Experimental demonstration that screening can enable the environmental recruitment of a defensive microbiome

Abstract

Many animals and plants recruit beneficial microbes from the environment, enhancing their defence against pathogens. However, we have only a limited understanding of the assembly mechanisms involved. A game-theoretical concept from economics, screening, potentially explains how a host can selectively recruit antibiotic-producing microbes from the environment, by fomenting and biasing competition among potential symbionts in such a way that the likely winners are mutualists. The cuticular microbiomes of Acromyrmex leaf-cutting ants inspired one of the first applications of screening theory to mutualisms, and here we use inoculation experiments to test the efficacy of screening in vitro. Using agar infused with antibacterial metabolites from the ants’ vertically transmitted Pseudonocardia symbionts, we show that secondary antibiotic-producing bacteria have higher growth rates than do non-producer strains and are more likely to win in direct competition. Our results demonstrate how game-theoretical concepts from economics can provide powerful insight into host-microbiome coevolution.