Antibiotic production reduces the cost of resource cheaters in Streptomyces coelicolor

Abstract

Soil is a competitive environment containing a variety of resources used for bacterial growth. Complex polysaccharides, like chitin or starch, require the secretion of enzymes that degrade these resources into smaller units before they can be consumed. However, exoenzymes and the products they create are public goods, meaning they can be used by competitors, called "cheaters", who benefit from public goods even if they do not produce enzymes themselves. Here, we test the hypothesis that antibiotics produced by Streptomyces are used to privatize public goods by restricting access to resource cheaters. Using experiments with Streptomyces coelicolor and Bacillus subtilis, we first show that B. subtilis cheating significantly reduces S. coelicolor fitness on complex medium (starch) but not on a simple carbon source (maltose) which does not require exoenzyme secretion. Next, we show that antibiotics produced by S. coelicolor markedly increase fitness against resource cheaters, despite evidence that antibiotic production is metabolically costly. Finally, we find that the benefits of antibiotic production and the costs of resource cheating are both higher during growth on lower resource concentrations. Our results provide novel insights into the context-dependent costs and benefits of antibiotic secretion in Streptomyces and highlight the role of resource complexity and concentration in mediating competitive strategies in bacteria.