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SociogeograPhy

Phylogeography of social interactomes in soil myxobacteria

Keywords: Kin selection - Phylogenetics - Phylogeography - Population genomics

Kin discrimination and outer membrane exchange in Myxococcus xanthus: A comparative analysis among natural isolates

Reference: Wielgoss et al. (2018) Molecular Ecology

Genetically similar cells of the soil bacterium Myxococcus xanthus cooperate at multiple social behaviours, including motility and multicellular development. Another social interaction in this species is outer membrane exchange (OME), a behaviour of unknown primary benefit in which cells displaying closely related variants of the outer membrane protein TraA transiently fuse and exchange membrane contents. Functionally incompatible TraA variants do not mediate OME, which led to the proposal that TraA incompatibilities determine patterns of intercellular cooperation in nature, but how this might occur remains unclear. Using natural isolates from a centimetre-scale patch of soil, we analyse patterns of TraA diversity and ask whether relatedness at TraA is causally related to patterns of kin discrimination in the form of both colony-merger incompatibilities (CMIs) and interstrain antagonisms. A large proportion of TraA functional diversity documented among global isolates is predicted to be contained within this cm-scale population. We find evidence of balancing selection on the highly variable PA14-portion of TraA and extensive transfer of traA alleles across genomic backgrounds. CMIs are shown to be common among strains identical at TraA, suggesting that CMIs are not generally caused by TraA dissimilarity. Finally, it has been proposed that interstrain antagonisms might be caused by OME-mediated toxin transfer. However, we predict that most strain pairs previously shown to exhibit strong antagonisms are incapable of OME due to TraA dissimilarity. Overall, our results suggest that most documented patterns of kin discrimination in a natural population of M. xanthus are not causally related to the TraA sequences of interactants.

The biogeography of kin discrimination across microbial neighbourhoods

Reference: Kraemer, Wielgoss et al. (2016) Molecular Ecology

The spatial distribution of potential interactants is critical to social evolution in all cooperative organisms. Yet the biogeography of microbial kin discrimination at the scales most relevant to social interactions is poorly understood. Here we resolve the microbiogeography of social identity and genetic relatedness in local populations of the model cooperative bacterium Myxococcus xanthus at small spatial scales, across which the potential for dispersal is high. Using two criteria of relatedness—colony-merger compatibility during cooperative motility and DNA-sequence similarity at highly polymorphic loci—we find that relatedness decreases greatly with spatial distance even across the smallest scale transition. Both social relatedness and genetic relatedness are maximal within individual fruiting bodies at the micrometre scale but are much lower already across adjacent fruiting bodies at the millimetre scale. Genetic relatedness was found to be yet lower among centimetre-scale samples, whereas social allotype relatedness decreased further only at the metre scale, at and beyond which the probability of social or genetic identity among randomly sampled isolates is effectively zero. Thus, in M. xanthus, high-relatedness patches form a rich mosaic of diverse social allotypes across fruiting body neighbourhoods at the millimetre scale and beyond. Individuals that migrate even short distances across adjacent groups will frequently encounter allotypic conspecifics and territorial kin discrimination may profoundly influence the spatial dynamics of local migration. Finally, we also found that the phylogenetic scope of intraspecific biogeographic analysis can affect the detection of spatial structure, as some patterns evident in clade-specific analysis were masked by simultaneous analysis of all strains.

devI is an evolutionarily young negative regulator of Myxococcus xanthus development

Reference: Rajagopalan, Wielgoss et al. (2015) J Bacteriol

Several mutations in the so-called dev CRISPR-Cas system of M. xanthus can impair sporulation efficiency. However, the connection between development and that CRISPR-Cas system has been enigmatic. Thus, it was surprising to find that DNA sequencing of natural isolates reveals that most appear to lack a functional dev promoter, while these strains sporulate normally. The deletion of the dev promoter or a small gene downstream of it suppresses the sporulation defect of a lab strain with mutations in dev genes encoding Cas proteins. Our results support a model in which the Cas proteins DevRS prevents the overexpression of the small gene devI, which codes for an inhibitor of sporulation. Our whole-genome based phylogenetic analyses of natural isolates suggest that devI and the dev promoter were only recently acquired in some lineages.
Figure (right): Map of the M. xanthus laboratory strain DK1622 dev operon and structural evolution of the dev promoter region among natural lineages. (A) Map of the DK1622 dev operon and expanded view of the dev promoter region. (B) Structure and evolution of the dev promoter region. The leftward part shows phylogenetic relationships among natural isolates inferred from 4.5 Mbp of orthologous sequence. M. fulvus HW-1 served as the outgroup. Bootstrap values supporting branch inferences are shown near each branch. The center part shows the structure of the dev promoter region. Black boxes highlight orthologous regions shared among natural isolates and the reference strain DK1622. Thin lines depict DK1622 sequence regions that are absent from the respective genomes, either because there is no sequence at all in the corresponding region or because the sequence that is present is nonorthologous to that of DK1622. The rightward part shows a phylogenetic tree of a conserved partial segment of MXAN_7267 highlighting recent evolutionary history of the orthologous coding region upstream of the dev promoter.

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