Research Article
26 March 2020

Coexistence of Two Chiral Helices Produces Kink Translation in Spiroplasma Swimming

ABSTRACT

The mechanism underlying Spiroplasma swimming is an enigma. This small bacterium possesses two helical shapes with opposite-handedness at a time, and the boundary between them, called a kink, travels down, possibly accompanying the dual rotations of these physically connected helical structures, without any rotary motors such as flagella. Although the outline of dynamics and structural basis has been proposed, the underlying cause to explain the kink translation is missing. We here demonstrated that the cell morphology of Spiroplasma eriocheiris was fixed at the right-handed helix after motility was stopped by the addition of carbonyl cyanide 3-chlorophenylhydrazone (CCCP), and the preferential state was transformed to the other-handedness by the trigger of light irradiation. This process coupled with the generation and propagation of the artificial kink, presumably without any energy input through biological motors. These findings indicate that the coexistence of two chiral helices is sufficient to propagate the kink and thus to propel the cell body.
IMPORTANCE Many swimming bacteria generate a propulsion force by rotating helical filaments like a propeller. However, the nonflagellated bacteria Spiroplasma spp. swim without the use of the appendages. The tiny wall-less bacteria possess two chiral helices at a time, and the boundary called a kink travels down, possibly accompanying the dual rotations of the helices. To solve this enigma, we developed an assay to determine the handedness of the body helices at the single-wind level, and demonstrated that the coexistence of body helices triggers the translation of the kink and that the cell body moves by the resultant cell bend propagation. This finding provides us a totally new aspect of bacterial motility, where the body functions as a transformable screw to propel itself forward.

INTRODUCTION

Many bacteria swim by rotating a thin helical filament, the flagellum, like a propeller to generate a propulsion force, and this marvelous nanomachine has been thoroughly studied by researchers for decades (1). Yet, can any other bacteria swim without this rotary motor?
Spiroplasma spp. are wall-less bacteria that swim in viscous media and infect a wide range of plants and insects (2, 3). Their propulsion, in contrast to the rotary motion of bacterial flagella, is generated by waves of helical transformation. They present two helical shapes, one right-handed and the other left-handed, simultaneously along their body axis. When the boundary between these helices, called a kink, travels down the length of the cell, one helical structure is forcibly unwound and thus rotates in one direction, while the other is wound and thus rotates in the reverse manner to cancel out the torques (4). These dual rotations within two helical structures can produce a propulsion force in the same direction (Fig. 1a) (57). The ability to maintain this distinct morphology is defined by internal cytoskeletal filaments that span the shortest helical path along the body helix, which is composed of the assembly of fibril proteins and possibly the actin homolog MreB (8, 9). One simple model to explain the reversal of body helicity during swimming is the structural change in the internal cytoskeletal filaments (10, 11). However, it remains unclear what triggers the translation of the kink.
FIG 1
FIG 1 Kink propagation and reversal of the handedness of the body helix during migration. (a) Schematic. (b) Sequential micrographs of a single migrating cell in the vicinity of the glass. The cell shapes, bending to the left and right upward along the body axis, define RH and LH in our experimental setup (see more detail in Fig. S2). Purple arrowheads indicate the positions of the kink. (c) Kink diagram of panel b. The kink position from the lagging pole of the cell was plotted. (d) A kink diagram for 6 s. KinkR→L and kinkL→R are defined as the kink generated at the cell pole of RH and at that of LH, respectively. (e) Histograms of the time that the cell stays only LH (blue) and only RH (red), respectively. The solid line shows the fit of double exponential decay with two parameters, n = const1 · exp(−t1) − const2 exp(−t2). The dashed line in the RH-only histogram shows the fit of single exponential decay, n = const · exp(−t/τ), where τ is estimated to be 0.27 s. Dwell times between the attainment of the kink to the rear end and the emergence of the next kink at the front end, distributed in a stochastic manner with single or double exponential functions. (f) Histograms of the time interval from kinkR→L to kinkL→R (LH only in panels d and e) and from kinkL→R to kinkR→L (RH only in panels d and e) generated at the leading pole of the cell. The line shows the Gaussian distribution. The average and its standard deviation (SD) were plotted in each panel.
Here, we use Spiroplasma eriocheiris, a pathogen of Chinese mitten crab (12), and report that its characteristic morphology is artificially fixed to be right-handed helix (RH) or left-handed helix (LH). We demonstrated that RH morphology is deformed to be LH by light irradiation, and we visualized that the process couples to the emergence and subsequent propagation of a kink. Partial photoinduced manipulation indicates that the coexistence of two helical structures is sufficient to propel the cell forward, and the dynamic deformation in the cell helicity is stimulated by the connection of two conformational states.

