Functional role of phenylacetic acid from metapleural gland secretions in controlling fungal pathogens in evolutionarily derived leaf-cutting ants

Abstract

Fungus-farming ant colonies vary four to five orders of magnitude in size. They employ compounds from actinomycete bacteria and exocrine glands as antimicrobial agents. Atta colonies have millions of ants and are particularly relevant for understanding hygienic strategies as they have abandoned their ancestors' prime dependence on antibiotic-based biological control in favour of using metapleural gland (MG) chemical secretions. Atta MGs are unique in synthesizing large quantities of phenylacetic acid (PAA), a known but little investigated antimicrobial agent. We show that particularly the smallest workers greatly reduce germination rates of Escovopsis and Metarhizium spores after actively applying PAA to experimental infection targets in garden fragments and transferring the spores to the ants' infrabuccal cavities. In vitro assays further indicated that Escovopsis strains isolated from evolutionarily derived leaf-cutting ants are less sensitive to PAA than strains from phylogenetically more basal fungus-farming ants, consistent with the dynamics of an evolutionary arms race between virulence and control for Escovopsis, but not Metarhizium. Atta ants form larger colonies with more extreme caste differentiation relative to other attines, in societies characterized by an almost complete absence of reproductive conflicts. We hypothesize that these changes are associated with unique evolutionary innovations in chemical pest management that appear robust against selection pressure for resistance by specialized mycopathogens.

Formicine ants swallow their highly acidic poison for gut microbial selection and control

“…Overall our study provides evidence that swallowing of formic acid containing poison gland secretions acts as a chemical filter for microbial selection and control of gut associated microbes, protecting formicine ants from food borne bacterial pathogens and structuring gut associated microbial communities. In ants and other animals that lack acidic poison gland secretions, acids produced by other exocrine glands (Fernández-Marín et al, 2015, Yek and Mueller, 2011) or acidic derivatives produced by defensive symbionts (Florez et al, 2015) or other environmental bacteria (Ratzke and Gore, 2018) might provide functionally similar roles to acidic poison gland secretions, as indicated in bees (Palmer-Young et al, 2018) and termites (Inagaki and Matsuura, 2018). Antimicrobials as external immune defence traits (Otti et al, 2014) may generally not only serve pathogen protection and microbial control but may also act as microbial filters to manage host associated microbes, be it in food or the environment, and thus contribute to a host’s ecological and evolutionary success.…”

Quality and quantity: transitions in antimicrobial gland use for parasite defense

“…; Fernández‐Marín et al. ). Additionally, the strength of this effect, and reliance on the MG, seems to be compounded by the efficacy of some of the MG secretions themselves; not only do the leaf‐cutting ants and S. amabilis use their glands more actively, but also the compounds in their secretions are more effective antifungal agents.…”

“…The leaf-cutting ants and S. amabilis all also showed higher rates of MG grooming behavior, and their secretions contained chemicals with stronger antifungal activity, including more acidic compounds phenylacetic acid and methyl oleate (Do Nascimento and Schoeters 1996;Yek et al 2012). This was particularly evident in Atta colombica, which was the only species in which the highly antifungal phenylacetic acid has been identified (Vieira et al 2012b;Fern andez-Mar ın et al 2015). Additionally, the strength of this effect, and reliance on the MG, seems to be compounded by the efficacy of some of the MG secretions Figure 3.…”

By their own devices: invasive Argentine ants have shifted diet without clear aid from symbiotic microbes

“…In species where these putative agents of garden pest control are absent or found at low density, the ants seem to invest in alternate strategies for the maintenance of healthy fungus gardens, including heightened grooming and the use of antimicrobial substances secreted from the metapleural gland (Fernandez‐Marin et al . , , ). Might large masses of gut bacteria, then, represent one strategy in a series of trade‐offs that ants navigate to meet the challenges imposed by nature?…”