Limits...
Emergence of complex behavior in pili-based motility in early stages of P. aeruginosa surface adaptation

View Article: PubMed Central - PubMed

ABSTRACT

Pseudomonas aeruginosa move across surfaces by using multiple Type IV Pili (TFP), motorized appendages capable of force generation via linear extension/retraction cycles, to generate surface motions collectively known as twitching motility. Pseudomonas cells arrive at a surface with low levels of piliation and TFP activity, which both progressively increase as the cells sense the presence of a surface. At present, it is not clear how twitching motility emerges from these initial minimal conditions. Here, we build a simple model for TFP-driven surface motility without complications from viscous and solid friction on surfaces. We discover the unanticipated structural requirement that TFP motors need to have a minimal amount of effective angular rigidity in order for cells to perform the various classes of experimentally-observed motions. Moreover, a surprisingly small number of TFP are needed to recapitulate movement signatures associated with twitching: Two TFP can already produce movements reminiscent of recently observed slingshot type motion. Interestingly, jerky slingshot motions characteristic of twitching motility comprise the transition region between different types of observed crawling behavior in the dynamical phase diagram, such as self-trapped localized motion, 2-D diffusive exploration, and super-diffusive persistent motion.

No MeSH data available.


Related in: MedlinePlus

Kinetic Monte Carlo simulations.(a) Examples of processes that bacteria can undergo in a KMC simulation step (black line: surface bound pilus, grey line: free pilus). Below is a sketch of a pilus eminating from the cell pole with the visualization of the two elastic terms. (b) The energy landscapes illustrating how the switching rate from a depolymerizing (dep) to a polymerizing (pol) state depends on the stretching tension (top) and how the pulling force on the pilus increases the rate of release from the surface KRel.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC5385500&req=5

f2: Kinetic Monte Carlo simulations.(a) Examples of processes that bacteria can undergo in a KMC simulation step (black line: surface bound pilus, grey line: free pilus). Below is a sketch of a pilus eminating from the cell pole with the visualization of the two elastic terms. (b) The energy landscapes illustrating how the switching rate from a depolymerizing (dep) to a polymerizing (pol) state depends on the stretching tension (top) and how the pulling force on the pilus increases the rate of release from the surface KRel.

Mentions: We designed a multiscale model of P. aeruginosa twitching motility linking the microscopic pili-based mechanisms with the macroscopic properties of bacterial trajectories. The cell is treated as a rigid rod-like body with 12 pili (the number is chosen in accordance with available experiments540) emanating from one of its poles5404142. The pili point to various directions, with equilibrium angles ϕeq that are randomly chosen from a Gaussian distribution with variance ν: . TFP length changes in time: it is governed by the action of the molecular motors that add or remove pilin monomers resulting in TFP elongation or retraction. The pili are attached to the motor at the cell surface via a flexible hook, while their other end is either free or bound to the surface in a non-specific way (Fig. 2a). In the experiments3, it was established that surface-bound pili predominantly retract - bound pili polymerization was observed only under high tension. However, free pili were observed to equally elongate and retract53443. In line with these observations, we assume that each pilus can be in one of the two modes and that the probability of switching between the elongation and retraction depends on the tension in the filament, which is schematically illustrated in Fig. 2b and detailed in the Methods section. The free pili retract or elongate with a rate 0.8 μm/s based on Skerker and Berg5 and the bound TFP retract with a rate 0.7 μm/s34. Here, we assume that this is also their elongation rate. TFP can shrink to zero length and disappear, however, the total number of pili is conserved and such events are followed by a “birth” of a new pilus in a random direction chosen from the distribution (in another system, of N. gonorrhoeae, it was suggested that there is orientational memory in new pili distribution for explaining directional twitching of bacteria that are assumed to be of spherical symmetry).


Emergence of complex behavior in pili-based motility in early stages of P. aeruginosa surface adaptation
Kinetic Monte Carlo simulations.(a) Examples of processes that bacteria can undergo in a KMC simulation step (black line: surface bound pilus, grey line: free pilus). Below is a sketch of a pilus eminating from the cell pole with the visualization of the two elastic terms. (b) The energy landscapes illustrating how the switching rate from a depolymerizing (dep) to a polymerizing (pol) state depends on the stretching tension (top) and how the pulling force on the pilus increases the rate of release from the surface KRel.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC5385500&req=5

f2: Kinetic Monte Carlo simulations.(a) Examples of processes that bacteria can undergo in a KMC simulation step (black line: surface bound pilus, grey line: free pilus). Below is a sketch of a pilus eminating from the cell pole with the visualization of the two elastic terms. (b) The energy landscapes illustrating how the switching rate from a depolymerizing (dep) to a polymerizing (pol) state depends on the stretching tension (top) and how the pulling force on the pilus increases the rate of release from the surface KRel.
Mentions: We designed a multiscale model of P. aeruginosa twitching motility linking the microscopic pili-based mechanisms with the macroscopic properties of bacterial trajectories. The cell is treated as a rigid rod-like body with 12 pili (the number is chosen in accordance with available experiments540) emanating from one of its poles5404142. The pili point to various directions, with equilibrium angles ϕeq that are randomly chosen from a Gaussian distribution with variance ν: . TFP length changes in time: it is governed by the action of the molecular motors that add or remove pilin monomers resulting in TFP elongation or retraction. The pili are attached to the motor at the cell surface via a flexible hook, while their other end is either free or bound to the surface in a non-specific way (Fig. 2a). In the experiments3, it was established that surface-bound pili predominantly retract - bound pili polymerization was observed only under high tension. However, free pili were observed to equally elongate and retract53443. In line with these observations, we assume that each pilus can be in one of the two modes and that the probability of switching between the elongation and retraction depends on the tension in the filament, which is schematically illustrated in Fig. 2b and detailed in the Methods section. The free pili retract or elongate with a rate 0.8 μm/s based on Skerker and Berg5 and the bound TFP retract with a rate 0.7 μm/s34. Here, we assume that this is also their elongation rate. TFP can shrink to zero length and disappear, however, the total number of pili is conserved and such events are followed by a “birth” of a new pilus in a random direction chosen from the distribution (in another system, of N. gonorrhoeae, it was suggested that there is orientational memory in new pili distribution for explaining directional twitching of bacteria that are assumed to be of spherical symmetry).

View Article: PubMed Central - PubMed

ABSTRACT

Pseudomonas aeruginosa move across surfaces by using multiple Type IV Pili (TFP), motorized appendages capable of force generation via linear extension/retraction cycles, to generate surface motions collectively known as twitching motility. Pseudomonas cells arrive at a surface with low levels of piliation and TFP activity, which both progressively increase as the cells sense the presence of a surface. At present, it is not clear how twitching motility emerges from these initial minimal conditions. Here, we build a simple model for TFP-driven surface motility without complications from viscous and solid friction on surfaces. We discover the unanticipated structural requirement that TFP motors need to have a minimal amount of effective angular rigidity in order for cells to perform the various classes of experimentally-observed motions. Moreover, a surprisingly small number of TFP are needed to recapitulate movement signatures associated with twitching: Two TFP can already produce movements reminiscent of recently observed slingshot type motion. Interestingly, jerky slingshot motions characteristic of twitching motility comprise the transition region between different types of observed crawling behavior in the dynamical phase diagram, such as self-trapped localized motion, 2-D diffusive exploration, and super-diffusive persistent motion.

No MeSH data available.


Related in: MedlinePlus