Aggregative chimeric multicellularity in the absence of lethal kin discrimination

Aggregative multicellularity is a cooperative strategy used by some microbes. Unlike plant and animal development, which proceeds through clonal expansion from a single progenitor cell, aggregation is susceptible to genetic conflict and cheating, threatening multicellular stability. Myxococcus xanthus and Dictyostelium spp. are soil-dwelling models that form spore-producing fruiting bodies by aggregation upon starvation. Studies of natural M. xanthus fruiting bodies show that this process is confined to clonemates or close relatives, whereas Dictyostelium spp. can form polyclonal fruiting bodies. Here, we examine kin recognition by co-culturing two distantly related M. xanthus strains under vegetative and starvation conditions. We show that strains segregate and antagonize via their type VI secretion systems (T6SS), yielding monoclonal fruiting bodies. In contrast, mixtures of T6SS mutant strains do not antagonize and form chimeric swarms and fruiting bodies with spores from both strains. Nevertheless, within these T6SS mutant swarms and fruiting bodies, strains segregate, thus revealing that nonlethal kin discrimination mechanisms also exist in this species. These findings further suggest that T6SS are a major mediator of lethal kin discrimination between distantly related strains. Thus, lethal kin discrimination ensures homogeneous populations and monoclonal fruiting body development, whereas nonlethal mechanisms play a more subtle and less discriminatory role similar to Dictyostelium spp.