Mechanisms of Signaling and Regulation of Membrane Properties by a Bacterial thermosensor

Abstract

The ability of bacteria to control the biophysical properties of their membrane phospholipids allows them to thrive in a wide range of physical environments. When bacteria are exposed to temperatures below those of their normal conditions, the lipids of their membrane become rigidified, leading to a suboptimal functioning of cellular activities. These organisms can acclimate to such new conditions by an increase in the desaturation of the acyl chain of membrane phospholipids. Phospholipids containing unsaturated fatty acids have a much lower transition temperature than those lipids made of saturated fatty acids. As a result, the physical properties (fluidity) of the membrane lipids return to their original state, or close to it, with restoration of normal cell activity at the lower temperature. We discovered that in the model Gram-positive bacterium Bacillus subtilis the transcription of the des gene, coding for an acyl lipid desaturase, is controlled by a two component system that senses changes in the membrane properties due to abrupt temperature change. The membrane component, named DesK, of this transcriptionally regulatory system is a thermosensor with histidin kinase and phosphatase activities that senses membrane biophysical properties and transmits this signal to the transcriptional apparatus. Combined X-ray crystallographic and functional studies of DesK show that helical rotations in the central four-helix bundle modulate its association with the ATP binding domains. We propose that this signaling-induced transitional rotation provides a switching mechanism to stimulate the kinase or phosphatase activities in response to changes in the lipid environment. These results also provide a new insight into temperature-sensing mechanisms.