Bacterial acrobatics on a surface: swirling packs, collisions, and reversals during swarming.

Swarming is a particular type of motility that is promoted by flagella and allows bacteria to move rapidly over and between surfaces and through viscous environments. Swarming must confer considerable survival benefit, as a heterogeneous group of bacteria exhibit this form of motility, including strains of Aeromonas, Azospirillum, Bacillus, Burkholderia, Chromobacterium, Clostridium, Escherichia coli, Photobacterium, Proteus, Pseudomonas, Rhizobium, Rhodospirillum, Salmonella, Serratia, Vibrio, and Yersinia (reviewed in references 7 and 19). Although swarming has been described for a long time (8; reviewed in reference 9) and the number of bacterial species known to swarm is increasing, surprisingly little is known about the dynamics or mechanics of swarming cells. This is beginning to change. Swarming collective behavior has significant consequences with respect to bacterial colonization strategies in the environment and in hosts (reviewed in reference 19); moreover, the population behavior of the swarm and the performance of individuals in the swarm provide attractive models for physicists and mathematicians studying group dynamics and self-organizing systems (3, 11, 14, 17). In this issue of Journal of Bacteriology and in other recent work from Howard Berg’s laboratory at the Rowland Institute, sophisticated visualization of swarming Escherichia coli cells provides some new and fascinating insights into the phenomenon of swarming (4, 18, 21). Although diverse types of bacteria exhibit a range of swarming proficiencies, swarm cells are usually (but not always) hyperflagellated and long in comparison to the cell type adapted for swimming in liquid environments (reviewed in reference 6). For example, Proteus mirabilis spectacularly increases its flagellar number, from fewer than 10 to up to 5,000, and its length, from 1 to 2 m to 20 to 80 m, upon differentiation from the swimmer to the swarm cell type (reviewed in reference 20). E. coli swarm cell differentiation is more modest: flagellar number and cell length increase 2to 3-fold (7a). The zone at the edge of an expanding swarm colony is a thin layer of highly motile cells, many of which seem to move together in packs and whirls (14–16). Looking at these vigorously swirling cells prompts numerous questions, many of which have been posed for a long time (e.g., see references 10 and 15). Why are there so many flagella? What do they do? Can a sole bacterium swarm or does it need the pack? How do swarming cells accommodate their neighbor’s copious numbers of filaments? Do the swarm cells use each other’s filaments to coordinate movement and/or generate thrust? How does a swarm colony advance? What patterns of movement and kinds of acrobatics are observed during swarming? Phase-contrast and fluorescence video microscopy studies are providing some answers to these questions. Individual bacteria can be tracked, and fluorescently labeled flagella allow direct observation of the flagellar movement during swarming. Turner and colleagues used conjugated Alexa Fluor dyes to visualize flagella (18), while Copeland et al. also recently labeled the flagella of swarming cells in another way, by using biarsenical dyes (2). Using these techniques, some old questions are put to rest—as highlighted below—and some new ones can now be addressed. Figure 1 shows a phase-contrast image of cells in a swarm from a tracking video, accompanied by a computer display in which the heading of each cell is indicated by the color of a line running from its head to tail (4, 18). Movement between layers. Movement on surfaces requires a fluid environment (17). As in swimming, flagellar bundles propel the swarm cell forward; in fact, the speed of translocation of a swarm cell is similar to the swimmer’s speed ( 40 m per s) (4, 18). However, Zhang et al. (21) noticed that the straight trajectory of a swarming cell is markedly different from the curving path observed for bacteria swimming close to a glass surface (12). It seems that the swarm cell’s path is straight because the torque generated at the subsurface (agar-fluid interface) is counteracted by the torque generated at the airfluid interface, i.e., the swarm cell is moving in a fluid environment between 2 surfaces. This was shown for E. coli by demonstrating that small smoke particles floating on the surface of a swarm diffuse only locally—they remain nearly stationary as the cells swarm underneath (21). Thus, swarming occurs between 2 stationary layers. Presumably, some sort of immobile surfactant layer that functions to preserve or promote wetness covers the fluid layer where swarming motility occurs. The nature of the E. coli surfactant is unknown. Maneuvers in the swarm. Turner et al. (18) observed four kinds of maneuvers during swarming: forward, essentially straight movement; stalling, which occurs mostly at the advancing edge; lateral movement, which is often caused by collisions with neighboring cells; and reversals. The reversing maneuver is quite amazing: the cell body backs up through its flagellar bundle, and the tail becomes the head. This feat is accomplished when the flagellar motors reverse and the filaments transition from their normal helical shape to the curly polymorphism and then relax again to the normal shape. Such an acrobatic maneuver is unique and probably highly suited to movement in constrained circumstances. Movement in the pack. Videos of swarming cells can be viewed online at http://www.rowland.harvard.edu/labs/bacteria /movies_swarmecoli.html. Movies of swarming E. coli and other bacteria have also been captured by the Weibel lab at the * Mailing address: Microbiology Department, The University of Iowa, Iowa City, IA 52242. Phone and fax: (319) 335-9721. E-mail: [email protected]. Published ahead of print on 30 April 2010.