Phycobilisome breakdown effector NblD is required to maintain the cellular amino acid composition during nitrogen starvation
Nitrogen starvation induces a coordinated nitrogen-saving program in cyanobacteria. NblD is the 66-amino-acid effector of nitrogen-limitation-induced phycobilisome breakdown, which is believed to replenish the cellular amino acid pools. To address the physiological functions of NblD, the concentrations of amino acids, intermediates of the ornithine-ammonia cycle and several organic acids were measured during the response to nitrogen starvation in the cyanobacterium Synechocystis sp. PCC 6803 wild type and in an nblD-deletion strain. A characteristic signature of metabolite pool composition was identified, which shows that NblD-mediated phycobilisome degradation is required to maintain the cellular amino acid and organic acid pools during nitrogen starvation. Specific deviations from the wild type suggest wider-reaching effects that also affect such processes as redox homeostasis via glutathione and tetrapyrrole biosynthesis, both of which are linked to the strongly decreased glutamate pool, carbon fixation because the pool of 3-phosphoglyceric acid, the stable CO2 fixation product of RubisCO, was also decreased, and transcriptional reprogramming via an enhanced concentration of 2-oxoglutarate, the metabolite coregulator of the NtcA transcription factor. The essential role played by NblD in metabolic homeostasis is consistent with the widespread occurrence of NblD throughout the cyanobacterial radiation and the previously observed strong positive selection for the nblD gene under fluctuating nitrogen supply.