Chimaeric load among sympatric social bacteria increases with genotype richness

Abstract

The total productivity of social groups can be determined by interactions among their constituents. Chimaeric load--the reduction of group productivity caused by antagonistic within-group heterogeneity--may be common in heterogeneous microbial groups due to dysfunctional behavioural interactions between distinct individuals. However, some instances of chimaerism in social microbes can increase group productivity, thus making a general relationship between chimaerism and group-level performance non-obvious. Using genetically similar strains of the soil bacterium Myxococcus xanthus that were isolated from a single centimetre-scale patch of soil, we tested for a relationship between degree of chimaerism (genotype richness) and total group performance at social behaviours displayed by this species. Within-group genotype richness was found to correlate negatively with total group performance at most traits examined, including swarming in both predatory and prey-free environments and spore production during development. These results suggest that interactions between such neighbouring strains in the wild will tend to be mutually antagonistic. Negative correlations between group performance and average genetic distance among group constituents at three known social genes were not found, suggesting that divergence at other loci that govern social interaction phenotypes is responsible for the observed chimaeric load. The potential for chimaeric load to result from co-aggregation among even closely related neighbours may promote the maintenance and strengthening of kin discrimination mechanisms, such as colony-merger incompatibilities observed in M. xanthus. The findings reported here may thus have implications for understanding the evolution and maintenance of diversity in structured populations of soil microbes.

Keywords: chimaerism; group performance; multicellular development; predation; soil bacteria.

Figure 1.

Genealogical tree of the strains used in this study. The identification names used in the paper originally describing these strains [15] are indicated in parentheses. The bar scales for the average number of nucleotide substitutions per site.

Figure 2.

Individual strain swarming rates and spore production. Swarming rate on (a) lawn of Curtobacterium citreum, (b) lawn of Escherichia coli, (c) nutrient-rich CTT 1.5% agar, (d) nutrient-rich CTT 0.5% agar and (e) TPM 1.5% agar (no added carbon source). Note that the y-axis swarming-rate scale varies across graphs. (f) Spore production on TPM 1.5% agar. Error bars indicate the standard error of the mean.

Figure 3.

Effects of chimaerism on predatory swarming. Average swarming rates on C. citreum and E. coli lawns for groups of variable genotypic richness are shown. Error bars represent the standard error of the mean.

Figure 4.

Effects of chimaerism on sporulation. The five cases of significant differences between expected (dark grey bars) and observed (light grey bars) spore production by chimaeric groups are shown. Error bars represent the standard error of the mean.