Bacillus subtilis Swarmer Cells Lead the Swarm, Multiply, and Generate a Trail of Quiescent Descendants.
Bacteria adopt social behavior to expand into new territory, led by specialized swarmers, before forming a biofilm. Such mass migration of Bacillus subtilis on a synthetic medium produces hyperbranching dendrites that transiently (equivalent to 4 to 5 generations of growth) maintain a cellular monolayer over long distances, greatly facilitating single-cell gene expression analysis. Paradoxically, while cells in the dendrites (nonswarmers) might be expected to grow exponentially, the rate of swarm expansion is constant, suggesting that some cells are not multiplying. Little attention has been paid to which cells in a swarm are actually multiplying and contributing to the overall biomass. Here, we show in situ that DNA replication, protein translation and peptidoglycan synthesis are primarily restricted to the swarmer cells at dendrite tips. Thus, these specialized cells not only lead the population forward but are apparently the source of all cells in the stems of early dendrites. We developed a simple mathematical model that supports this conclusion.



Swarming motility enables rapid coordinated surface translocation of a microbial community, preceding the formation of a biofilm. This movement occurs in thin films and involves specialized swarmer cells localized to a narrow zone at the extreme swarm edge. In the B. subtilis system, using a synthetic medium, the swarm front remains as a cellular monolayer for up to 1.5 cm. Swarmers display high-velocity whirls and vortexing and are often assumed to drive community expansion at the expense of cell growth. Surprisingly, little attention has been paid to which cells in a swarm are actually growing and contributing to the overall biomass. Here, we show that swarmers not only lead the population forward but continue to multiply as a source of all cells in the community. We present a model that explains how exponential growth of only a few cells is compatible with the linear expansion rate of the swarm.
Institut de Biologie Physico-Chimique, UMR 8261, CNRS-Université Paris Diderot, Paris, France.
Lina
L
Hamouche
Institut de Biologie Physico-Chimique, UMR 8261, CNRS-Université Paris Diderot, Paris, France.
Soumaya
S
Laalami
Matière et Systèmes Complexes, UMR 7057, CNRS-Université Paris Diderot, Paris, France.
Adrian
A
Daerr
Matière et Systèmes Complexes, UMR 7057, CNRS-Université Paris Diderot, Paris, France.
Solène
S
Song
Institute for Integrative Biology of the Cell, UMR 8621, CNRS-University Paris-Sud, Orsay, France.
I Barry
IB
Holland
Institute for Integrative Biology of the Cell, UMR 8621, CNRS-University Paris-Sud, Orsay, France.
Simone J
SJ
Séror
Lebanese University, Faculty of Science, Section 1, Beirut, Lebanon.
Kassem
K
Hamze
Institut de Biologie Physico-Chimique, UMR 8261, CNRS-Université Paris Diderot, Paris, France putzer@ibpc.fr.
Harald
H
Putzer
D001412:Bacillus subtilis / Q000254:growth & development*; D003470:Culture Media / Q000737:chemistry; D004261:DNA Replication; D008962:Models, Theoretical; D010457:Peptidoglycan / Q000096:biosynthesis; D014176:Protein Biosynthesis
D003470:Culture Media; D010457:Peptidoglycan