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

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 cooperative social behavior in P. mirabilis through a distinct mechanism: selectively and transiently inducing nonself cells into a 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 found that entry into this state requires a temporary activation of the stringent response in non-self cells and results 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. self recognition | Proteus mirabilis | kin selection | swarm motility | stringent response | antibiotic tolerance | bacterial communities | social evolution | cellcell communication | sociomicrobiology Correspondence: kagibbs@mcb.harvard.edu Briefly, two proteins, IdsD and IdsE, govern self iden-Tipping et al. | bioRχiv | December 9, 2018 | 1-47 2 | bioRχiv Tipping et al. | Ids controls access to swarming

The conserved serine transporter SdaC moonlights to enable self recognition

“…Therefore, internal serine levels, partially controlled by SdaC activity, are important during collective motility. And it is during this collective motility that self recognition occurs (Tipping & Gibbs, 2019). Expanding upon proposals for phage receptors, the coupling of SdaC functions may limit the emergence of mutations in both pathways.…”

“…Individual cells communicate using self-recognition proteins to discern clonal siblings from others. Siblings gain preferred access to collective motility; non-self cells enter a transient altered state, resulting in exclusion from the swarming population (Cardarelli et al, 2015; Saak & Gibbs, 2016; Tipping & Gibbs, 2019). Unlike many cooperative self-recognition proteins found on the cell’s surface (Hirose et al, 2017; Pathak et al, 2013) , P. mirabilis cells inject the protein signal IdsD into adjacent neighbors.…”

Biofilms 2018: a Diversity of Microbes and Mechanisms

“…Proteus mirabilis, a pathogen that causes persistent and recurrent infections, encodes receptors that permit it to distinguish "self" from "nonself" (82). Receptor mutants that cannot distinguish self from nonself exhibit, among other things, decreased flagellar transcription and increased levels of stress response, including increased tolerance of antibiotics (83). The dynamics of the interactions between self and nonself are readily apparent in the oscillatory (bullseye) patterns of swarmer cell migration, where mixtures of strains eventually result in self-only cells on the outer edges of the swarm.…”

Coaggregation properties of trimeric autotransporter adhesins

“…Eukaryotic micro‐organisms such as amoebae, yeasts, and ciliates exhibit kin recognition and kin selection when forming multicellular structures (Chaine, Schtickzelle, Polard, Huet, & Clobert, 2010; Mehdiabadi et al, 2006; Queller, Ponte, Bozzaro, & Strassmann, 2003; Smukalla et al, 2008). Many bacteria also discriminate between related and nonrelated strains in multicellular settings such as when swarming, which require the bacteria to co‐operate (Stefanic, Kraigher, Lyons, Kolter, & Mandic‐Mulec, 2015; Tipping & Gibbs, 2019; Vos & Velicer, 2009). A recent example of co‐operation mediated by aggregation of related bacteria comes from Vibrio cholerae , where the major type IV pilus subunit PilA varies from strain to strain and the pili interact selectively to form kin‐selected co‐operative communities on chitinous surfaces (Adams, Stutzmann, Stoudmann, & Blokesch, 2019).…”