Distinct constitutive and low-CO2-induced CO2 uptake systems in cyanobacteria:: Genes involved and their phylogenetic relationship with homologous genes in other organisms

Cyanobacteria possess a CO2-concentating mechanism that involves active CO2 uptake and HCO3- transport. For CO2 uptake, we have identified two systems in the cyanobacterium Synechocystis sp. strain PCC 6803, one induced at low CO2 and one constitutive. The low CO2-induced system showed higher maximal activity and higher affinity for CO2 than the constitutive system. On the basis of speculation that separate NAD(P)H dehydrogenase complexes were essential for each of these systems, we reasoned that inactivation of one system would allow selection of mutants defective in the other. Thus, mutants unable to grow at pH 7.0 in air were recovered after transformation of a Delta ndhD3 mutant with a transposon-bearing library. Four of them had tags within slr1302 (designated cupB), a homologue of sll1734 (cupA), which is cotranscribed with ndhF3 and ndhD3. The Delta cupB, Delta ndhD4, and Delta ndhF4 mutants showed CO2-uptake characteristics of the low CO2-induced system observed in wild type. In contrast, mutants Delta cupA, Delta ndhD3, and Delta ndhF3 showed characteristics of the constitutive CO2-uptake system. Double mutants impaired in one component of each of the systems were unable to take up CO2 and required high CO2 for growth. Phylogenetic analysis indicated that the ndhD3/ndhD4-, ndhF3/ndhF4-, and cupA/cupB-type genes are present only in cyanobacteria. Most of the cyanobacterial strains studied possess the ndhD3/ndhD4-, ndhF3/ndhF4-, and cupA/cupB-type genes in pairs. Thus, the two types of NAD(P)H dehydrogenase complexes essential for low CO2-induced and constitutive CO2-uptake systems associated with the NdhD3/NdhF3/CupA-homologues and NdhD4/NdhF4/CupB-homologues, respectively, appear to be present in these cyanobacterial strains but not in other organisms.