eDNA-stimulated cell dispersion from Caulobacter crescentus biofilms upon oxygen limitation is dependent on a toxin–antitoxin system

In their natural environment, most bacteria preferentially live as complex surface-attached multicellular colonies called biofilms. Biofilms begin with a few cells adhering to a surface, where they multiply to form a mature colony. When conditions deteriorate, cells can leave the biofilm. This dispersion is thought to be an important process that modifies the overall biofilm architecture and that promotes colonization of new environments. In Caulobacter crescentus biofilms, extracellular DNA (eDNA) is released upon cell death and prevents newborn cells from joining the established biofilm. Thus, eDNA promotes the dispersal of newborn cells and the subsequent colonization of new environments. These observations suggest that eDNA is a cue for sensing detrimental environmental conditions in the biofilm. Here, we show that the toxin–antitoxin system (TAS) ParDE(4) stimulates cell death in areas of a biofilm with decreased O(2) availability. In conditions where O(2) availability is low, eDNA concentration is correlated with cell death. Cell dispersal away from biofilms is decreased when parDE(4) is deleted, probably due to the lower local eDNA concentration. Expression of parDE(4) is positively regulated by O(2) and the expression of this operon is decreased in biofilms where O(2) availability is low. Thus, a programmed cell death mechanism using an O(2)-regulated TAS stimulates dispersal away from areas of a biofilm with decreased O(2) availability and favors colonization of a new, more hospitable environment.