Peer pressure from a Proteus mirabilis self-recognition system controls participation in cooperative swarm motility

by Murray J. Tipping, Karine A. Gibbs

Colonies of the opportunistic pathogen Proteus mirabilis can distinguish self from non-self: in swarming colonies of two different strains, one strain excludes the other from the expanding colony edge. Predominant models characterize bacterial kin discrimination as immediate antagonism towards non-kin cells, typically through delivery of toxin effector molecules from one cell into its neighbor. Upon effector delivery, receiving cells must either neutralize it by presenting a cognate anti-toxin as would a clonal sibling, or suffer cell death or irreversible growth inhibition as would a non-kin cell. Here we expand this paradigm to explain the non-lethal Ids self-recognition system, which stops access to a social behavior in P. mirabilis by selectively and transiently inducing non-self cells into a growth-arrested lifestyle incompatible with cooperative swarming. This state is characterized by reduced expression of genes associated with protein synthesis, virulence, and motility, and also causes non-self cells to tolerate previously lethal concentrations of antibiotics. We show that temporary activation of the stringent response is necessary for entry into this state, ultimately resulting in the iterative exclusion of non-self cells as a swarm colony migrates outwards. These data clarify the intricate connection between non-lethal recognition and the lifecycle of P. mirabilis swarm colonies.