RESULTS

The assay to determine the helicity of moving Spiroplasma body at the single wind level.

The helical shape of Spiroplasma is recognized as a series of slanted segments at the defocus image plane to the cell axis under phase-contrast microscopy (see Fig. S1 in the supplemental material). Although temporal observation revealed that the cell helicity could invert during swimming (4), the absolute handedness of the body helix has not been technically determined because of the ambiguity of the position of the focal plane (13). To observe single cells and kink translation in detail, we developed an assay that keeps the cell position at the same image plane. When the sample chamber was pretreated with bovine serum albumin, the cell moved at the same image plane near the glass surface, typically >10 s (Movies S1 and S2). In this migration mode, some regions of the cell surface may interact with the glass. However, the cell movements remained coupled with the kink translation, and, most notably, the parameters of cell movement near the surface were the same as those that were free swimming (Fig. S2). From these observations, we judged that the interaction did not disturb the proper swimming motility. Thus, our experimental system can successfully quantify the handedness of a body helix at any time.
We here set three criteria for the presentation of micrographs: cells moving close to the bottom glass were observed, all images were captured under an inverted microscope as “mirror” images on the camera, and the focal plane was fixed slightly below the cell (position i in Fig. S1b). Using this framework, the cell helicity was uniquely determined from the direction of the slanted segment relative to the helical axis (Fig. 1b): northwest and northeast arrows represent the structures of the right-handed helix (RH) and the left-handed helix (LH), respectively, when the cell body is aligned north to south. As reported in reference 13, the helicity reverses at the kink without exception (n = 30 in observations for >10 s). The angle of the cell bend at the kink was 126° ± 13° (n = 30 cells). By analyzing sequential images, we constructed a graphic representation, called a kink diagram, of the time course of the spatial position of the kink along the body axis measured from the cell pole, highlighting the absolute handedness of the body helix with different color codes (Fig. 1c and d). The speed of the kink was estimated from the slopes of the diagrams as 13.8 ± 2.3 μm/s. The parameters of the kink have a similar distribution to those in related species of Spiroplasma melliferum (4) and Spiroplasma citri (14). Although dwells between the attaining of the kink to the rear pole and the emergence of the next kink at the leading pole distributed in a stochastic manner with single- or double-exponential functions (Fig. 1e), histograms of time intervals between the kink emergence at the front pore showed peaks (Fig. 1f). These analyses suggest that the kink intervals include the certain time for the kink to pass through the whole cell body at a constant speed, and the attaining somehow triggers the emergence of the kink with an unknown mechanism, presumably through distortion of cytoskeletons penetrating the whole cell body. These features are good agreements with the previous measurement in S. melliferum (4), whereas S. eriocheiris mostly showed only one kink at a time in one cell.

Finding of two independent conditions to fix the body helicity in the reverse manner.

We found two independent conditions under which we could fix the body helicity. First, when the proton motive force was depleted by adding carbonyl cyanide 3-chlorophenylhydrazone (CCCP), a conventional uncoupler, the kink did not emerge anymore, and thus, the cell motility was completely stopped within a few seconds (Fig. 2a). Notably, the handedness of the body helix represented RH without exception (Fig. 2b, left). This may imply that the role of the energy input is to facilitate the transition from the elementary RH morphology to the biased LH as reported in references 9 and 15, whereas the molecular bases responsible for the chemomechanical coupling are still unknown. Second, when we applied strong-light irradiation to the cells in the presence of the fluorescent dye for cell membranes FM4-64, the cells also prohibited the alternation of helicity (Fig. 2a and c and Movie S3). This is presumably caused by damage to the membrane or proteins caused by the reactive oxygen species (ROS) that light irradiation to the dye produced (16, 17). The inhibitory effect of ROS on the kink formation and propagation has been previously suggested in S. melliferum (18). Unexpectedly, the body helicity was LH (Fig. 2b, right), which is the opposite of the case with CCCP. This light irradiation did not significantly damage the cell because the stopped cell started swimming again about 1 h after the irradiation. We measured the pitch angles for both helices under an optical microscope and found no apparent difference (Fig. 2d). Electron microscopy (EM) observation confirmed that the helical morphology did not present any obvious difference between two inhibitions (Fig. S3). These data show that the inhibitions strongly affect the stability of cell morphology at the preferential handedness with an inherent pitch angle of the body helix.
FIG 2
FIG 2 Handedness of body helix stabilized in cells that have stopped moving. (a) Average swimming speed after motility inhibition treatment. (b) Helical morphology under phase-contrast microscopy. Arrows present the directions of slanted portions of the cell relative to the helical axis. Scale bar, 1 μm. (c) Experimental setup of the motility inhibition by light irradiation to the cell. BP, band-pass filter; DM, dichroic mirror. (d) Apparent pitch angle of cell shapes. (d, top) Schematic of the definition of the angle. (Bottom) Histogram of the pitch angle.

