSII). Variability in co-localization/separation of photosystems and their antennae proteins in higher plants are shown in presence of granal and stromal thylakoids that differs in photosystems composition and in membrane organization. Such membrane heterogeneity has not been described in cyanobacteria, an evolutional ancestor of plant chloroplasts.

Therefore, we have addressed the native organization of photosystems and antennae proteins (phycobilisomes – PBS) in cyanobacteria. We have applied 3D single-cell confocal imaging to Synechocystis PCC 6803 cells with PSI fluorescently tagged by yellow fluorescent protein (YFP). By using the new approach, we have found heterogeneous organization of cyanobacteria thylakoid membrane with three dominant microdomains (see Figure): “PSI” (with high PSI content); “PSII-PBS” (with high “PSII-PBS” content); and “PSI-PSII-PBS” (PSI, PSII and PBS in balance). The organization indicates two photosystems can either be spatially segregated or work as a supercomplex with phycobilisomes. The data are in line with our previous 2D measurements obtained by cryoimaging method [1]. The absence of areas with dominancy of phycobilisomes and missing of PBS-PSI microdomain explains mechanism of the excitation energy flow between phycobilisomes and both reaction centers. The organization also restricts feasible mechanisms of state transitions. The detailed picture analysis has revealed that PBS/PSI/PSII ratios in all microdomains is highly restricted and controlled only by a single “protein-arrangement factor”. Our data suggest that the specialized microdomains in cyanobacteria thylakoids represent functional precursors of evolutionary later invention of photosystems segregation into granal and stromal thylakoids.

Reference

[1] J. Photochem. Photobiol. B: Biology 2015, 152, 395-399