Abstract
BackgroundThe cuticular microbiomes of Acromyrmex leaf-cutting ants pose a conundrum in microbiome biology because they are freely colonisable, and yet the prevalence of the vertically transmitted bacteria Pseudonocardia, which contributes to the control of Escovopsis fungus garden disease, is never compromised by the secondary acquisition of other bacterial strains. Game theory suggests that competition-based screening can allow the selective recruitment of antibiotic-producing bacteria from the environment, by providing abundant resources to foment interference competition between bacterial species and by using Pseudonocardia to bias the outcome of competition in favour of antibiotic producers.ResultsHere, we use RNA-stable isotope probing (RNA-SIP) to confirm that Acromyrmex ants can maintain a range of microbial symbionts on their cuticle by supplying public resources. We then used RNA sequencing, bioassays, and competition experiments to show that vertically transmitted Pseudonocardia strains produce antibacterials that differentially reduce the growth rates of other microbes, ultimately biassing the bacterial competition to allow the selective establishment of secondary antibiotic-producing strains while excluding non-antibiotic-producing strains that would parasitise the symbiosis.ConclusionsOur findings are consistent with the hypothesis that competition-based screening is a plausible mechanism for maintaining the integrity of the co-adapted mutualism between the leaf-cutting ant farming symbiosis and its defensive microbiome. Our results have broader implications for explaining the stability of other complex symbioses involving horizontal acquisition.
Highlights
The cuticular microbiomes of Acromyrmex leaf-cutting ants pose a conundrum in microbiome biology because they are freely colonisable, and yet the prevalence of the vertically transmitted bacteria Pseudonocardia, which contributes to the control of Escovopsis fungus garden disease, is never compromised by the secondary acquisition of other bacterial strains
Labelled and unlabelled RNA within a sample can be separated via ultracentrifugation and fractionation; these fractions can be used as templates for 16S rRNA gene amplicon sequencing so that the bacterial taxa that do use host-supplied resources can be identified [44]
We further show that the resource is public, meaning that the resource is used for growth by vertically transmitted Pseudonocardia and by multiple species of environmentally acquired bacteria on the ant cuticle (Fig. 2)
Summary
The cuticular microbiomes of Acromyrmex leaf-cutting ants pose a conundrum in microbiome biology because they are freely colonisable, and yet the prevalence of the vertically transmitted bacteria Pseudonocardia, which contributes to the control of Escovopsis fungus garden disease, is never compromised by the secondary acquisition of other bacterial strains. The diversity of insect-associated microbial communities is staggering. They may consist of single intracellular symbionts with reduced genomes owing to coadaptation at one extreme [1] and to dynamic microbiomes in open host compartments such as guts at the other end of the scale [2]. While relentless competition is the default setting of the microbial world [7], hosts appear to evolve control by holding their microbiome ecosystems on a leash [8], but how dynamic stability under continuing turnover is achieved remains unclear. Despite an abundance of microbiome research, recent reviews have concluded that “integration between theory and experiments is a crucial ‘missing link’ in current microbial ecology” [9] and that ‘our ability to make predictions about these dynamic, highly complex communities is limited’ [10]
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