Mechanisms for bacterial gliding motility on soft substrates

Abstract

The motility mechanism of certain rod-shaped bacteria has long been a mystery, since no external appendages (pili, flagella or cilia) are involved in their motion which is known as "gliding". The physical principles behind gliding motility still remain poorly understood. As a canonical example of such organisms, myxobacteria exhibit a gliding motility where the gliding speed depends on the substrate stiffness (1, 2): an effect known as mechanosensitivity. While there exist some physical models for the mechanosensitivity of eukaryotic cells in tissues due to adhesion (3), the mechanism of myxobacterial gliding motility remains unclear mainly due to the existence of a thin slime layer secreted between the cell and the substrate (4). Here we identify the physical principles behind gliding motility, and develop a theoretical model that predicts a two-regime behavior of the gliding speed as a function of the substrate stiffness. Our theory describes the elastic, viscous, and capillary interactions between the bacterial membrane carrying a traveling wave, the slime layer acting as a lubricating viscous film, and the substrate which we model as a soft solid. Defining the gliding motility as the horizontal translation under zero net force, we find the two-regime behavior is due to two different mechanisms of motility thrust. On stiff substrates, the gliding thrust arises from the elasto-hydrodynamic interactions between the bacteria, the slime and the substrate, whereby the bacterial shape deformations create a flow of slime exerting a pressure along the bacterial length. This pressure in conjunction with the bacteria shape provides the necessary thrust for propulsion. However, we show that such a mechanism cannot lead to gliding on very soft substrates. Instead, we show that including capillary effects along with the elasto-hydrodynamic interactions leads to formation of a ridge at the slime-substrate-air interface, which creates a thrust in the form of a localized pressure gradient at the tip of the bacteria. To test our theory, we performed experiments with isolated M. xanthus cells on agar substrates of varying stiffness. Over the whole range of substrate stiffness here investigated, the measured gliding speeds are found to be in good agreement with the predictions from our elasto-capillary-hydrodynamic model. The physical mechanisms of mechanosensitivity we propose serve as an important step towards an accurate theory of friction and substrate-mediated interaction between bacteria in a swarm of cells proliferating in soft media (5).Myxobacteria | gliding motility | mechanosensitivity | lubrication | elasto-capillary-hydrodynamics

Pectin Induced Colony Expansion of Soil-Derived Flavobacterium Strains

“…However following this stage, colonies rapidly expanded and after 22 h, the fluorescent signal of colonies grown on pectin surpassed both the control (without sugar amendment) and the glucose and other amended compounds, after 36 h (according to Student T -test test). Plates coated with polyethylene glycol (PEG8000) served as an additional control to rule out mechanosensitivity associated with substrate stiffness ( Tchoufag et al, 2019 ), since its viscosity is similar to that of pectin. Colony expansion on Peg8000 was similar to the DDW control without amended sugars, suggesting that effects were specific to pectin.…”

Three-Dimensional Observations of an Aperiodic Oscillatory Gliding Behavior in Myxococcus xanthus Using Confocal Interference Reflection Microscopy

“…This could perhaps be demonstrated by the use of fine graphite particles, scanning electron microscopy, or atomic force microscopy, which are all effective in revealing the otherwise invisible slime secretions. A recent study by Tchoufag et al proposed an elastohydrodynamic mechanism for bacterial gliding where a sinusoidal basal shape is adopted when myxobacteria glide upon a soft substrate (56). This was observed using membrane-stained gliding cells on semisolid agar pads with TIRF microscopy and revealed distinct foci where the cell membrane was lifted approximately 100 nm above the substrate surface (outside the TIRF evanescent field).…”

Methods to Evaluate Bacterial Motility and Its Role in Bacterial–Host Interactions

“…Sliding 0.3-0.4%, or 1-2% has also been used [37,38] Gliding ≤7% in Myxococcus xanthus [39] 1 The plate is inoculated at the bottom of the media instead of the top.…”