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Infectious polymorphic toxins delivered by outer membrane exchange discriminate kin in myxobacteria.

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.

SUBMITTER: Vassallo CN

PROVIDER: S-EPMC5562445 | biostudies-literature | 2017 Aug

REPOSITORIES: biostudies-literature

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Infectious polymorphic toxins delivered by outer membrane exchange discriminate kin in myxobacteria.

Vassallo Christopher N CN Cao Pengbo P Conklin Austin A Finkelstein Hayley H Hayes Christopher S CS Wall Daniel D

eLife 20170818

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, <i>traA</i> 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 polymorphi ...[more]

PMID: 28820387

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Project description:Bacteria compete against related individuals by delivering toxins. In myxobacteria, a key delivery and kin discrimination mechanism is called outer membrane (OM) exchange (OME). Here, cells that display compatible polymorphic cell surface receptors recognize one another and bidirectionally transfer OM content. Included in the cargo is a suite of polymorphic SitA lipoprotein toxins. Consequently, OME between compatible cells that are not clonemates results in intoxication, while exchange between clonemates is harmonious because cells express a cognate repertoire of immunity proteins, which themselves are not transferred. SitA toxins belong to six nonhomologous families classified by sequence conservation within their N-terminal "escort domains" (EDs), while their C termini contain polymorphic nucleases that target the cytoplasmic compartment. To investigate how toxins delivered to the OM by OME translocate to the cytoplasm, we selected transposon mutants resistant to each family. Our screens identified eight genes that conferred resistance in a SitA family-specific manner. Most of these genes are predicted to localize to the cell envelope, and some resemble proteins that colicins exploit to gain cell entry. By constructing functional chimeric SitAs between families, we show that the ED determines the specificity of resistance. Importantly, a mutant that confers resistance to all six SitA families was discovered. This gene was named traC and plays an accessory role with traAB in OME. This work thus provides insight into the mechanism of kin discrimination in myxobacteria and provides working models for how SitA toxins exploit host proteins to gain cytoplasmic entry. IMPORTANCE Many bacterial species use diverse systems to deliver bacteriocins or toxins to neighboring competing cells. These systems are often selective in targeting cells that are related to themselves and therefore compete in the same niches for resources. How these systems specifically identify target cells and deliver toxins to particular cellular compartments is a fundamental question. This study uses the model social bacterium Myxococcus xanthus to unravel how its kin discrimination system, called outer membrane exchange, works. Along with the TraA polymorphic cell surface receptor that identifies related individuals with compatible receptors, this work discovered a new protein, called TraC, that functions in this discrimination system. Additionally, genetic screens identified host factors that are proposed to be involved in the cytoplasmic entry of lipoprotein toxins from the OM. This work complements and broadens our mechanistic understanding of how bacteria use transport systems to discriminate against related foes to build clonal populations.

Dataset Information

Infectious polymorphic toxins delivered by outer membrane exchange discriminate kin in myxobacteria.

Publications

Infectious polymorphic toxins delivered by outer membrane exchange discriminate kin in myxobacteria.

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