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