Inverse transcriptional activities during complementary chromatic adaptation are controlled by the response regulator RcaC binding to red and green light-responsive promoters

Complementary chromatic adaptation (CCA) provides cyanobacteria with the ability to shift between red and blue-green phenotypes that are optimized for absorption of different wavelengths of light. Controlled by the ratio of green to red light, this process results from differential expression of two groups of operons, many of which encode proteins involved in photosynthetic light harvesting antennae biogenesis. In the freshwater species Fremyella diplosiphon, the inverse regulation of these two classes is complex and occurs through different mechanisms. It also involves a two-component pathway that includes a phytochrome-class photoreceptor and the response regulator RcaC. Here we uncover the mechanism through which this system controls CCA by demonstrating that RcaC binds to the L Box within promoters of both classes of light-regulated operons. We provide functional evidence that complementary regulation of these operons occurs by RcaC's simultaneous activation and repression of transcription in red light. We identify rcaC and L Boxes in the genome of a marine cyanobacterium capable of CCA, suggesting widespread use of this control system. These results provide important insights into the long-standing enigma of CCA regulation and complete the first description of an entire two-component system controlled by a phytochrome-class photoreceptor.