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Peer pressure from a Proteus mirabilis self-recognition system controls participation in cooperative swarm motility
Murray J Tipping1, Karine A Gibbs1
1Department of Molecular and Cellular Biology, Harvard University, Cambridge, Massachusetts, United States of America.
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.
Insights
Proteus mirabilis colonies distinguish self from non-self using a non-lethal system. This system temporarily arrests non-kin cells, preventing their participation in cooperative swarming behavior.
Area of Science:
- Microbiology
- Bacterial behavior
- Social interactions in bacteria
Background:
- Proteus mirabilis is an opportunistic pathogen.
- Bacterial kin discrimination models typically involve lethal antagonism via toxin delivery.
- Existing models do not fully explain non-lethal self-recognition systems.
Purpose of the Study:
- To elucidate the non-lethal Ids self-recognition system in Proteus mirabilis.
- To understand how this system mediates exclusion of non-self cells from swarming colonies.
- To connect non-lethal recognition mechanisms to the lifecycle of P. mirabilis swarm colonies.
Main Methods:
- Observational studies of swarming colonies of different P. mirabilis strains.
- Analysis of gene expression changes in non-self cells induced into a growth-arrested state.
- Investigation of the role of the stringent response in mediating this non-lethal recognition.
Main Results:
- P. mirabilis employs a non-lethal self-recognition system (Ids) to exclude non-kin cells from swarming colony edges.
- Non-self cells are transiently induced into a growth-arrested state, reducing expression of genes for protein synthesis, virulence, and motility.
- Temporary activation of the stringent response is essential for entering this growth-arrested state, which also confers antibiotic tolerance.
Conclusions:
- The Ids system represents an expansion of bacterial kin discrimination paradigms beyond lethal antagonism.
- This non-lethal recognition mechanism plays a crucial role in the social behavior and lifecycle of P. mirabilis swarm colonies.
- Understanding this system clarifies the intricate interplay between bacterial recognition and cooperative behaviors.
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