Competition-based screening secures the evolutionary stability of a defensive microbiome

Cuticular microbiomes of Acromyrmex leaf-cutting ants are exceptional because they are freely colonizable, and yet the prevalence of Pseudonocardia, a native vertically transmitted symbiont that controls Escovopsis fungus-garden disease, is never compromised. Game theory suggests that competition-based screening can allow the selective recruitment of antibiotic-producing bacteria from the environment, by fomenting and biasing competition for abundant host resources. Mutual symbiont aggression benefits the host and also maintains native symbiont viability. Here we use RNA-stable isotope probing (RNA-SIP) to confirm predictions that Acromyrmex cuticles can maintain a range of microbial symbionts. We then used dual-RNA-sequencing and bioassays to show that vertically transmitted Pseudonocardia strains produce antibacterials that differentially reduce the growth rates of other microbes, ultimately eliminating non-antibiotic-producing strains that might parasitize the symbiosis while still allowing antibiotic-producing Streptomyces strains to survive. Open cuticular microbiomes can thus maintain a specific co-evolved mutualism by restricting access for other bacterial strains.