Allosteric Properties of Cyanobacterial Cytochrome c Oxidase: Inhibition of the Coupled Enzyme by ATP and Stimulation by ADP

Abstract

Thorough analysis of the cta operon of Synechocystis sp. PCC6803 (grown in high‐concentration salt medium to enhance the expression of respiratory proteins) showed that, apart from ctaCDE and Fb genes potentially encoding subunits I, II, III, and a small pseudo‐bacteria‐like subunit‐IV of unknown function, a large mitochondria‐like cta‐Fm gene and a pronounced terminator structure are additional components of the operon. The deduced cta Fm gene product shows 50% and 20% sequence identity to the Saccharomyces cerevisiae and beef heart mitochondrial COIV proteins, respectively. It also shows amino acid regions (near the N terminus, on the cytosolic side) with conspicuous sequence similarities to adenylate‐binding proteins such as ATP synthase beta subunit Walker A and B consensus regions or to adenylate kinase. We suggest that, similar to the situation with beef heart mitochondria, it is the mitochondria‐like subunit‐IV of the cyanobacterial aa3‐type cytochrome‐c oxidase that confers allosteric properties to the cyanobacterial enzyme, the H+/e‐ ratios of cytochrome c oxidation being significantly lowered by ATP (intravesicular or intraliposomal) but enhanced by ADP. Therefore, the antagonistic action of ATP and ADP was in a way that the redox reaction proper, was always significantly less affected than the coupled proton translocation. Evolutionary and ecological implications of the unusualallosteric regulation ofa prokaryotic cytochrome‐c oxidase is discussed.