Natural variation in developmental life-history traits of the bacterium Myxococcus xanthus

Abstract

The soil bacterium Myxococcus xanthus is a model for the study of cooperative microbial behaviours such as social motility and fruiting body formation. Several M. xanthus developmental traits that are frequently quantified for laboratory strains are likely to be significant components of fitness in natural populations, yet little is known about the degree such traits vary in the wild and may therefore be subject to natural selection. Here we have tested whether several key M. xanthus developmental life-history traits have diverged significantly among strains both from globally distant origins and from within a sympatric, cm-scale population. The isolates examined here were found to vary greatly, in a heritable manner, in their rate of developmental aggregation and in both their rate and efficiency of spore production. Isolates also varied in the nutrient concentration threshold triggering spore formation and in the heat resistance of spores. The extensive diversity in developmental phenotypes documented here opens questions regarding the relative roles of selection and genetic drift in shaping the diversity of local soil populations with respect to these developmental traits. It also raises the question whether fitness in the wild is largely determined by traits that are expressed independently of social context or by behaviors that are expressed only in genetically heterogeneous social groups.

Endemic social diversity within natural kin groups of a cooperative bacterium

“…3A and Table S3; Kruskal Wallis-test: P < 0.001). This result is consistent with previous work that documented extensive variation in several developmental phenotypes among natural M. xanthus isolates (34,36,42,48).…”

“…1A) (45) and several developmental phenotypes, including spore production (Fig. 3A), the rate of development, responsiveness to nutrient depletion in triggering development (42), and competitiveness in forced isolate pairings (36). Here we have now also shown that pronounced social variation is present at high frequencies within many natural fruiting bodies-indeed within a majority of those fruiting bodies sampled here.…”

“…A high level of phenotypic and genetic diversity has been documented among cm-scale M. xanthus isolates (7,36,(42)(43)(44)(45), despite the fact that genetic diversity at this scale was found to be much lower than at only slightly larger sampling scales (8). For example, genetically similar centimeter-scale isolates were found to show extremely divergent competitive abilities during fruiting body development in forcibly mixed pairings (36).…”

Social complementation and growth advantages promote socially defective bacterial isolates

“…These subsets include clones that exhibited significant within-fruiting-body variation in swarming rate, spore production or both. Social trait phenotypes vary continuously in natural populations of M. xanthus [14,20,21,[40][41][42][43]. Nonetheless, we found previously that subsets of isolate samples from a single fruiting body often cluster, apparently discretely, within significantly different social phenotype ranges in a manner detectable by a k-means cluster algorithm [14].…”

“…Naturally variable traits include developmental competitiveness in mixed groups [11,27,42], social swarming rates [20], rate of development [21], allee effects during development [43] and predation range [40]. Kraemer & Velicer [14] found that even closely related clones isolated from within a single fruiting body often vary markedly in their expression of social phenotypes.…”