Microfungal “Weeds” in the Leafcutter Ant Symbiosis

Abstract

Leafcutter ants (Formicidae: tribe Attini) are well-known insects that cultivate basidiomycete fungi (Agaricales: Lepiotaceae) as their principal food. Fungus gardens are monocultures of a single cultivar strain, but they also harbor a diverse assemblage of additional microbes with largely unknown roles in the symbiosis. Cultivar-attacking microfungi in the genus Escovopsis are specialized parasites found only in association with attine gardens. Evolutionary theory predicts that the low genetic diversity in monocultures should render ant gardens susceptible to a wide range of diseases, and additional parasites with roles similar to that of Escovopsis are expected to exist. We profiled the diversity of cultivable microfungi found in 37 nests from ten Acromyrmex species from Southern Brazil and compared this diversity to published surveys. Our study revealed a total of 85 microfungal strains. Fusarium oxysporum and Escovopsis were the predominant species in the surveyed gardens, infecting 40.5% and 27% of the nests, respectively. No specific relationship existed regarding microfungal species and ant-host species, ant substrate preference (dicot versus grass) or nesting habit. Molecular data indicated high genetic diversity among Escovopsis isolates. In contrast to the garden parasite, F. oxysporum strains are not specific parasites of the cultivated fungus because strains isolated from attine gardens have similar counterparts found in the environment. Overall, the survey indicates that saprophytic microfungi are prevalent in South American leafcutter ants. We discuss the antagonistic potential of these microorganisms as "weeds" in the ant-fungus symbiosis.

Diversity of Fungi Associated withAtta bisphaerica(Hymenoptera: Formicidae): The Activity ofAspergillus ochraceusandBeauveria bassiana

“…It is believed that these fungi are frequently found due to their cosmopolitan distribution, being acquired from the environment and dispersed during the founding of a colony by queens or forage worker ants carrying leaves. The role of the Cladosporium species inside the ant colonies is not known for sure, but they have been considered potential antagonists of the fungus garden [28]. The same kind of reasoning can be adopted for the Mucor fungi species, which have also been found in the nests of leaf-cutting ants, however, without knowing exactly how they interact with these ants or the fungus garden.…”

Generalized antifungal activity and 454-screening ofPseudonocardiaandAmycolatopsisbacteria in nests of fungus-growing ants

“…The living biomass of an attine garden is dominated by a monoculture of basidiomycete fungus that is tended by the ants as food (1), but additional microbes such as filamentous fungi, yeasts, and bacteria grow alongside the cultivated fungus in the garden matrix, as well as on the ants themselves. These secondary microbes interact in antagonistic, commensal, or mutualistic ways with each other, with the cultivated fungus, and with the host ants (1)(2)(3)(4)(5)(6)(7)(8).…”

“…A diversity of nonmutualistic ''weed'' fungi are known to grow in attine gardens, such as microfungi in the genera Trichoderma, Fusarium, or Syncephalastrum (1,6,7,9,10) but the best-studied fungal invaders in attine gardens are filamentous, ascomycetous fungi in the genus Escovopsis (Hypocreaceae, Hypocreales) (9). Because of an ability to parasitize cultivar mycelium (11), Escovopsis can devastate an entire garden (9).…”

Specialized Fungal Parasites and Opportunistic Fungi in Gardens of Attine Ants

“…is associated with several genera of attine ants and is considered a parasite of the fungus cultivated by these insects [43]. Except for fungus-growing ants in the Cyphomyrmex rimosus group, this parasite has been found in most attine ant genera with frequency of occurrence ranging from 11% to 75% [37,38,44,45]. Escovopsis sp.…”

“…Despite such mechanisms to suppress the development of alien microbes, a plethora of bacteria, filamentous fungi and yeasts are still found in ant gardens [35,[37][38][39][40][41].…”