Linear motor driven-rotary motion of a membrane-permeabilized ghost in Mycoplasma mobile

Kinosita, Yoshiaki; Miyata, Makoto; Nishizaka, Takayuki

doi:10.1038/s41598-018-29875-9

Cited by 20 publications

(15 citation statements)

References 33 publications

(56 reference statements)

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“…S2 in the supplemental material). A previous study shows that the ghosts of M. mobile exhibit directed rotational motility around the membrane protrusion driven by the linear motion of the legs (34). In contrast, the rotary motion in M. gallisepticum seems to be driven by thermal fluctuation because it has no regularity of rotational direction (see Fig.…”

Section: Discussionmentioning

confidence: 93%

“…In these experiments, M. mobile cells were permeabilized with Triton X-100 and stopped for gliding. Gliding was then reactivated by the addition of ATP (32)(33)(34). In contrast, the reactivation of permeabilized cells of M. pneumoniaetype gliding mycoplasmas has not been successful so far (6).…”

Section: Resultsmentioning

confidence: 99%

“…The gliding motility of M. mobile is driven by ATP using a "gliding ghost," which has a permeabilized membrane and can be reactivated by the addition of ATP (32)(33)(34). In contrast, the direct energy source for M. pneumoniae-type gliding motility is still unclear (6).…”

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confidence: 99%

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Behaviors and Energy Source of Mycoplasma gallisepticum Gliding

Mizutani

Miyata

2019

J Bacteriol

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Mycoplasma gallisepticum, an avian-pathogenic bacterium, glides on host tissue surfaces by using a common motility system with Mycoplasma pneumoniae. In the present study, we observed and analyzed the gliding behaviors of M. gallisepticum in detail by using optical microscopes. M. gallisepticum glided at a speed of 0.27 ± 0.09 μm/s with directional changes relative to the cell axis of 0.6 degree ± 44.6 degrees/5 s without the rolling of the cell body. To examine the effects of viscosity on gliding, we analyzed the gliding behaviors under viscous environments. The gliding speed was constant in various concentrations of methylcellulose but was affected by Ficoll. To investigate the relationship between binding and gliding, we analyzed the inhibitory effects of sialyllactose on binding and gliding. The binding and gliding speed sigmoidally decreased with sialyllactose concentration, indicating the cooperative binding of the cell. To determine the direct energy source of gliding, we used a membrane-permeabilized ghost model. We permeabilized M. gallisepticum cells with Triton X-100 or Triton X-100 containing ATP and analyzed the gliding of permeabilized cells. The cells permeabilized with Triton X-100 did not show gliding; in contrast, the cells permeabilized with Triton X-100 containing ATP showed gliding at a speed of 0.014 ± 0.007 μm/s. These results indicate that the direct energy source for the gliding motility of M. gallisepticum is ATP. IMPORTANCE Mycoplasmas, the smallest bacteria, are parasitic and occasionally commensal. Mycoplasma gallisepticum is related to human-pathogenic mycoplasmas—Mycoplasma pneumoniae and Mycoplasma genitalium—which cause so-called “walking pneumonia” and nongonococcal urethritis, respectively. These mycoplasmas trap sialylated oligosaccharides, which are common targets among inﬂuenza viruses, on host trachea or urinary tract surfaces and glide to enlarge the infected areas. Interestingly, this gliding motility is not related to other bacterial motilities or eukaryotic motilities. Here, we quantitatively analyze cell behaviors in gliding and clarify the direct energy source. The results provide clues for elucidating this unique motility mechanism.

