Phycobilisomes

The phycobiliproteins are accessory photosynthetic pigments aggregated in cells as phycobilisomes that are attached to the thylakoid membrane of the chloroplast. The red phycobiliproteins (phycoerythrin) and the blue phycobiliprotein (phycocy-anin) are soluble in water and can serve as natural colorants in foods, cosmetics, and pharmaceuticals. Chemically, the phycobiliproteins are built from chro-mophores — bilins — that are open-chain tetrapyrroles covalently linked via thio-ether bonds to an apoprotein. ... 

Despite their absence in phycobilisomes, carotenoids, especially the so-called secondary carotenoids such as echinenone, were presumed to play a role in cyanobacterial photoprotection. Indeed, classic biochemical approaches have led to several reports of cyanobacterial carotenoid-proteins and evidence for their photoprotective function (Kerfeld et al. 2003, Kerfeld 2004b). One of these, the water soluble orange carotenoid protein (OCP), has been structurally characterized and has recently emerged as a key player in cyanobacterial photoprotection. 

In contrast to the photosynthetic eukaryotes, photoprotection in cyanobacteria is not induced by the presence of a transthylakoid ApH or the excitation pressure on PSII. Instead, intense blue-green light (400-550 nm) induces a quenching of PSII fluorescence that is reversible in minutes even in the presence of translation inhibitors (El Bissati et al. 2000). Fluorescence spectra measurements and the study of the NPQ mechanism in phycobilisome- and PSII-mutants of the cyanobacterium Synechocystis PCC6803 indicate that this mechanism involves a specific decrease of the fluorescence emission of the phycobilisomes and a decrease of the energy transfer from the phycobilisomes to the RCs (Scott et al. 2006, Wilson et al. 2006). The site of the quenching appears to be the core of the phycobilisome (Scott et al. 2006, Wilson et al. 2006, Rakhimberdieva et al. 2007b). 

NPQ (Rakhimberdieva et al. 2004) exactly matches the absorption spectrum of the carotenoid, 3 -hydrox yech i nenone (Polivka et al. 2005) in the OCP. The OCP is now known to be specifically involved in the phycobilisome-associated NPQ and not in other mechanisms affecting the levels of fluorescence such as state transitions or D1 damage (Wilson et al. 2006). Studies by immunogold labeling and electron microscopy showed that most of the OCP is present in the interthylakoid cytoplasmic region, on the phycobilisome side of the membrane, Figure 1.2 (Wilson et al. 2006). The existence of an interaction between the OCP and the phycobilisomes and thylakoids was supported by the co-isolation of the OCP with the phycobilisome-associated membrane fraction (Wilson et al. 2006, 2007). 

The known structure of the OCP is a snapshot of the presumably dark-state-adapted form of the protein. From the model, it is difficult to imagine how the concealed carotenoid could interact with one of the components of the phycobilisome in order to quench the absorbed energy. However, the surface of the OCP has numerous surface cavities and clefts, as shown in Figure 1.3b, including two... 

Adir, N. (2005). Elucidation of the molecular structures of components of the phycobilisome Reconstructing a giant. Photosynth Res 85(1) 15-32. 

Joshua, S., S. Bailey, N. H. Mann, and C. W. Mullineaux (2005). Involvement of phycobilisome diffusion in energy quenching in cyanobacteria. Plant Physiol 138(3) 1577-1585. 

Mullineaux, C. W. (1992). Excitation energy transfer from phycobilisomes to photosystem-I in a cyanobacterium. Biochim Biophys Acta 1100(3) 285-292. 

Rakhimberdieva, M. G., Y. V. Bolychevtseva, I. V. Elanskaya, and N. V. Karapetyan (2007a). Protein-protein interactions in carotenoid triggered quenching of phycobilisome fluorescence in Synechocystis sp. PCC 6803. FEBS Lett 581(13) 2429-2433. 

Wilson, A., G. Ajlani, J. M. Verbavatz et al. (2006). A soluble carotenoid protein involved in phycobilisome-related energy dissipation in cyanobacteria. Plant Cell 18(4) 992-1007. 

Glazer, A.N. (1985) Light harvesting by phycobilisomes. Annu. Rev. Biophys. Chem. 14, 47-77. 

Grabowski, J., and Gantt, E. (1978) Photophysical properties of phycobiliproteins from phycobilisomes Fluorescence lifetimes, quantum yields, and polarization spectra. Photochem. Pbotobiol. 28, 39-45. 

FIGURE 19-43 A phycobilisome. In these highly structured assemblies found in cyanobacteria and red algae, phycobilin pigments bound to specific proteins form complexes called phycoerythrin (PE), phycocyanin (PC), and allophycocyanin (AP). The energy of photons absorbed by PE or PC is conveyed through AP (a phycocyanobilin-binding protein) to chlorophyll a of the reaction center by exciton transfer, a process discussed in the text. 

Fig. 3 Schematic model of light-harvesting compartments in photosynthetic organisms and their position with respect to the membrane and the reaction centers. RC1(2) Photosystem I(II) reaction centre. Peripheral membrane antennas Chlorosome/FMO in green sulfur and nonsulfur bacteria, phycobilisome (PBS) in cyanobacteria and rhodophytes and peridinin-chlorophyll proteins (PCP) in dyno-phytes. Integral membrane accessory antennas LH2 in purple bacteria, LHC family in all eukaryotes. Integral membrane core antennas B808-867 complex in green nonsulfur bacteria, LH1 in purple bacteria, CP43/CP47 (not shown) in cyanobacteria and all eukaryotes.

Phycobiliproteins are found also in cryptophytes but, differently from cyanobacteria and red algae, they are not organized into a phycobilisome, but instead they are located in the thylakoid lumen. Unique for cryptophytes, their phycobiliproteins do not exhibit a trimeric aggregation state characteristic for cyanobacteria, but instead they are present as ai(3a2(3 heterodimers, with each a subunit having a distinct amino acid sequence. [40]... 

Ashby, M. K., and Mullineaux, C. W. 1999. Cyanobacterial ycf27 gene products regulate energy transfer from phycobilisomes to photosystems I and II. FEMSMicrobiol. Lett. 181, 253-260. 

Bryant, D. 1991. Cyanobacterial phycobilisomes progress toward complete structural and functional analysis via molecular genetics. In Bogorad L. and Vails IK (eds) Cell Structure Somatic Cell Genetics of Plants, Vol. 7B (The Photosynthetic Apparatus Molecular Biology and Operation), pp 257-300. Academic Press, New York. 

Carotenoids are found in all native photosynfhetic organisms. They serve a dual function, as both accessory antenna pigment and also are essential in photoprotection of photosynfhetic systems from the effects of excess light, especially in the presence of oxygen. Bilins are open-chain tetrapyrroles that are present in antenna complexes called phycobilisomes. These complexes are found in cyanobacteria and red algae. Structures of representative carotenoid pigments are shown in Figure 3. 

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