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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

Tension-mediated pili cooperativity.The correlation of bacterial instantaneous crawling speed u and the tension in the filaments F/ks for ‘two-legged crawling’ with rotationally flexible TFP. The TFP configuration in various parts of the diagram are illustrated above: If pili are not antiparallel, they can relax the tension by reorientation and the cell motion is slow and persistent. In the HTAPC the tension cannot be relaxed resulting in either obstructed tug-of-war configuration or a fast ‘sling shot’ jump if one of the pili is released. The parameter values are KRel = 130 s−1, KAd = 5 s−1 (corresponding to 〈NB〉 = 1.7), ka = 10−14 and ν = π/8.
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f5: Tension-mediated pili cooperativity.The correlation of bacterial instantaneous crawling speed u and the tension in the filaments F/ks for ‘two-legged crawling’ with rotationally flexible TFP. The TFP configuration in various parts of the diagram are illustrated above: If pili are not antiparallel, they can relax the tension by reorientation and the cell motion is slow and persistent. In the HTAPC the tension cannot be relaxed resulting in either obstructed tug-of-war configuration or a fast ‘sling shot’ jump if one of the pili is released. The parameter values are KRel = 130 s−1, KAd = 5 s−1 (corresponding to 〈NB〉 = 1.7), ka = 10−14 and ν = π/8.

Mentions: The tension-mediated cooperative action of TFP is illustrated in Fig. 5 where crawling sequences were isolated from the full trajectories. Each point on the diagram represents a translocation event in the simulation. The instantaneous speed u during the translocation is plotted against the tension in the filaments F/ks. The distinct types of two-legged motion are illustrated above: if picked at random, a likely configuration is that on the left-hand side with two bound TFP pointing into different directions. In such a state the two bound TFP retract by depolymerization which can potentially increase their tension. Assuming that pili cell-attachments are flexible, allowing for free rotation of TFP around them (see Fig. 6), the accompanying stress in the filaments can be relaxed by rotating relative to the cell axis, which results in slow and persistent motion of the cell with relatively small tension in the filaments. Bacteria spend most of the time in this mode. If a pilus is released in such a state, no jump is observed, since there is not enough tension in the filaments. If, however, the cell persists long enough in the slow mode, it moves down the lower branch of points on the speed-tension plot on Fig. 5, reaching an almost antiparallel pili configuration, and then it becomes difficult to relax the tension in the filaments by re-orientation - as the TFP are now puling into opposite directions. This (at the right-hand side of the lower branch) is the so-called high tension antiparallel configuration, HTAPC, indicative of the obstructed motion phase. At this stage, the probability for a pilus release increases - leading to the fast jump, i.e. hopping to the upper branch of the plot in Fig. 5.


Emergence of complex behavior in pili-based motility in early stages of P. aeruginosa surface adaptation
Tension-mediated pili cooperativity.The correlation of bacterial instantaneous crawling speed u and the tension in the filaments F/ks for ‘two-legged crawling’ with rotationally flexible TFP. The TFP configuration in various parts of the diagram are illustrated above: If pili are not antiparallel, they can relax the tension by reorientation and the cell motion is slow and persistent. In the HTAPC the tension cannot be relaxed resulting in either obstructed tug-of-war configuration or a fast ‘sling shot’ jump if one of the pili is released. The parameter values are KRel = 130 s−1, KAd = 5 s−1 (corresponding to 〈NB〉 = 1.7), ka = 10−14 and ν = π/8.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

f5: Tension-mediated pili cooperativity.The correlation of bacterial instantaneous crawling speed u and the tension in the filaments F/ks for ‘two-legged crawling’ with rotationally flexible TFP. The TFP configuration in various parts of the diagram are illustrated above: If pili are not antiparallel, they can relax the tension by reorientation and the cell motion is slow and persistent. In the HTAPC the tension cannot be relaxed resulting in either obstructed tug-of-war configuration or a fast ‘sling shot’ jump if one of the pili is released. The parameter values are KRel = 130 s−1, KAd = 5 s−1 (corresponding to 〈NB〉 = 1.7), ka = 10−14 and ν = π/8.
Mentions: The tension-mediated cooperative action of TFP is illustrated in Fig. 5 where crawling sequences were isolated from the full trajectories. Each point on the diagram represents a translocation event in the simulation. The instantaneous speed u during the translocation is plotted against the tension in the filaments F/ks. The distinct types of two-legged motion are illustrated above: if picked at random, a likely configuration is that on the left-hand side with two bound TFP pointing into different directions. In such a state the two bound TFP retract by depolymerization which can potentially increase their tension. Assuming that pili cell-attachments are flexible, allowing for free rotation of TFP around them (see Fig. 6), the accompanying stress in the filaments can be relaxed by rotating relative to the cell axis, which results in slow and persistent motion of the cell with relatively small tension in the filaments. Bacteria spend most of the time in this mode. If a pilus is released in such a state, no jump is observed, since there is not enough tension in the filaments. If, however, the cell persists long enough in the slow mode, it moves down the lower branch of points on the speed-tension plot on Fig. 5, reaching an almost antiparallel pili configuration, and then it becomes difficult to relax the tension in the filaments by re-orientation - as the TFP are now puling into opposite directions. This (at the right-hand side of the lower branch) is the so-called high tension antiparallel configuration, HTAPC, indicative of the obstructed motion phase. At this stage, the probability for a pilus release increases - leading to the fast jump, i.e. hopping to the upper branch of the plot in Fig. 5.

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