Swarming and complex pattern formation in Paenibacillus vortex studied by imaging and tracking cells.
BACKGROUND
Swarming motility allows microorganisms to move rapidly over surfaces. The Gram-positive bacterium Paenibacillus vortex exhibits advanced cooperative motility on agar plates resulting in intricate colonial patterns with geometries that are highly sensitive to the environment. The cellular mechanisms that underpin the complex multicellular organization of such a simple organism are not well understood.


RESULTS
Swarming by P. vortex was studied by real-time light microscopy, by in situ scanning electron microscopy and by tracking the spread of antibiotic-resistant cells within antibiotic-sensitive colonies. When swarming, P. vortex was found to be peritrichously flagellated. Swarming by the curved cells of P. vortex occurred on an extremely wide range of media and agar concentrations (0.3 to 2.2% w/v). At high agar concentrations (> 1% w/v) rotating colonies formed that could be detached from the main mass of cells by withdrawal of cells into the latter. On lower percentage agars, cells moved in an extended network composed of interconnected "snakes" with short-term collision avoidance and sensitivity to extracts from swarming cells. P. vortex formed single Petri dish-wide "supercolonies" with a colony-wide exchange of motile cells. Swarming cells were coupled by rapidly forming, reversible and non-rigid connections to form a loose raft, apparently connected via flagella. Inhibitors of swarming (p-Nitrophenylglycerol and Congo Red) were identified. Mitomycin C was used to trigger filamentation without inhibiting growth or swarming; this facilitated dissection of the detail of swarming. Mitomycin C treatment resulted in malcoordinated swarming and abortive side branch formation and a strong tendency by a subpopulation of the cells to form minimal rotating aggregates of only a few cells.


CONCLUSIONS
P. vortex creates complex macroscopic colonies within which there is considerable reflux and movement and interaction of cells. Cell shape, flagellation, the aversion of cell masses to fuse and temporary connections between proximate cells to form rafts were all features of the swarming and rotation of cell aggregates. Vigorous vortex formation was social, i.e. required > 1 cell. This is the first detailed examination of the swarming behaviour of this bacterium at the cellular level.
Ingham
Colin J
CJ
Department of Medical Microbiology and Infection Control, Jeroen Bosch Hospital,'s-Hertogenbosh, The Netherlands. colin.ingham@wur.nl
Ben Jacob
Eshel
E
D000362:Agar; D000900:Anti-Bacterial Agents / Q000494:pharmacology; D018441:Biofilms / Q000254:growth & development*; D003224:Congo Red / Q000494:pharmacology; D004352:Drug Resistance, Microbial; D016936:Gram-Positive Endospore-Forming Bacteria / Q000187:drug effects / Q000502:physiology* / Q000648:ultrastructure; D008124:Locomotion / Q000187:drug effects; D008855:Microscopy, Electron, Scanning; D016685:Mitomycin / Q000494:pharmacology; D009578:Nitrobenzenes / Q000494:pharmacology; D019384:Nucleic Acid Synthesis Inhibitors / Q000494:pharmacology
D000900:Anti-Bacterial Agents; D009578:Nitrobenzenes; D019384:Nucleic Acid Synthesis Inhibitors; D003224:Congo Red; C016014:4-nitrophenylglycerol; D016685:Mitomycin; D000362:Agar