Summary The model heterocyst-forming filamentous cyanobacterium, Anabaena sp. PCC 7120 ( Anabaena ) represents multicellular organisms capable of simultaneously performing oxygenic photosynthesis in vegetative cells and the O 2 -sensitive N 2 -fixation inside the heterocysts. The flavodiiron proteins (FDPs) have been shown to participate in photoprotection of photosynthesis by driving excess electrons to O 2 (Mehler-like reaction). Here, we addressed the physiological relevance of the vegetative cell-specific Flv1A and Flv3A on the bioenergetic processes occurring in diazotrophic Anabaena under variable CO 2 . We demonstrate that both Flv1A and Flv3A are required for proper induction of the Mehler-like reaction upon a sudden increase in light intensity, which is likely important for the activation of carbon-concentrating mechanisms (CCM) and CO 2 fixation. Under ambient CO 2 diazotrophic conditions, Flv3A is capable of mediating moderate O 2 photoreduction, independently of Flv1A, but in coordination with Flv2 and Flv4. Strikingly, the lack of Flv3A resulted in strong downregulation of the heterocyst-specific uptake hydrogenase, which led to enhanced H 2 photoproduction under both oxic and micro-oxic conditions. These results reveal a novel regulatory network between the Mehler-like reaction and the diazotrophic metabolism, which is of great interest for future biotechnological applications.

Flv3A facilitates O2 photoreduction and affects H2 photoproduction independently of Flv1A in diazotrophic Anabaena filaments