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

Murray J Tipping,Karine A Gibbs,Matthew R Parsek

doi:10.1371/journal.ppat.1007885

Abstract

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.

Highlights

IntroductionLiving in a community can provide benefits to each individual
Several examples of kin discrimination in bacteria have been elegantly described, including those mediated by Type IV [4], Type VI [5, 6], and Type VII [7] secretion system based effector exchange, contact-dependent inhibition (CDI) [8, 9], and the MafB toxins of the Neisseria [10]
Given the lack of lethality and the stark attenuation of swarm colony expansion observed during Ids-mediated territorial exclusion [15, 17], we hypothesized that an Ids mismatch caused broad changes in gene expression of the recipient cell

Summary

Introduction

Living in a community can provide benefits to each individual. A stable evolutionary strategy is for individuals to preferentially direct advantages to close kin [1,2,3]. This behavior, known as kin discrimination, has been the subject of focused study. One common thread between these systems is that they characterize discrimination as immediate antagonism towards cells or strains that are non-kin, typically through delivery of lethal toxin effector molecules. Upon effector delivery, receiving cells must either neutralize it by presenting a cognate anti-toxin or suffer immediate negative consequences, typically cell death [5] or permanent inhibition of growth [8]. We describe an expansion of these mechanisms: the Ids self-recognition system mediates kin discrimination in Proteus mirabilis by selectively inducing non-self cells into a growth-arrested lifestyle incompatible with social behavior, thereby controlling access to that behavior

Methods

Results

Conclusion