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Catch bond drives stator mechanosensitivity in the bacterial flagellar motor

  1. Francesco Pedacia,1
  1. aCentre de Biochimie Structurale (CBS), INSERM, CNRS, Université de Montpellier, 34090 Montpellier, France;
  2. bDepartment of Mathematics, University College London, London WC1E 6BT, United Kingdom;
  3. cBiophysics Graduate Group, University of California, Berkeley, CA 94720;
  4. dDepartment of Physics, Clarendon Laboratory, University of Oxford, Oxford OX1 2JD, United Kingdom
  1. Edited by Steven M. Block, Stanford University, Stanford, CA, and approved October 27, 2017 (received for review September 11, 2017)

Significance

The bacterial flagellar motor (BFM) is the rotary motor powering swimming of many motile bacteria. Many of the components of this molecular machine are dynamic, a property which allows the cell to optimize its behavior in accordance with the surrounding environment. A prime example is the stator unit, a membrane-bound ion channel that is responsible for applying torque to the rotor. The stator units are mechanosensitive, with the number of engaged units dependent on the viscous load on the motor. We measure the kinetics of the stators as a function of the viscous load and find that the mechanosensitivity of the BFM is governed by a catch bond: a counterintuitive type of bond that becomes stronger under force.

Abstract

The bacterial flagellar motor (BFM) is the rotary motor that rotates each bacterial flagellum, powering the swimming and swarming of many motile bacteria. The torque is provided by stator units, ion motive force-powered ion channels known to assemble and disassemble dynamically in the BFM. This turnover is mechanosensitive, with the number of engaged units dependent on the viscous load experienced by the motor through the flagellum. However, the molecular mechanism driving BFM mechanosensitivity is unknown. Here, we directly measure the kinetics of arrival and departure of the stator units in individual motors via analysis of high-resolution recordings of motor speed, while dynamically varying the load on the motor via external magnetic torque. The kinetic rates obtained, robust with respect to the details of the applied adsorption model, indicate that the lifetime of an assembled stator unit increases when a higher force is applied to its anchoring point in the cell wall. This provides strong evidence that a catch bond (a bond strengthened instead of weakened by force) drives mechanosensitivity of the flagellar motor complex. These results add the BFM to a short, but growing, list of systems demonstrating catch bonds, suggesting that this “molecular strategy” is a widespread mechanism to sense and respond to mechanical stress. We propose that force-enhanced stator adhesion allows the cell to adapt to a heterogeneous environmental viscosity and may ultimately play a role in surface-sensing during swarming and biofilm formation.

Footnotes

  • ?1To whom correspondence should be addressed. Email: francesco.pedaci{at}cbs.cnrs.fr.
  • Author contributions: A.L.N. and F.P. designed research; A.L.N. and E.G. performed research; R.P.-C. contributed new reagents/analytic tools; A.L.N., R.P.-C., J.A.N., A.B., R.M.B., and F.P. analyzed data; and A.L.N., R.M.B., and F.P. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at www.danielhellerman.com/lookup/suppl/doi:10.1073/pnas.1716002114/-/DCSupplemental.

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