Factors that influence the caste ratio in a bacterial division of labour

Abstract

Colonies of the bacteria Streptomyces coelicolor divide labour between cells that specialize on growth and sporulation and cells that specialize on antibiotic production. This division of labour arises due to costly chromosome deletions in the antibiotic overproducers. However, little is known about when and where these mutations occur or whether their frequency, which we liken to the caste ratio in social insects, is phenotypically plastic. To elucidate changes in the proportions of specialized cells (measured as the mutation frequency), we sampled S. coelicolor colonies grown under different conditions. Temporally, mutation frequency increased linearly with colony age and size. Spatially, mutations accumulated disproportionately in the colony center, despite greater growth and sporulation at the periphery. Exposing colonies to sub-inhibitory concentrations of some antibiotics, a competitive cue in Streptomyces, increased mutation frequencies. Finally, direct competition with other Streptomyces that naturally produce antibiotics increased mutation frequencies, while also increasing spore production. Our findings provide insights into the intrinsic and environmental factors driving division of labor in Streptomyces colonies by showing that mutation frequencies are dynamic and responsive to the competitive environment. These results show that chromosome deletions are phenotypically plastic and suggest that Streptomyces can flexibly adjust their caste ratio.