In natural environments, photosynthetic organisms adjust their metabolism to cope with the fluctuating availability of combined nitrogen sources, a growth-limiting factor. For acclimation, the dynamic degradation/synthesis of tetrapyrrolic pigments, as well as of the amino acid arginine, is pivotal; however, there has been no evidence that these processes could be functionally coupled. Using co-immunopurification and spectral shift assays, we found that in the cyanobacterium Synechocystis sp. PCC 6803, the arginine metabolism-related ArgD and CphB enzymes form protein complexes with Gun4, an essential protein for chlorophyll biosynthesis. Gun4 binds ArgD with high affinity, and the Gun4-ArgD complex accumulates in cells supplemented with ornithine, a key intermediate of the arginine pathway. Elevated ornithine levels restricted de novo synthesis of tetrapyrroles, which arrested the recovery from nitrogen deficiency. Our data reveal a direct crosstalk between tetrapyrrole biosynthesis and arginine metabolism that highlights the importance of balancing photosynthetic pigment synthesis with nitrogen homeostasis.

Biology Centre of the Czech Academy of Sciences Branišovská 1160 31 370 05 České Budějovice Czech Republic

Laboratory of Photosynthesis Centre Algatech Institute of Microbiology The Czech Academy of Sciences 37901 Třeboň Czech Republic

Laboratory of Photosynthesis Centre Algatech Institute of Microbiology The Czech Academy of Sciences 37901 Třeboň Czech Republic; Faculty of Science University of South Bohemia 37005 České Budějovice Czech Republic

NanoTemper Technologies Floessegasse 4 81369 Munich Germany

NanoTemper Technologies Floessegasse 4 81369 Munich Germany; Department of Molecular Biology and Biotechnology University of Sheffield Sheffield S10 2TN UK

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