Photoinduced switch of the body helicity.

Next, we applied these two inhibitions sequentially to the same cells; CCCP-treated cells were subsequently exposed to light irradiation in the presence of FM4-64. Remarkably, the cells immediately changed their shape from RH to LH in less than 0.5-s light irradiation by the current setup; see more detail in Materials and Methods (Fig. 3a and Movie S4). This morphological transition accompanied the emergence of the kink at one pole, and the kink was translated to the other pole at a speed of 10.2 ± 1.6 μm/s, which is of the same order as with swimming cells (Fig. 3b and c). Its one-way translation induced the cell propulsion (Movie S4), whereas the kink emerged only once, as schematized in Fig. 3d. Note that the helical morphology was not changed when we looked at the same cell before and after light illumination (Fig. S4). On the basis of these observations, we conclude that the RH conformation fixed by CCCP is still reversible and can be switched to LH simply by light irradiation, presumably without any apparent energy inputs through biological molecular motors.
FIG 3
FIG 3 Photoinduced switch of the handedness of the body helix. (a) Single-cell images under phase-contrast microscopy. Cell was pretreated with CCCP and FM4-64 and was then submitted to strong-light irradiation. The irradiation was turned on at 2.69 s. Scale bar, 1 μm. (b) Kink diagram of the cell in panel a and Movie S4. (c) Speed of kink propagation. (d) Schematic illustration of the processive change in body helicity induced by light irradiation. RH and LH morphologies are represented by red and blue lines, respectively.

Artificial coexistence of two helicities by partial-light irradiation.

To get more insights into the mechanism underlying the kink translation, we modified the excitation system of a conventional microscope to set a small iris (Fig. 4a) and then applied the photoinduced switch with partial-light illumination to the same cell twice (Fig. 4b). With the first irradiation targeting the bottom region of the cell, a single kink immediately emerged and moved to the pole within the illuminated region (Movie S5). This process was repeated several times (3 to 14 s) (shown in Fig. 4c), indicating that the coexistence of two chiral helices is sufficient to translate the kink. With the second irradiation targeting the larger part of the cell (14 s) (shown in Fig. 4c), the kink still emerged, but the direction of translation was the opposite, i.e., the kink moved to the pole within the unilluminated region, which originally represented RH (Fig. 4c and d). This is the first evidence that a kink can potentially propagate in both directions and that the composition of the chiral conformation in helicity might determine its translation direction. In the above successive partial irradiations, the speed of the kink translation and the frequency of kink generation were decreased to be 35% to 70% and 15% to 25%, respectively, of the values in native motility mode (Fig. 4e).
FIG 4
FIG 4 Kink propagation induced by partial-light irradiation. (a) Diagram of partial-light irradiation at cell edge. (b) Single-cell images under phase-contrast microscopy. The partial light was applied to the lower part represented by the green boxed areas in panels c and d. Scale bars, 1 μm. (c) Kink diagram of the cell in panel a and Movie S5. (d) Schematic illustration of the effect of partial-light irradiation. (e) Speed and frequency of kink propagation.

Paired kinks induced by spotlight irradiation.

