A field guide to bacterial swarming motility

Abstract

How bacteria regulate, assemble and rotate flagella to swim in liquid media is reasonably well understood. Much less is known about how some bacteria use flagella to move over the tops of solid surfaces in a form of movement called swarming. The focus of bacteriology is changing from planktonic to surface environments, and so interest in swarming motility is on the rise. Here, I review the requirements that define swarming motility in diverse bacterial model systems, including an increase in the number of flagella per cell, the secretion of a surfactant to reduce surface tension and allow spreading, and movement in multicellular groups rather than as individuals.

Figure 1. Bacteria move by a range of mechanisms

Swarming is multicellular surface movement powered by rotating helical flagella. Swimming is individual movement in liquid powered by rotating flagella. Twitching is surface movement powered by the extension and retraction of pili. Gliding is active surface movement that does not require flagella or pili and involves focal adhesion complexes. Sliding is passive surface translocation powered by growth and facilitated by a surfactant. The direction of cell movement is indicated by a gray arrow and the motors that power the movement are indicated by colored circles.

Figure 2. Phylogenetic distribution of swarming motility

A Bacterial phylogeny based on the 16S rRNA gene. Species names in colored text indicate the presence of swarming motility. Species names in black text indicate bacteria for which swarming motility has not yet been demonstrated. Trees generated by Dr. Dave Kysela from 1547 aligned positions using the neighbor joining algorithm on distances determined under the HKY85+I+G substitution model in PAUP* v4.0b10. Scale bar corresponds to a distance of 0.1 substitutions per site.

Figure 3. Rafting

A) A timelapse series of images of a raft of B. subtilis cells moving in a swarming monolayer. Images cropped from movie S3 published in reference¹¹. B) Images of elongated P. mirabilis cells swarming as a large raft in a catheter. Panels taken from figure 3 of reference¹³⁷. See also reference²⁶.

Figure 4. Surfactants

Swarming bacteria use chemically distinct secreted surfactants to spread over solid surfaces. Polymyxin B is an antibiotic that is included here for comparison to the swarming surfactants.

Figure 5. Swarming lag

A) A lag precedes active swarming of B. subtilis when bacteria are transferred from broth culture to a solid surface (open circles). The lag is abolished if actively swarming cells are re-inoculated onto a fresh surface (closed circles). Data reproduced from reference¹¹. B) The lag period of B. subtilis decreases with increasing cell density whether broth grown (open circles) or actively swarming cells (closed circles) are used as inoculum when saturating amounts of purified surfactant are added to the plates prior to inoculation.

Figure 6. Cell filaments and cell chains

B. subtilis mutant cells are compared using phase contrast and fluorescence microscopy (membrane dye FM4-64, false colored red). Chains of cells (from a swrA mutant) have regular septa whereas filaments (from a minJ mutant) do not.

Figure 7. Swarming pattern formation

Featureless: Bacillus subtilis 3610, Bull's eye: Proteus mirabilis PM7002 (generous gift of Phil Rather, Emory University). Dendritic: Pseudomonas aeruginosa PA14 (generous gift of George O'Toole, Dartmouth College). Vortex: Paenibacillus vortex V (generous gift of Rivka Rudner, Hunter College). A non-swarming mutant and subsequent suppressor in Bacillus subtilis 3610. Uncolonized agar appears black and bacterial biomass is white.