Coordination of Cyanobacterial Nitrate Assimilation and Photosynthesis by a Novel PsbO-Interacting Protein PirN

Nitrogen assimilation relies on photosynthetically produced energy and reducing equivalents. Here, we identify a small protein, PsbO-interacting regulator of nitrate assimilation (PirN), as a key coordinator of photosynthesis and nitrate assimilation in Synechocystis sp. PCC 6803 (Synechocystis). PirN specifically accumulates in nitrate-grown cells and interacts with the photosystem II (PSII) subunit PsbO. Deletion of pirN (ΔpirN) under nitrate impairs growth, reduces PSII contents and oxygen evolution, and upregulates most nitrogen transport and assimilation proteins except the nitrate reductase NarB, mimicking nitrogen starvation response likely due to impaired nitrate reduction. PsbO expression is markedly reduced in both ΔpirN and ΔnarB mutants. Complementation of narB or psbO in the ΔpirN mutant background largely rescued the growth defect of the mutant and led to increased expression of PsbO or NarB, respectively. These findings suggest that PirN is a nitrate-inducible regulator that hierarchically modulates NarB and PsbO expression to couple nitrate assimilation with photosynthetic activity. This coordination likely safeguards redox homeostasis when nitrate assimilation or photosynthetic electron production is perturbed.