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New light on photosynthesis regulation in the ancient cyanobacteria

​Plants, algae, cyanobacteria regulate their photosynthesis so that it is as effective as possible and not deleterious. A study, published in Plant Cell and led by a SB2SM team (CEA-Joliot) unveils one of the mechanisms of regulation in cyanobacteria and show that it is very different from that equivalent in plants and algae.

Published on 20 March 2019

​All oxygen evolving photosynthetic organisms including the cyanobacteria, the first of them, must continuously adjust to changing light conditions to maximize photosynthetic efficiency while protecting their photochemical centers. Not only the intensity but also the quality of light fluctuates during the day-life of cyanobacteria, algae and plants. This later can be induced in plants by the leaf movement creating temporal shadow of other leaves and in water leaving organisms, by traveling in the water column. Since the light wavelength that is preferentially absorbed by photosystem I (PSI) or PSII, which works in tandem to convert the light energy into chemical energy, are different, a change in light quality creates an energy imbalance, leading to the reduction or oxidation of the intersystem electron transport chain. A mechanism known as state transitions, which is triggered by changes  in the redox state of the membrane-soluble plastoquinone (PQ) pool located in the electron transport chain between PSII and the cytochrome b6f (cyt b6f) complex, tries to correct this imbalance. In plants and green algae, the sensor for the redox state of the PQ pool is the cyt b6f, which interacts with a specific kinase of the plant antenna, the light-harvesting complex II (LHCII). The phosphorylation state of LHCII regulates its binding to PSII or PSI, redistributing excitation energy between the photosystems as needed. This allows an efficient utilization of the absorbed light to construct organic molecules from carbon dioxide and water, which helps life on Earth. 

While much is known about state transitions in plants and algae, the knowledge about this mechanism in cyanobacteria is very poor. In this article we show that surprisingly, state transitions in the model cyanobacteria Synechocystis PCC 6803 and Synechococcus elongatus occur via a process quite different from that of plants and green algae. By following PS II fluorescence changes induced by conditions triggering changes in the PQ pool redox state in cyanobacteria treated or not with different chemicals affecting the redox state of the PQ pool and cyt b6f activity, we demonstrated that the cyt b6f complex is not involved in state transitions in S. elongatus or Synechocystis. In addition, it appears that no specific phosphorylation reaction participates in cyanobacterial state transitions either. State transitions were not hindered or modified in 21 protein kinase and phosphatase mutants. In addition, kinase and phosphatase inhibitors which inhibit state transitions in green algae, have no effect on cyanobacterial state transitions.  Finally, we confirmed the hypothesis proposed by Ranjbar Choubeh et al, 2018, that cyanobacterial state transitions involve a large reversible PSII fluorescence quenching that it is not connected to changes of spillover (direct energy transfer from PSII to PSI).

While much remains to be learned about the signal transduction pathway underlying state transitions in cyanobacteria, we now know that this pathway is completely different from that of plants and green algae. Further analysis of this process in cyanobacteria would shed light on the evolution of photosynthesis, a process so crucial for life on Earth.

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