Expression of the F0F1 ATP synthase inhibitor Atp{Theta} depends on small basic DNA-binding proteins and differential mRNA stability

F0F1 ATP synthases produce ATP, the universal biological energy source. ATP synthase complexes on cyanobacterial thylakoid membranes use proton gradients generated either by photosynthesis or respiration. Atp{Theta} is an ATP synthase regulator in cyanobacteria encoded by atpT. Atp{Theta} inhibits the hydrolysis of ATP (reverse reaction) that otherwise would occur under unfavorable conditions. In the cyanobacterium Synechocystis sp. PCC 6803, Atp{Theta} is expressed at very low levels under optimum phototrophic growth conditions or in the presence of glucose, but its expression is substantially increased 10 min after transfer into darkness. DNA coimmunoprecipitation experiments followed by mass spectrometry identified the binding of the two transcriptional regulators cyAbrB1 and cyAbrB2 to the promoter and the histone-like protein HU to the 5-UTR of atpT. GFP reporter assays revealed a detectable but small effect on transcriptional regulation. However, atpT transcript stabilities differed dramatically, half-lives were 1.6 min in the light, 33 min in the dark and substantial changes were observed if glucose or DCMU were added. Basic transcriptional control of atpT involves nucleoid-associated DNA-binding proteins, while the major effect on the condition-dependent regulation of atpT expression is mediated by controlling mRNA stability, which is related to the cellular redox and energy status.