Effect of ligand sensing on flagellar bundle formation in bacteria

Author:

Agrawal Megha,Chakraborty Soumyadeep,Tirumkudulu Mahesh S.,Venkatesh K.V

Abstract

AbstractE. coli swims in liquid media by rotating long appendages called flagella. The direction of rotation of each flagellum is governed by a transmembrane rotary nanomotor, which receives signals from ligand-specific receptors. Attractants bias the motor to rotate in CCW direction causing flagella to bundle and provide thrust for locomotion. Recent studies have shown that sensing not only leads to increase in CCW bias but also increases the motor rotation speed due to the recruitment of additional stator units bound to the rotor. Despite the detailed studies on bacterial motility, the effect of ligand sensing on the synchronization of flagellar filaments leading to bundle formation and changes in bundle geometry are not clear. In this work, we performed real-time imaging of the flagellar bundle of swimming cells in metabolising (glucose) and non-metabolisable (2-Deoxy-d-glucose) attractants. We characterized bundles during swimming by measuring visible distal length and the spread of filaments at poles. We show that sensing of attractant by receptor leads to the formation of tight bundles when compared to control buffer. Contrary to previous studies, the swimming speeds were proportional to the bundle tightness with the latter dependent not only on the bias but also on the torque exerted by the motor. We further show that the observed wiggles in the swimming trajectory of cells is directly proportional to the spread angles of bundle and is effected by both motor CCW bias and torque. Mutant cells, which were rendered non-motile due to the absence of the PTS (phosphotransferase system) sugar uptake mechanism, exhibited motility when exposed to the non-metabolisable attractant confirming that mere sensing can induce torque in flagellar motor. These results clarify the role of sensing and metabolism on bundle formation and its impact on the motility of cells.Statement of significancePeritrichously flagellated E. coli swims away or towards ligands by biasing the direction of rotation of its flagellar motor. Recently, it has been shown that motor speed is also modulated on merely sensing a ligand. How does this impact flagellar bundle formation and swimming behavior? Using real-time imaging, we show that the bundle geometry changes in response to both metabolisable and non-metabolisable ligand. Mere sensing of a ligand temporarily increases the motor torque and CCW bias that causes tight flagellar bundles and leads to smooth swimming trajectories at high speeds. Our result provides strong evidence of a new signalling pathway that controls the flagellar motor speed to enable the bacteria to respond efficiently to changes in its environment.

Publisher

Cold Spring Harbor Laboratory

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