Large-Scale Vortices with Dynamic Rotation Emerged from Monolayer Collective Motion of Gliding Flavobacteria

Abstract

A collective motion of self-driven particles has been a fascinating subject in physics and biology. Sophisticated macroscopic behavior emerges through a population in thousands or millions of bacterial cells, propelling itself by flagellar rotation and its chemotactic response. Here we found a series of collective motions accompanying successive phase-transitions in a non-flagellated rod-shaped soil bacterium, Flavobacterium johnsoniae , which was driven by a surface cell movement known as gliding motility. When we spot the cells on an agar plate with a low level of nutrients, the bacterial community exhibited vortex patterns that spontaneously appeared as lattice and integrated into a large-scale circular plate. All patterns exhibit with monolayer of bacteria, which enable to visualize an individual cell with a high resolution among a wide-range pattern two-dimensionally. The single cells moved at random orientation, but the cells connected with one another showed left-turn biased trajectories in starved environment. This feature is possibly due to the collision of cells inducing a nematic alignment of dense cells as self-propelled rods. Subsequently, each vortex oscillated independently, and then transformed to the rotating mode as an independent circular plate. Notably, the rotational direction of the circular plate was counterclockwise without exception. The plates developed accompanying rotation with constant angular velocity, suggesting that the mode is an efficient strategy for bacterial survival. Importance Self-propelled bacteria propelled by flagella rotation often display highly organized dynamic patterns at high cell densities. Here we found a new mode of collective motion in non-flagellated bacteria: vortex patterns were spontaneously appeared as lattice and integrated into a large-scale circular plate comprising hundreds of thousands of cells, which exhibited unidirectional rotation in a counterclockwise manner and expanded in size on agar. A series of collective motions was driven by gliding motility of the rod-shaped soil bacterium Flavobacterium johnsoniae . In a low nutrient environment, single cells moved at random orientation while cells at high density moved together as a unitary cluster. This might be an efficient strategy for cells of this species to find nutrients.

Design Principles of the Rotary Type 9 Secretion System

“…It has long been known that F. johnsoniae forms spreading colonies on agar plates ( Wolkin and Pate, 1984 ; Gorski et al, 1993 ). A recent study showed that the cells at high density are connected with one another and that in a starved environment they move in counterclockwise trajectories ( Nakane et al, 2021 ). A F. johnsoniae swarm exhibits a vortex pattern that spontaneously appears as a lattice that is integrated into a large-scale circular plate ( Figure 3A ).…”

“…This two-dimensional pattern possibly appears due to the collision of cells and it further induces a nematic alignment of dense cells ( Sumino et al, 2012 ). It is hypothesized that swarm behavior of T9SS driven Bacteroidetes may be involved in survival strategies and the efficient search of nutrients ( Figure 3C ; Nakane et al, 2021 ). A three-dimensional spherical microcolony was recently studied in a microfluidic device and it was reported that this biofilm-like microcolony self-assembles by the gliding motility ( Li et al, 2021 ).…”

The dgc2 gene encoding di-guanylate cyclase suppresses both motility and biofilm formation in the filamentous cyanobacterium Leptolyngbya boryana

“…It is made available under a preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in The copyright holder for this this version posted January 11, 2022. ; https://doi.org/10.1101/2022.01.10.475764 doi: bioRxiv preprint direction (Student's t-test, p << 0.01). Interestingly, Flavobacterium johnsoniae was also recently shown to perform gliding motility and vortex formation with the CCW preference (6). It shows a CCW trajectory even from the singlecell state, and remains unified in the CCW direction while rotating as a group, but moves in the CW direction just before it stops its rotation.…”

“…Although the distribution of probability density for median perturbation angle and duration showed no significant difference in the distribution of median perturbation angle between CCW and CW (Mardia-Watson-Wheeler test, p = 0.6369), the duration of the CCW direction was statistically longer than that of the CW direction (Student's t-test, p << 0.01). Interestingly, Flavobacterium johnsoniae was also recently shown to perform gliding motility and vortex formation with the CCW preference (6). It shows a CCW trajectory even from the singlecell state, and remains unified in the CCW direction while rotating as a group, but moves in the CW direction just before it stops its rotation.…”

Cell motility greatly empowers bacterial contact weapons

“…Using a variety of different molecular appendages, they move by sliding, gliding, twitching and swimming (10). However, it is surface-associated motility mechanisms such as gliding motility or Type IV pilus-based twitching motility that are most commonly used when cells are at the high cell densities where contact-based weapons are effective (11, 12). Consistent with this, these conditions are also closely associated with the expression of T6SS (13) and CDI genes (14).…”