Structure, function, and regulation of the cyanobacterial high-affinity bicarbonate transporter

Abstract

Exposure of high-CO2-grown cells of cyanobacteria to inorganic carbon-limitation induces transcription of particular genes and expression of high-affinity CO2 and HCO3- transport systems. Among the low-CO2-inducible transcription units of Synechococcus sp. strain PCC 7942 is the cmpABCD operon, which encodes an ATP-binding cassette (ABC) transporter involved in HCO3- uptake. The three genes, cmpBCD, encode membrane components of an ABC transporter, whereas cmpA encodes a 42-kD protein anchored to the plasma membrane, which binds HCO3- with high affinity (Kd = 5 m M) and acts as the substrate-binding protein of the transporter. A deletion mutant of cmpAB (M42) retains low CO2-inducible activity of HCO3- transport, indicating occurrence of HCO3- transporter(s) distinct from the one encoded by cmpABCD. Since HCO3- uptake by low CO2-induced M42 cells shows lower affinity for external HCO3- than for wild-type cells under the same conditions, it is deduced that the HCO3- transporter encoded by cmpABCD has the highest affinity for HCO3- among the HCO3- transporters present in the cyanobacterium. The low CO2-responsive induction of the cmpABCD operon requires a LysR family protein CmpR, which is similar to CbbR (RbcR), the activator of the CO2 fixation operons of chemoautotrophic and purple photosynthetic bacteria. In the mutant of cmpR, low CO2-induced upregulation of the rbcLS and ccmKLMNO operons was not abolished but enhanced, indicating presence of multiple mechanisms for low CO2-responsive gene activation in cyanobacteria.