Multiple Pilus Motors Cooperate for Persistent Bacterial Movement in Two Dimensions

Holz, Claudia; Opitz, Dirk; Greune, Lilo; Kurre, Rainer; Koomey, Michael; Schmidt, M. Alexander; Maier, Berenike

doi:10.1103/physrevlett.104.178104

Cited by 56 publications

(138 citation statements)

References 15 publications

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“…This finding was more notable in the magnified view (Fig. 5E, Inset), proving that the twitching motility was activated randomly with an apparent diffusion coefficient of 1.2 μm 2 /s, which is good agreement with the scaling behavior of the motility in other bacteria (26,27). The start point of the parabolic line indicates the phase transition to directed twitching motility as a result of the negative phototaxis.…”

Section: Resultssupporting

confidence: 72%

Asymmetric distribution of type IV pili triggered by directional light in unicellular cyanobacteria

Nakane

Nishizaka

2017

Proc. Natl. Acad. Sci. U.S.A.

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The type IV pili (T4P) system is a supermolecular machine observed in prokaryotes. Cells repeat the cycle of T4P extension, surface attachment, and retraction to drive twitching motility. Although the properties of T4P as a motor have been scrutinized with biophysics techniques, the mechanism of regulation remains unclear. Here we provided the framework of the T4P dynamics at the single-cell level in Synechocystis sp. PCC6803, which can recognize light direction. We demonstrated that the dynamics was detected by fluorescent beads under an optical microscope and controlled by blue light that induces negative phototaxis; extension and retraction of T4P was activated at the forward side of lateral illumination to move away from the light source. Additionally, we directly visualized each pilus by fluorescent labeling, allowing us to quantify their asymmetric distribution. Finally, quantitative analyses of cell tracking indicated that T4P was generated uniformly within 0.2 min after blue-light exposure, and within the next 1 min the activation became asymmetric along the light axis to achieve directional cell motility; this process was mediated by the photo-sensing protein, PixD. This sequential process provides clues toward a general regulation mechanism of T4P system, which might be essentially common between archaella and other secretion apparatuses.Synechocystis sp. PCC6803 | twitching motility | phototaxis | signal transduction | fluorescence T ype IV pili (T4P) are fascinating supermolecular machines that drive twitching motility, protein secretion, and DNA uptake in prokaryotes (1). Twitching motility is now widely accepted as a form of bacterial translocation involving repetition of the cycle of extension and retraction of the pili (2, 3) (Fig. 1A), which is powered by assembly and disassembly ATPase at the base of helical pilus fibers (4). The mechanical response of a single pilus has been scrutinized in great detail using biophysical approaches such as optical tweezers methodology in Neisseria gonorrheae (3, 5-7), although the dynamic properties resulting from the response to various environmental signals remain less understood than those of bacterial flagella. T4P is also evolutionarily and structurally related to flagella in archaea, which have recently been designated archaella (8-11). Although newly developed techniques enable us to examine the dynamic properties of the machinery, little is known about the regulation mechanism of T4P because tens of components cooperate to orchestrate the dynamics of both the archaella and T4P system. Such complexity hampers the design of an experimental setup with quantitative and reproducible evaluations.To address how the T4P system is activated or repressed by environmental signals over a short timescale, we here used Synechocystis sp. PCC6803, a model cyanobacteria (12)(13)(14). This species exhibits T4P-dependent twitching motility on surfaces such as soft-agar plates at speeds of a few micrometers per minute, and the cell motility direction is regulated both posi...

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Section: Resultssupporting

confidence: 72%

Asymmetric distribution of type IV pili triggered by directional light in unicellular cyanobacteria

Nakane

Nishizaka

2017

Proc. Natl. Acad. Sci. U.S.A.

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“…1a). No biochemical mechanism coordinating their retraction is known, yet the quantitative analysis of bacterial trajectories provides clear evidence for the cooperation of multiple pili 15 . These observations suggested that the coordination of multiple pilus motors may be mediated mechanically via a tug-of-war of pilus motors pulling in different directions 15 .…”

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confidence: 99%

“…No biochemical mechanism coordinating their retraction is known, yet the quantitative analysis of bacterial trajectories provides clear evidence for the cooperation of multiple pili 15 . These observations suggested that the coordination of multiple pilus motors may be mediated mechanically via a tug-of-war of pilus motors pulling in different directions 15 . Furthermore, diplococci (pairs of bacteria) were observed to align and meander in micro-topographic grooves, consistent with a tug-of-war between pili on either side of the bacterium 33 .…”

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confidence: 99%

“…Furthermore, diplococci (pairs of bacteria) were observed to align and meander in micro-topographic grooves, consistent with a tug-of-war between pili on either side of the bacterium 33 . Moreover, type IV pili fulfil several prerequisites of a tug-of-war mechanism: the persistence time of the motion increases with the number of pili present on the cell surface and the average unbinding force is by an order of magnitude lower than the maximum force that one pilus can generate 15 . The latter feature is a key requirement for a tug-of-war mechanism 8 , and enables pili to pull other pili off the surface.…”

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confidence: 99%

“…In this study, we use a combined theoretical and experimental approach and introduce a two-dimensional tug-of-war model for the twitching motility of Neisseria gonorrhoeae 15 . Twitching is a mechanism for bacterial motility along a surface driven by type IV pili [16][17][18][19][20] , micron-sized polymeric cell appendages that play a role not only in motility but also in cell-cell adhesion, cell-surface adhesion and horizontal gene transfer [20][21][22] .…”

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confidence: 99%

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Bacterial twitching motility is coordinated by a two-dimensional tug-of-war with directional memory

et al. 2014

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Type IV pili are ubiquitous bacterial motors that power surface motility. In peritrichously piliated species, it is unclear how multiple pili are coordinated to generate movement with directional persistence. Here we use a combined theoretical and experimental approach to test the hypothesis that multiple pili of Neisseria gonorrhoeae are coordinated through a tug-of-war. Based on force-dependent unbinding rates and pilus retraction speeds measured at the level of single pili, we build a tug-of-war model. Whereas the one-dimensional model robustly predicts persistent movement, the two-dimensional model requires a mechanism of directional memory provided by re-elongation of fully retracted pili and pilus bundling. Experimentally, we confirm memory in the form of bursts of pilus retractions. Bursts are seen even with bundling suppressed, indicating re-elongation from stable core complexes as the key mechanism of directional memory. Directional memory increases the surface range explored by motile bacteria and likely facilitates surface colonization.

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Three‐Dimensional Obstacles for Bacterial Surface Motility

Meel

Kouzel

Oldewurtel

et al. 2011

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Multiple Pilus Motors Cooperate for Persistent Bacterial Movement in Two Dimensions

Cited by 56 publications

References 15 publications

Asymmetric distribution of type IV pili triggered by directional light in unicellular cyanobacteria

Asymmetric distribution of type IV pili triggered by directional light in unicellular cyanobacteria

Bacterial twitching motility is coordinated by a two-dimensional tug-of-war with directional memory

Three‐Dimensional Obstacles for Bacterial Surface Motility

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