Cyanobacteriochrome CcaS regulates phycoerythrin accumulation in Nostoc punctiforme, a group II chromatic adapter

Responding to green and red light, certain cyanobacteria change the composition of their light-harvesting pigments, phycoerythrin (PE) and phycocyanin (PC). Although this phenomenon-complementary chromatic adaptation-is well known, the green light-sensing mechanism for PE accumulation is unclear. The filamentous cyanobacterium Nostoc punctiforme ATCC 29133 (N. punctiforme) regulates PE synthesis in response to green and red light (group II chromatic adaptation). We disrupted the green/red-perceiving histidine-kinase gene (ccaS) or the cognate response regulator gene (ccaR), which are clustered with several PE and PC genes (cpeC-cpcG2-cpeR1 operon) in N. punctiforme. Under green light, wild-type cells accumulated a significant amount of PE upon induction of cpeC-cpcG2-cpeR1 expression, whereas they accumulated little PE with suppression of cpeC-cpcG2-cpeR1 expression under red light. Under both green and red light, the ccaS mutant constitutively accumulated some PE with constitutively low cpeC-cpcG2-cpeR1 expression, whereas the ccaR mutant accumulated little PE with suppression of cpeC-cpcG2-cpeR1 expression. The results of an electrophoretic mobility shift assay suggest that CcaR binds to the promoter region of cpeC-cpcG2-cpeR1, which contains a conserved direct-repeat motif. Taken together, the results suggest that CcaS phosphorylates CcaR under green light and that phosphorylated CcaR then induces cpeC-cpcG2-cpeR1 expression, leading to PE accumulation. In contrast, CcaS probably represses cpeC-cpcG2-cpeR1 expression by dephosphorylation of CcaR under red light. We also found that the cpeB-cpeA operon is partially regulated by green and red light, suggesting that the green light-induced regulatory protein CpeR1 activates cpeB-cpeA expression together with constitutively induced CpeR2.