Competition-based screening helps to secure the evolutionary stability of a defensive microbiome

Abstract

Background 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. 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. Results Here, 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. Conclusions Our 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.

Partner fidelity and environmental filtering preserve stage‐specific turtle ant gut symbioses for over 40 million years

“…Partner fidelity is the most widely documented, being evidenced by the many symbionts passaged to offspring through transovarial transfer (Koga et al, 2012; Luan et al, 2016), or a range of “out‐of‐body” mechanisms (Salem et al, 2015). But many insects acquire symbionts from the environment, retaining specific subsets of the inoculated microbes (Birer et al, 2020; Chandler et al, 2011; Jones et al, 2019; Ravenscraft et al, 2019) due to their physiology and behavior (Engel & Moran, 2013; Tragust et al, 2020), or the actions of their regular symbiont partners (Itoh et al, 2019; Worsley et al, 2021). Among those adopting such environmental filtering mechanisms, some have evolved means for partner choice, selecting beneficial microbial partners amid a broader set of symbiotic suitors (Ohbayashi et al, 2015).…”

A new competitive strategy to unveil the antibiotic-producing Actinobacteria

“…Our design exploits the natural selection of more competitive strains along with enrichment conditions in liquid suspensions that also influence the retrieval of actinobacterial cultures. Consequently, non-producing bacteria likely have growth rates faster than antibiotic-producing microorganisms and are often more common in the environment than producing microorganisms as these organisms do not have a load of antibiotic production [37-38]. In the competition approach, where conditions of antibiotics as selection pressure may also favour the vertical transmission of primary antibiotic producers among interacting communities that may cause the selective horizontal recruitment of extra antibiotic-producing microorganisms in-vitro.…”

Bacterial Associates of a Desert Specialist Fungus-Growing Ant Antagonize Competitors with a Nocamycin Analog

“…12 Competition is expected when multiple bacterial strains co-occur in an ant population, and conceptual frameworks have been developed for such bacteria−bacteria competition in the context of fungusgrowing ants. 9,13,14 Chemical defenses from bacterial symbionts of fungusgrowing ants, both antibacterial and antifungal, have recently been a productive source for chemical discovery. We have turned our attention to the chemical ecology of desert-dwelling fungus-growing ants as their microbial partnerships are largely unexplored and their adaptation to a unique environment may include unique defensive compounds from their microbial associates.…”

“…Actinobacteria other than Pseudonocardia have been detected on the cuticle of fungus-growing ants in both culture-dependent and sequencing-dependent studies, and it remains debated whether these additional bacteria are transient or instead are maintained by the ants as part of a more complex cuticular microbiome . Competition is expected when multiple bacterial strains co-occur in an ant population, and conceptual frameworks have been developed for such bacteria–bacteria competition in the context of fungus-growing ants. ,, …”