Abstract

Myxobacteria are known for complex social behaviors including outer membrane exchange (OME), in which cells exchange large amounts of outer membrane lipids and proteins upon contact. The TraA cell surface receptor selects OME partners based on a variable domain. However, traA polymorphism alone is not sufficient to precisely discriminate kin. Here, we report a novel family of OME-delivered toxins that promote kin discrimination of OME partners. These SitA lipoprotein toxins are polymorphic and widespread in myxobacteria. Each sitA is associated with a cognate sitI immunity gene, and in some cases a sitB accessory gene. Remarkably, we show that SitA is transferred serially between target cells, allowing the toxins to move cell-to-cell like an infectious agent. Consequently, SitA toxins define strong identity barriers between strains and likely contribute to population structure, maintenance of cooperation, and strain diversification. Moreover, these results highlight the diversity of systems evolved to deliver toxins between bacteria.

Highlights

  • Cooperative, social organisms benefit by resource sharing and division of labor between individuals in a population

  • Downstream of sitA1 is a gene that shows homology to the SUKH-family of immunity proteins commonly found in polymorphic toxin systems (Zhang et al, 2011) (Figure 1A)

  • M. xanthus cells that express heterologous sitAI3Mf1 or sitBAI1Mf1 outcompeted the parental strain in a traA-dependent manner (Figure 2—figure supplement 3). These results indicate that SitA toxin delivery is not limited by its specific species/strain of origin, and that the systems are functional after horizontal gene transfer (HGT) of a minimal set of components

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Summary

Introduction

Cooperative, social organisms benefit by resource sharing and division of labor between individuals in a population. These behaviors entail directing beneficial action toward kin, often at a fitness cost to the actor. Relatedness between individuals must be high for such cooperative action to remain evolutionarily viable (Hamilton, 1964a, 1964b). This requires that social organisms recognize their kin, and direct preferential action toward them (kin discrimination). Insights in this area will help us to understand the organization of microbes into social groups and the behaviors that maintain cooperation despite seemingly opposing evolutionary pressures to be selfish

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