We applied spotlight irradiation only to the center part of the cell; the area of irradiation was a similar size to the pitch of the body helix (Fig. 5a and Movie S6). The spotlight irradiation induced a morphological change starting at the center part of the cell as a sharp bend and propagating to the rest of the cell repeatedly (Fig. 5b). This sharp bend was not defined as a kink because the bend was connected with two apparent RH forms. The speed and frequency of the sharp bend were similar to those of the kink in the partial-light experiment (Fig. 5), whereas the angle of the sharp bend was measured to be 61° ± 21° from micrographs (Fig. 5e). We interpret that the bend consists of the paired kinks. With this formation, the helicity was reversed twice in the limited area and thus returned to the original helicity (Fig. 5f). The acute angle coincides with an estimated value of [180 − 2 × (θRH − θLH)] = 64°, where θRH and θLH are the pitch angles of RH and LH, respectively, assuming that the two parallel, thick filaments similar to fibril ribbons are arranged around the innermost line of the body helix (8) with a constant pitch angle of ±29° (Fig. S5) (4, 7). Therefore, the propagation of the cell bend is triggered by the insertion of a small fragment of left-handed conformation, as in the case of the kink.
FIG 5
FIG 5 Kink propagation induced by spotlight irradiation. (a) Diagram of spotlight irradiation. Single-cell images under phase-contrast microscopy are shown. The middle region of the cell was irradiated by spotlight illumination in the presence of FM4-64 and CCCP. The data are from Movie S6. (b) Angle at cell bend. (c) “Cell bend” diagram. The light-illuminated region is shown in green. (d) Speed and frequency of cell bend position. (e, left) Schematic illustration of the effect of spotlight irradiation. (Right) Sharp cell bend explained by helical compositions.

DISCUSSION

Our observations provide two clues about the swimming mechanism with the artificial kink formation (Fig. 3 and 5). First, when two helices are forcibly set in one Spiroplasma cell, the kink appears at the boundary to cancel out the two opposite torsions in two helicities having a physical connection. The emergence of the paired kinks by spotlight irradiation also supports the above idea because two kinks are needed in which both ends are fixed in the same helix under the boundary condition (Fig. 5). Second, the kink travels down, perhaps without any apparent energy sources, once it emerges. The direction of kink propagation is determined by the composition of the two helices (Fig. 4b and c). It implies that the propagation is purely mechanical. The time constant required for the conformational change of a single cytoskeletal monomer is calculated as 1/(400 monomers/μm × 14 μm/s) = 0.2 ms based on the speed of the translation and the periodicity of the cytoskeletal structure (19, 20).
ATP hydrolysis drives their cell motility in the wall-less bacterium Mycoplasma mobile (21), and it is also implied to be required for the motility in Spiroplasma (18, 22). On the other hand, we showed in this study that cell motility was completely stopped after adding CCCP, suggesting that membrane potential may be the driving force behind the motility. But we could not rule out the possibility that ATP hydrolysis drives the motility. The concentration of the inhibitor used here is 50 times higher than that for inhibition of bacterial flagellar rotation (23), and this may cause adverse effects on the multiple cellular processes.
What is the difference between the natural swimming mode and the artificial kink formation induced by light irradiation? Here, we hypothesize the existence of a “twistase” at the leading pole of Spiroplasma. It perhaps functions to reverses the helicity of the small region of cytoskeletons and holds the distortion in the natural swimming mode. Once this situation happens, the kink spontaneously emerges at the leading pole, and it passively travels down until it attains to the rear pole. Alternatively, since the cell has a tapered pole (19), this tip structure may function as a molecular modulator that locally controls the coexistence of two conformational states. Notably, the helical transformation observed here is reminiscent of the polymorphism of bacterial flagella (24, 25). Likewise, this tiny helical bacterium provides us a totally new ingenious mechanism that humans never invented, by which the body functions as a transformable screw to propel itself forward.

MATERIALS AND METHODS

Bacterial strains and culture conditions.

The type strain, TDA-040725-5T, of S. eriocheiris was grown in R2 medium (2.5% [wt/vol] heart infusion broth, 8% sucrose, and 15% newborn calf serum) at 30°C to an optical density of 0.06 to 0.1 at 600 nm (12).

Optical microscopy and data analyses.

Cells were visualized under an inverted microscope (IX73; Olympus) equipped with 100× lens objectives (UPLFLN 100×O2PH, 1.3 numerical aperture; Olympus), a high-speed charge-coupled-device (CCD) camera system (VCC-H1600; Digimo), and an optical table (HAX0806; JVI). Projection of the image to the camera was made at 67 nm per pixel. Sequential images of cells were captured as 8-bit images with a camera under 10-ms resolution and converted into a sequential TIF file without any compression. All data were analyzed by ImageJ 1.48v (http://rsb.info.nih.gov/ij/) and its plugins. For the kink diagram, the position of the kink, which is clearly defined by the direction of the slanted portions of RH and LH, was plotted.

