Chlorophyll biosynthesis under the control of arginine metabolism

• Published in: Cell reports (Cambridge) Vol. 42; no. 11; p. 113265
• Main Authors: Kiss, Éva, Talbot, Jana, Adams, Nathan B.P., Opekar, Stanislav, Moos, Martin, Pilný, Jan, Kvasov, Tatjana, Schneider, Emilia, Koník, Peter, Šimek, Petr, Sobotka, Roman
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 28.11.2023; Cell Press; Elsevier
• Subjects: Arginine - metabolism; bilins; chlorophyll; Chlorophyll - metabolism; CP: Plants; genome-uncoupled-4; Nitrogen; nitrogen homeostasis; Ornithine; Synechocystis; Synechocystis - metabolism; tetrapyrrole biosynthesis; CP: Plants; genome-uncoupled-4; tetrapyrrole biosynthesis; nitrogen homeostasis; chlorophyll; Synechocystis; arginine metabolism; bilins
• ISSN: 2211-1247; 2211-1247
• DOI: 10.1016/j.celrep.2023.113265

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. [Display omitted] •ArgD of arginine pathway interacts with the Gun4 protein of chlorophyll biosynthesis•Ornithine stimulates the ArgD-Gun4 interaction and inhibits tetrapyrrole synthesis•The inhibition by ornithine is released in a strain lacking the ArgD-Gun4 complex Kiss et al. demonstrate that the synthesis of the main photosynthetic pigment, chlorophyll, and the metabolism of arginine (managing N-stockpile) are functionally coupled via protein-protein interactions in cyanobacteria.