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Section: Discussionmentioning

confidence: 93%

Section: Resultsmentioning

confidence: 99%

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Behaviors and Energy Source of Mycoplasma gallisepticum Gliding

Mizutani

Miyata

2019

J Bacteriol

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“…The flow chamber was composed of two coverslips (no. 1, 0.12–0.17 mm thickness, Matsunami Glass) with different sizes (18 × 18 and 24 × 36 mm) [23, 24]. The 24×36 mm cover glass was glow-discharged with a hydrophilic treatment device (PIB-10; Vacuum Device) to clean its surface.…”

Section: Methodsmentioning

confidence: 99%

Distinct chemotactic behavior in the originalEscherichia coliK-12 depending on forward-and-backward swimming, not on run-tumble movements

Kinosita

Ishida

Yoshida

et al. 2020

Preprint

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Most motile bacteria are propelled by rigid, helical, flagellar filaments and display distinct swimming patterns to explore their favorable environments. Escherichia coli cells have a reversible rotary motor at the base of each filament. They exhibit a run-tumble swimming pattern, driven by switching of rotatory direction which causes polymorphic flagellar transformation. Here we report a novel swimming mode in E. coli ATCC10798, which is one of the original K-12 clones. High-speed tracking of single ATCC10798 cells showed forward and backward swimming with an average turning angle of 150°. The flagellar helicity remained right-handed with a 1.3 μm pitch and 0.14 μm helix radius, which is assumed to be a curly type, regardless of motor switching; the flagella of ATCC10798 did not show polymorphic transformation. The torque and rotational switching of the motor was almost identical to the E. coli W3110 strain, which is a derivative of K-12 and a wild-type for chemotaxis. The single point mutation of N87K in FliC, one of the filament subunits, is critical to the change in flagellar morphology and swimming pattern, and lack of flagellar polymorphism. E. coli cells expressing FliC(N87K) sensed ascending a chemotactic gradient in liquid but did not form rings on a semi-solid surface. Based on these findings, we propose a flagellar polymorphism-dependent migration mechanism in structured environments.

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“…A single colony was inoculated on a 0.25% (wt/vol) T-broth soft-agar plate and incubated at 30 °C for 7 h. Cell motility was evaluated according to the colony's diameter by Image J 1.45 s (https ://rsb.info.nih.gov/ij/). 59,60 . The 24 × 36 mm cover glass was glow-discharged with a hydrophilic treatment device (PIB-10; Vacuum Device) to clean its surface.…”

Section: Motility Assay On Soft-agar Platesmentioning

confidence: 99%

Distinct chemotactic behavior in the original Escherichia coli K-12 depending on forward-and-backward swimming, not on run-tumble movements

Kinosita

Ishida

Yoshida

et al. 2020

Sci Rep

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Most motile bacteria are propelled by rigid, helical, flagellar filaments and display distinct swimming patterns to explore their favorable environments. Escherichia coli cells have a reversible rotary motor at the base of each filament. They exhibit a run-tumble swimming pattern, driven by switching of the rotational direction, which causes polymorphic flagellar transformation. Here we report a novel swimming mode in E. coli ATCC10798, which is one of the original K-12 clones. High-speed tracking of single ATCC10798 cells showed forward and backward swimming with an average turning angle of 150°. The flagellar helicity remained right-handed with a 1.3 μm pitch and 0.14 μm helix radius, which is consistent with the feature of a curly type, regardless of motor switching; the flagella of ATCC10798 did not show polymorphic transformation. The torque and rotational switching of the motor was almost identical to the E. coli W3110 strain, which is a derivative of K-12 and a wild-type for chemotaxis. The single point mutation of N87K in FliC, one of the filament subunits, is critical to the change in flagellar morphology and swimming pattern, and lack of flagellar polymorphism. E. coli cells expressing FliC(N87K) sensed ascending a chemotactic gradient in liquid but did not spread on a semi-solid surface. Based on these results, we concluded that a flagellar polymorphism is essential for spreading in structured environments.

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Linear motor driven-rotary motion of a membrane-permeabilized ghost in Mycoplasma mobile

Cited by 20 publications

References 33 publications

Behaviors and Energy Source of Mycoplasma gallisepticum Gliding

Behaviors and Energy Source of Mycoplasma gallisepticum Gliding

Distinct chemotactic behavior in the originalEscherichia coliK-12 depending on forward-and-backward swimming, not on run-tumble movements

Distinct chemotactic behavior in the original Escherichia coli K-12 depending on forward-and-backward swimming, not on run-tumble movements

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