Motility assay.

Cells were centrifuged at 12,000 × g for 4 min and suspended with motility buffer (MB) (75 mM sodium phosphate [pH 7.3], 68 mM NaCl, 235 mM sucrose, and 0.25% methylcellulose) at 10-fold the density of the culture. The following procedures were performed at room temperature (RT) unless otherwise noted. Cells were poured into a tunnel chamber assembled by taping a coverslip as previously described (26). The coverslip was pretreated with 20% (wt/vol) bovine serum albumin (BSA) in MB before use. Cells were then observed within 20 min.

Inhibition of cell motility.

Cell motility was inhibited by two different methods. For inhibition by an uncoupler of the proton motive force, the medium in the sample chamber described above was replaced by 500 μM carbonyl cyanide 3-chlorophenylhydrazone (CCCP), and the remaining cells on the glass surface were observed. For inhibition by light irradiation, cells were subjected to a strong blue light in the presence of FM4-64. The cells were suspended in MB containing 50 μM FM4-64 and poured into the chamber, as described above. Green light from a mercury lamp (U-HGLGPS; Olympus) was separately irradiated onto the specimen on the sample stage of a microscope from the lens objective with a filter set (excitation, FF01-531/40, and dichroic mirror, FF593-Di03; Semrock) (Fig. 2c). Green light illumination was controlled by an electronic shutter (SSH-C4B; Sigma Koki). The intensity of the green light was measured to be 2 × 107 W/m2 on the sample stage through an objective lens, as previously described (26). For the partial and spot illuminations, an iris diaphragm and a pinhole were set at the conjugative position of the sample plane (Fig. 4a and 5a).

Electron microscopy.

Samples bound to the grids were stained with ammonium molybdate and observed by transmission electron microscopy, as previously described (26). Carbon film-coated EM grids, which were glow discharged by a polybutene (PIB)-10 hydrophilic treatment device (vacuum device) before use. The following procedures were performed at RT unless otherwise noted. Cells suspended in MB without methylcellulose at 10-fold the density of the culture were put on the grid. After incubation for 5 min, the cells were chemically fixed with 1% (vol/vol) glutaraldehyde in MB for 10 min. After washing three times with buffer consisting of 10 mM Tris-HCl, pH 7.2, the cells were stained with 3% ammonium molybdate and air dried. Samples were observed under a transmission electron microscope (JEM-1400; JEOL) at 100 kV. The EM images were captured by a CCD camera.

Data availability.

The data that support the findings of this study are available from the corresponding author upon reasonable request.

ACKNOWLEDGMENTS

We thank W. Wang for supplying the bacterial strain.
This study was supported in part by KAKENHI grants from the Japan Society for the Promotion of Science (no. JP15H01329 and JP16H06230 to D.N. and JP16H00808, JP87003306, and JP15H04364 to T.N.).
D.N. and T.N. designed the research. D.N. and T.I. performed the experiments. D.N., T.I., and T.N. performed the data analyses. D.N. and T.N. wrote the paper.
We declare no competing financial interests.

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Published In

Journal of Bacteriology cover image
Journal of Bacteriology
Volume 202Number 826 March 2020
eLocator: e00735-19
Editor: Ann M. Stock, Rutgers University-Robert Wood Johnson Medical School
PubMed: 32041794

History

Received: 27 November 2019
Accepted: 31 January 2020
Published online: 26 March 2020

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KEYWORDS

  1. cell polarity
  2. cytoskeleton
  3. helical shape
  4. motility
  5. video microscopy

Contributors

Authors

Department of Physics, Gakushuin University, Tokyo, Japan
Tatsuro Ito
Department of Physics, Gakushuin University, Tokyo, Japan
Takayuki Nishizaka
Department of Physics, Gakushuin University, Tokyo, Japan

Editor

Ann M. Stock
Editor
Rutgers University-Robert Wood Johnson Medical School

Notes

Address correspondence to Daisuke Nakane, [email protected], or Takayuki Nishizaka, [email protected].
Daisuke Nakane and Tatsuro Ito contributed equally to this work. Author order was determined by seniority.

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