Swarming bacteria undergo localized dynamic phase transition to form stress-induced biofilms

Swarming and biofilm formation are two modes of bacterial collective behavior that enable cells to increase their tolerance to anti-microbial stressors. Swarming is a rapid type of surface colonization, and therefore its ability to withstand high antibiotic concentrations could lead to the subsequent establishment of highly resilient biofilms in regions that could not otherwise have been colonized. However, whether swarms can transit into biofilm at all, and how, remains unclear. Using Bacillus subtilis, we reveal that a biophysical mechanism, reminiscent of motility-induced phase separation (MIPS), underpins a swarming-to-biofilm transition through a localized dynamic phase transition. Guided by the MIPS paradigm, we demonstrate that the transition is triggered by environmental stressors such as an antibiotic gradient or even a simple physical barrier. Based on the biophysical insight, we propose a promising strategy of antibiotic treatment to effectively inhibit the transition from swarms to biofilms, by targeting the localized phase transition. The biophysical origin of such a transition suggests that biophysics-based approaches could emerge as a potential tool to control and understand collective stress response in bacterial communities. Significance StatementBacteria can organize in different types of communities to better tolerate stresses taking advantage of novel properties that lack in the planktonic state. Here we show that bacterial swarms, characterized by a rapid group motility on a surface, can use a biophysical mechanism resembling motility induced phase separation to transit into biofilms, a more resistant form of bacterial collectives. The transition is promoted by a slowing down in the swarm expansion, leading to the subsequent accumulation of multiple layers of bacteria near the swarming front. Such accumulation results in large inhomogeneities in cell density which triggers wrinkle formation, the morphological feature of biofilms. Our data suggest that wrinkle formation can be inhibited can be inhibited by locally targeting the swarming front, where the phase transition takes place.