Phycobilisome Diffusion Is Required for Light-State Transitions in Cyanobacteria

Abstract

Phycobilisomes are the major accessory light-harvesting complexes of cyanobacteria and red algae. Studies using fluorescence recovery after photobleaching on cyanobacteria in vivo have shown that the phycobilisomes are mobile complexes that rapidly diffuse on the thylakoid membrane surface. By contrast, the PSII core complexes are completely immobile. This indicates that the association of phycobilisomes with reaction centers must be transient and unstable. Here, we show that when cells of the cyanobacterium Synechococcus sp. PCC7942 are immersed in buffers of high osmotic strength, the diffusion coefficient for the phycobilisomes is greatly decreased. This suggests that the interaction between phycobilisomes and reaction centers becomes much less transient under these conditions. We discuss the possible reasons for this. State transitions are a rapid physiological adaptation mechanism that regulates the way in which absorbed light energy is distributed between PSI and PSII. Immersing cells in high osmotic strength buffers inhibits state transitions by locking cells into whichever state they were in prior to addition of the buffer. The effect on state transitions is induced at the same buffer concentrations as the effect on phycobilisome diffusion. This implies that phycobilisome diffusion is required for state transitions. The main physiological role for phycobilisome mobility may be to allow such flexibility in light harvesting.

Lateral Segregation of Photosystem I in Cyanobacterial Thylakoids

“…State transitions in cyanobacteria involve responses to fluctuations in the quantity and quality of incident light and the redistribution of energy harvested by phycobilisomes to mainly PSI or PSII (van Thor et al, 1998). The PSI/ PSII regions identified in Figures 5A, 5B, and 7 and Supplemental Figure 10 represent a functionally flexible array of traps where small adjustments in phycobilisome-photosystem interactions, either through local conformational changes in the phycobilisome or in underlying membrane proteins (Biggins et al, 1984) or through movement of phycobilisomes on the membrane surface (Joshua and Mullineaux, 2004), alter the destination for energy harvested by the phycobilisome. Whether the PSI-only zones in Figure 1A are also visited by phycobilisomes as part of the state transition mechanism is not known.…”

Changes in the transthylakoid proton gradient are caused by the movement of phycobilisomes in the cyanobacterium Synechocystis sp. strain PCC 6803

“…The transition was strongly inhibited when the PBSs were immobilized by GB (Figures 2(c) and 3(c)). These results clearly show that light-induced state transitions depend predominantly on the movement of PBSs [7,25].…”

“…Similarly, treatments with 1 mol L -1 phosphate, sucrose and potassium chloride solutions, which are also inhibitors of PBS movement [7,35], also significantly reduced the intensity of the slow phase of ms-DLE (data not shown). Taken together, it appears that the movement of PBSs on the surface of the thylakoid membrane is responsible for the effective establishment of ΔpH in cyanobacteria.…”

“…This dynamic and rapid process of achieving energy balance is called "state transition" [5,6]. Because phycobilisome (PBS) movement is a prerequisite for cyanobacterial state transitions [7,8], "mobile PBSs" are believed to play a key role in allowing state transitions in cyanobacteria. A recent study indicated that the movement of PBSs between PSII and PSI affects both cyclic and respiratory electron transport [9].…”

The role of the orange carotenoid protein and PsbU protein in photoprotection in cyanobacteria

“…The first one is based on the fact that PBs can migrate along the surface of the thylakoid membrane. It proposes that the PBs are the mobile elements which, by changing their association with PSII and PSI, deliver energy preferentially to one or the other photosystems (Mullineaux and Holzwarth, 1990;Mullineaux et al, 1997;Sarcina et al, 2001;Joshua and Mullineaux, 2004). The second theory based on results suggesting that the mobile elements are the photosystems (Biggins and Bruce, 1985;Schluchter et al, 1996;El Bissati et al, 2000).…”