A membrane-bound cAMP receptor protein, SyCRP1 mediates inorganic carbon response in Synechocystis sp. PCC 6803

The availability of inorganic carbon (C_i) as the source for photosynthesis is fluctuating in aquatic environments. Despite the involvement of transcriptional regulators CmpR and NdhR in regulating genes encoding C_i transporters at limiting CO₂, the C_i-sensing mechanism is largely unknown among cyanobacteria. Here we report that a cAMP-dependent transcription factor SyCRP1 mediates C_i response in Synechocystis. The mutant ∆sycrp1 exhibited a slow-growth phenotype and reduced maximum rate of bicarbonate-dependent photosynthetic electron transport (V_max) compared to wild-type at the scarcity of CO₂. The number of carboxysomes was decreased significantly in the ∆sycrp1 at low CO₂ consistent with its reduced V_max. The DNA microarray analysis revealed the upregulation of genes encoding C_i transporters in ∆sycrp1. The membrane-localized SyCRP1 was released into the cytosol in wild-type cells shifted from low to high CO₂ or upon cAMP treatment. Soluble His-tagged SyCRP1 was shown to target DNA-binding sites upstream of the C_i-regulated genes sbtA and ccmK3. In addition, cAMP enhanced the binding of SyCRP1 to its target sites. Our data collectively suggest that the C_i is sensed through the second messenger cAMP releasing membrane-bound SyCRP1 into cytoplasm under sufficient CO₂ conditions. Hence, SyCRP1 is a possible regulator of carbon concentrating mechanism, and such a regulation might be mediated via sensing C_i levels through cAMP in Synechocystis.