Unforeseen swimming and gliding mode of an insect gut symbiont, Burkholderia sp. RPE64, with wrapping of the flagella around its cell body

Abstract

A bean bug symbiont, Burkholderia sp. RPE64, selectively colonizes the gut crypts by flagella-mediated motility: however, the mechanism for this colonization remains unclear. Here, to obtain clues to this mechanism, we characterized the swimming motility of the Burkholderia symbiont under an advanced optical microscope. High-speed imaging of cells enabled the detection of turn events with up to 5-ms temporal resolution, indicating that cells showed reversal motions (θ ~ 180°) with rapid changes in speed by a factor of 3.6. Remarkably, staining of the flagellar filaments with a fluorescent dye Cy3 revealed that the flagellar filaments wrap around the cell body with a motion like that of a ribbon streamer in rhythmic gymnastics. A motility assay with total internal reflection fluorescence microscopy revealed that the left-handed flagellum wound around the cell body and propelled it forward by its clockwise rotation. We also detected periodic-fluorescent signals of flagella on the glass surface, suggesting that flagella possibly contacted the solid surface directly and produced a gliding-like motion driven by flagellar rotation. Finally, the wrapping motion was also observed in a symbiotic bacterium of the bobtail squid, Aliivibrio fischeri, suggesting that this motility mode may contribute to migration on the mucus-filled narrow passage connecting to the symbiotic organ.

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

“…We next determined flagellar structure and function, simultaneously, using TIRFM [10, 21, 22]. We found that a cell attached to the glass surface can rotate its flagellar filament freely, by treating coverslips with poly-L-lysine and BSA.…”

“…Polar flagellated bacteria show flagellar polymorphic change from a normal to curly state in the single polar, flagellated species Pseudomonas spp, [47, 48] and from normal to coiled state for Rhodobacter sphaeroides [49]. A novel type of flagellar wrapping motion has recently been observed in the single polar, flagellated species Shewanella putrefaciens [11], multiple polar flagellated bacteria such as Allivibrio fischeri, Burkholderia insecticola, and P. putida [10, 50], and bipolar flagellated bacteria such as Helicobacter suis [51] and Magnetospirillum magneticus AMB-1 [52]. These bacteria reverse their direction of motion by the transition from CCW rotation of left-handed normal filaments into CW rotation of right-handed coiled filaments to escape from being trapped in structured environments.…”

“…Carbon-coated electron microscope grids were glow-discharged with a hydrophilic treatment device (PIB-10; Vacuum Device) [10, 22]. Cells in buffer B were placed on the grid and incubated for 10 min at room temperature.…”

“…Additionally, cells of V. alginolyticus change their swimming direction by ∼90° due to a buckling instability of their straight hook (flick). Recently, a novel type of chemotactic behavior has been discovered, where the right-handed flagellum wraps around the cell body and propels the cell forward by its CW rotation [10, 11].…”

Bacterial predation under changing viscosities

“…Cell shape however (B. bacteriovorus HD100 and M. aeruginosavorus are comma shaped, while B. bacteriovorus is rod shaped) appears to little change cell propulsion (Constantino et al, 2016). Finally, it was recently shown that polar flagella can wrap around the cell when this becomes trapped or is found in a viscous medium, with the type of macromolecule affecting the rate of transition from the normal state to the wrapped, coiled state, changing swimming behavior (Kühn et al, 2017;Kinosita et al, 2018).…”