Nature of the interactions between hypocrealean fungi and the mutualistic fungus of leaf-cutter ants

Varanda-Haifig, Sadala Schmidt; Albarici, Tatiane Regina; Nunes, Pablo Henrique; Haifig, Ives; Vieira, Paulo C.

doi:10.1007/s10482-016-0826-y

Cited by 20 publications

(27 citation statements)

References 34 publications

(81 reference statements)

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“…This may be possibly related to the use of metabolites derived from FF2006 as nutrient source in culture, since high exploitation competition is a common trait of Trichoderma, known as an environment opportunistic fungus [41]. On the other hand, E. nivea showed delayed growth in the presence of L. gongylophorus, this result supports its less aggressive pattern observed previously [32], as well as the minor resistance of the mutualistic fungus to some filamentous fungi, even in absence of tending ants.…”

Section: Discussionsupporting

confidence: 84%

“…These comparisons were carried out separately for each day, not accounting the time (days) as a dependent variable. For the mutualistic fungus, we first used one-way analysis of variance to ensure absence of differences between all control Camacan/BA Antagonist of ant cultivar [32] groups (cultivar growing in the absence of filamentous fungi) with an alpha threshold of 0.05 ( Figure S1). Then, we selected the distribution with the largest interquartile range.…”

Section: Dual Culture Bioassaysmentioning

confidence: 99%

“…Nevertheless, the real impact and modes of action of the invading filamentous fungi against the ant cultivar are still elusive. Considering fungus-fungus interactions, several studies showed growth inhibition of L. gongylophorus by filamentous fungi [14,[28][29][30][31][32]. Such interactions can be understood as interference and/or exploitation competition [33].…”

Section: Introductionmentioning

confidence: 99%

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Soluble Compounds of Filamentous Fungi Harm the Symbiotic Fungus of Leafcutter Ants

et al. 2018

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Chemical compounds are key to understand symbiotic interactions. In the leafcutter ant-microbe symbiosis a plethora of filamentous fungi continuously gain access the ant colonies through plant substrate collected by workers. Many filamentous fungi are considered transient in attine ant colonies, however, their real ecological role in this environment still remains unclear. A possible role of these microorganisms is the antagonism towards Leucoagaricus gongylophorus, the mutualistic fungus that serve as food for several leafcutter ant species. Here, we showed the antagonism of filamentous fungi isolated from different sources, and the negative impacts of their metabolites on the growth of the ant-fungal cultivar. Our results demonstrate that the chemical compounds produced by filamentous fungi can harm the mutualistic fungus of leafcutter ants.

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Section: Discussionsupporting

confidence: 84%

Section: Dual Culture Bioassaysmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Soluble Compounds of Filamentous Fungi Harm the Symbiotic Fungus of Leafcutter Ants

et al. 2018

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“…However, until now, no other secondary metabolites from E. weberi have been identified and it has not been established which compounds from E. weberi contribute to overpower the mutualistic fungus of leaf‐cutting ants . Here, we present the isolation and identification of secondary metabolites from E. weberi and evaluate their biological function, in particular their impact on L. gongylophorus and A. octospinosus leaf‐cutting ants.…”

Section: Introductionmentioning

confidence: 98%

“…Some of these gene clusters including polyketide synthase gene clusters were significantly up‐regulated when growing with L. gongylophorus . Moreover, crude extracts of several Escovopsis species were reported to inhibit the growth of L. gongylophorus . In a co‐cultivation study of E. weberi with microbial symbionts of leaf‐cutting ants Férnandez‐Marín et al.…”

Section: Introductionmentioning

confidence: 99%

Secondary Metabolites from Escovopsis weberi and Their Role in Attacking the Garden Fungus of Leaf‐Cutting Ants

Dhodary

Schilg

Wirth

et al. 2018

Chemistry A European J

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The specialized, fungal pathogen Escovopsis weberi threatens the mutualistic symbiosis between leaf-cutting ants and their garden fungus (Leucoagaricus gongylophorus). Because E. weberi can overwhelm L. gongylophorus without direct contact, it was suspected to secrete toxins. Using NMR and mass spectrometry, we identified several secondary metabolites produced by E. weberi. E. weberi produces five shearinine-type indole triterpenoids including two novel derivatives, shearinine L and shearinine M, as well as the polyketides, emodin and cycloarthropsone. Cycloarthropsone and emodin strongly inhibited the growth of the garden fungus L. gongylophorous at 0.8 and 0.7 μmol, respectively. Emodin was also active against Streptomyces microbial symbionts (0.3 μmol) of leaf-cutting ants. Shearinine L instead did not affect the growth of L. gongylophorus in agar diffusion assays. However, in dual choice behavioral assays Acromyrmex octospinosus ants clearly avoided substrate treated with shearinine L for the garden fungus after a 2 d learning period, indicating that the ants quickly learn to avoid shearinine L.

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Escovopsis kreiselii specialization to its native hosts in the fungiculture of the lower attine ant Mycetophylax morschi

Custódio

Rodrigues

2018

Antonie van Leeuwenhoek

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Parasite-host associations are widespread in nature and the fungus-growing ants are considered model organisms to study such interactions. These insects cultivate basidiomycetous fungi for food, which are threatened by mycotrophic fungi in the genus Escovopsis. Although recently described from colonies of the lower attine ant Mycetophylax morschi, the biology and pathogenicity of Escovopsis kreiselii are unknown. Herein, we evaluated the interaction of E. kreiselii with fungi cultivated by M. morschi (native hosts) and with a fungus cultivated by another attine ant species (non-native host). In addition, we examined the physical interactions between hypha of E. kreiselii and hypha from its native hosts using scanning electron microscopy. Escovopsis kreiselii inhibited the growth of fungal cultivars by 24% or more (with exception of one isolate), when compared to the fungal cultivars growing alone. Escovopsis kreiselii is attracted towards its native hosts through chemotaxis and inhibition occurs when there is physical contact with the hyphae of the fungal cultivar. As reported for Escovopsis parasites associated with leafcutter ants (higher attines), E. kreiselii growth increased in the presence of its native hosts, even before contact between both fungi occurred. In interactions with the fungal cultivar that is not naturally infected by E. kreiselii (non-native host), it caused inhibition but not at the same magnitude as in native hosts. Multiple lines of evidence suggest that E. kreiselii is an antagonist of the fungus cultivated by M. morschi and can chemically recognize such fungus.

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Nature of the interactions between hypocrealean fungi and the mutualistic fungus of leaf-cutter ants

Cited by 20 publications

References 34 publications

Soluble Compounds of Filamentous Fungi Harm the Symbiotic Fungus of Leafcutter Ants

Soluble Compounds of Filamentous Fungi Harm the Symbiotic Fungus of Leafcutter Ants

Secondary Metabolites from Escovopsis weberi and Their Role in Attacking the Garden Fungus of Leaf‐Cutting Ants

Escovopsis kreiselii specialization to its native hosts in the fungiculture of the lower attine ant Mycetophylax morschi

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