Membrane fluidity controls redox-regulated cold stress responses in cyanobacteria

Eugene G. Maksimov, Kirill S. Mironov, Marina S. Trofimova, Natalya L. Nechaeva, Daria A. Todorenko, Konstantin E. Klementiev, Georgy V. Tsoraev, Eugene V. Tyutyaev, Anna A. Zorina, Pavel V. Feduraev, Suleyman I. Allakhverdiev, Vladimir Z. Paschenko, Dmitry A. Los

Membrane fluidity is the important regulator of cellular responses to changing ambient temperature. Bacteria perceive cold by the transmembrane histidine kinases that sense changes in thickness of the cytoplasmic membrane due to its rigidification. In the cyanobacterium Synechocystis, about a half of cold-responsive genes is controlled by the light-dependent transmembrane histidine kinase Hik33, which also partially controls the responses to osmotic, salt, and oxidative stress. This implies the existence of some universal, but yet unknown signal that triggers adaptive gene expression in response to various stressors. Here we selectively probed the components of photosynthetic machinery and functionally characterized the thermodynamics of cyanobacterial photosynthetic membranes with genetically altered fluidity. We show that the rate of oxidation of the quinone pool (PQ), which interacts with both photosynthetic and respiratory electron transport chains, depends on membrane fluidity. Inhibitor-induced stimulation of redox changes in PQ triggers cold-induced gene expression. Thus, the fluidity-dependent changes in the redox state of PQ may universally trigger cellular responses to stressors that affect membrane properties.