Transcriptional regulation of the CO₂-concentrating mechanism in a euryhaline, coastal marine cyanobacteriurn, Synechococcus sp. strain PCC 7002: Role of NdhR/CcmR

Cyanobacterial photosynthesis occurs in radically diverse habitats and utilizes various forms of a CO₂-concentrating mechanism (CCM) featuring multiple inorganic carbon (C_i) transporters. Cyanobacteria from dynamic environments can transform CCM activity depending on C_i availability, and yet the molecular basis for this regulation is unclear, especially in coastal strains. LysR family transcription factors resembling the Calvin cycle regulator CbbR from proteobacteria have been implicated in the expression of C_i transporter genes in freshwater cyanobacteria. Our survey of related factors revealed a group of divergent CbbR-like sequences confined to freshwater and coastal or offshore cyanobacteria. Inactivation of the single gene (termed ccmR) from this variable cluster in the euryhaline (coastal) strain Synechococcus sp. strain PCC 7002 led to constitutive expression of a high-affinity CCM. Derepression of HCO₃^- transporter gene transcription, including that of BicA, a recently discovered HCO₃^- transporter (G. D. Price et al., Proc. Natl. Acad. Sci. USA 101:18228-18233, 2004), was observed. A unique CcmR-regulated operon containing bicA plus 9 open reading frames encoding likely Na⁺/H ⁺ antiporters from the CPA1 and Mnh families was defined that is essential for maximal HCO₃^--dependent oxygen evolution. The promoter region required for C_i-regulated transcription of this operon was defined. We propose that CcmR (and its associated regulon) represents a specialization for species inhabiting environments subject to fluctuating C_i concentrations.