Redox-based sensing controls bacterial chemotaxis to copper

Abstract

AbstractChemotaxis is a widespread strategy used by unicellular and multicellular living organisms to maintain their fitness in stressful environments. In bacteria, the control of chemotaxis relies on the sensing of environmental changes by chemoreceptors, which modulate flagellar rotation via the well-characterized CheA-CheY two-component system. However, the molecular mechanisms underlying signal recognition and activation of the chemoreceptors remain largely unclear.Here we address this gap in the frame of a chemotactic response sustaining bacterial flight from toxic copper (Cu). We found that a significant Cu accumulation in the cytosol triggers an oxidative stress, which can be abrogated by the overexpression of the superoxide dismutase SodB or of the catalase KatG. Interestingly, the inhibition of ROS production not only improves cell growth but also impedes Cu-chemotaxis, suggesting that ROS derived from cytosolic Cu mediate the control of Cu chemotaxis. We also provide evidence that cellular Cu accumulation favors Cu binding to the sensor domain of the newly identified chemoreceptor McpR. Finally, we discovered that the redox cycling of the McpR-bound Cu modulates McpR conformation. Overall our study provides mechanistic insights on a redox-based sensing by a chemoreceptor, indicating that the cellular redox status can play a key role in bacterial chemotaxis.