Flavodiiron Proteins in Oxygenic Photosynthetic Organisms: Photoprotection of Photosystem II by Flv2 and Flv4 in Synechocystis sp PCC 6803

Background: Flavodiiron proteins (FDPs) comprise a group of modular enzymes that function in oxygen and nitric oxide detoxification in Bacteria and Archaea. The FDPs in cyanobacteria have an extra domain as compared to major prokaryotic enzymes. The physiological role of cyanobacteria FDPs is mostly unknown. Of the four putative flavodiiron proteins (Flv1-4) in the cyanobacterium Synechocystis sp. PCC 6803, a physiological function in Mehler reaction has been suggested for Flv1 and Flv3. Principal Findings: We demonstrate a novel and crucial function for Flv2 and Flv4 in photoprotection of photosystem II (PSII) in Synechocystis. It is shown that the expression of Flv2 and Flv4 is high under air level of CO2 and negligible at elevated CO2. Moreover, the rate of accumulation of flv2 and flv4 transcripts upon shift of cells from high to low CO2 is strongly dependent on light intensity. Characterization of FDP inactivation mutants of Synechocystis revealed a specific decline in PSII centers and impaired translation of the D1 protein in Delta flv2 and Delta flv4 when grown at air level CO2 whereas at high CO2 the Flvs were dispensable. Delta flv2 and Delta flv4 were also more susceptible to high light induced inhibition of PSII than WT or Delta flv1 and Delta flv3. Significance: Analysis of published sequences revealed the presence of cyanobacteria-like FDPs also in some oxygenic photosynthetic eukaryotes like green algae, mosses and lycophytes. Our data provide evidence that Flv2 and Flv4 have an important role in photoprotection of water-splitting PSII against oxidative stress when the cells are acclimated to air level CO2. It is conceivable that the function of FDPs has changed during evolution from protection against oxygen in anaerobic microbes to protection against reactive oxygen species thus making the sustainable function of oxygen evolving PSII possible. Higher plants lack FDPs and distinctly different mechanisms have evolved for photoprotection of PSII.