skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.

Explore Research Products in the PAR
It may take a few hours for recently added research products to appear in PAR search results.


Title: Interactions among Escovopsis, Antagonistic Microfungi Associated with the Fungus-Growing Ant Symbiosis
Fungi in the genus Escovopsis (Ascomycota: Hypocreales) are prevalent associates of the complex symbiosis between fungus-growing ants (Tribe Attini), the ants’ cultivated basidiomycete fungi and a consortium of both beneficial and harmful microbes found within the ants’ garden communities. Some Escovopsis spp. have been shown to attack the ants’ cultivated fungi, and co-infections by multiple Escovopsis spp. are common in gardens in nature. Yet, little is known about how Escovopsis strains impact each other. Since microbe–microbe interactions play a central role in microbial ecology and evolution, we conducted experiments to assay the types of interactions that govern Escovopsis–Escovopsis relationships. We isolated Escovopsis strains from the gardens of 10 attine ant genera representing basal (lower) and derived groups in the attine ant phylogeny. We conducted in vitro experiments to determine the outcome of both intraclonal and interclonal Escovopsis confrontations. When paired with self (intraclonal interactions), Escovopsis isolated from lower attine colonies exhibited antagonistic (inhibitory) responses, while strains isolated from derived attine colonies exhibited neutral or mutualistic interactions, leading to a clear phylogenetic pattern of interaction outcome. Interclonal interactions were more varied, exhibiting less phylogenetic signal. These results can serve as the basis for future studies on the costs and benefits of Escovopsis coinfection, and on the genetic and chemical mechanisms that regulate the compatibility and incompatibility observed here.  more » « less
Award ID(s):
1754595
PAR ID:
10331130
Author(s) / Creator(s):
; ; ; ; ;
Date Published:
Journal Name:
Journal of Fungi
Volume:
7
Issue:
12
ISSN:
2309-608X
Page Range / eLocation ID:
1007
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. ; ; ; ; ; ; ; ; ; (, Applied and Environmental Microbiology)
    Rudi, Knut (Ed.)
    ABSTRACT Within animal-associated microbiomes, the functional roles of specific microbial taxa are often uncharacterized. Here, we use the fungus-growing ant system, a model for microbial symbiosis, to determine the potential defensive roles of key bacterial taxa present in the ants’ fungus gardens. Fungus gardens serve as an external digestive system for the ants, with mutualistic fungi in the genus Leucoagaricus converting the plant substrate into energy for the ants. The fungus garden is host to specialized parasitic fungi in the genus Escovopsis . Here, we examine the potential role of Burkholderia spp. that occur within ant fungus gardens in inhibiting Escovopsis. We isolated members of the bacterial genera Burkholderia and Paraburkholderia from 50% of the 52 colonies sampled, indicating that members of the family Burkholderiaceae are common inhabitants in the fungus gardens of a diverse range of fungus-growing ant genera. Using antimicrobial inhibition bioassays, we found that 28 out of 32 isolates inhibited at least one Escovopsis strain with a zone of inhibition greater than 1 cm. Genomic assessment of fungus garden-associated Burkholderiaceae indicated that isolates with strong inhibition all belonged to the genus Burkholderia and contained biosynthetic gene clusters that encoded the production of two antifungals: burkholdine1213 and pyrrolnitrin. Organic extracts of cultured isolates confirmed that these compounds are responsible for antifungal activities that inhibit Escovopsis but, at equivalent concentrations, not Leucoagaricus spp. Overall, these new findings, combined with previous evidence, suggest that members of the fungus garden microbiome play an important role in maintaining the health and function of fungus-growing ant colonies. IMPORTANCE Many organisms partner with microbes to defend themselves against parasites and pathogens. Fungus-growing ants must protect Leucoagaricus spp., the fungal mutualist that provides sustenance for the ants, from a specialized fungal parasite, Escovopsis . The ants take multiple approaches, including weeding their fungus gardens to remove Escovopsis spores, as well as harboring Pseudonocardia spp., bacteria that produce antifungals that inhibit Escovopsis. In addition, a genus of bacteria commonly found in fungus gardens, Burkholderia , is known to produce secondary metabolites that inhibit Escovopsis spp. In this study, we isolated Burkholderia spp. from fungus-growing ants, assessed the isolates’ ability to inhibit Escovopsis spp., and identified two compounds responsible for inhibition. Our findings suggest that Burkholderia spp. are often found in fungus gardens, adding another possible mechanism within the fungus-growing ant system to suppress the growth of the specialized parasite Escovopsis . 
    more » « less
  2. ; ; ; ; ; ; ; ; ; ; et al (, Proceedings of the National Academy of Sciences)
    Fungi shape the diversity of life. Characterizing the evolution of fungi is critical to understanding symbiotic associations across kingdoms. In this study, we investigate the genomic and metabolomic diversity of the genus Escovopsis , a specialized parasite of fungus-growing ant gardens. Based on 25 high-quality draft genomes, we show that Escovopsis forms a monophyletic group arising from a mycoparasitic fungal ancestor 61.82 million years ago (Mya). Across the evolutionary history of fungus-growing ants, the dates of origin of most clades of Escovopsis correspond to the dates of origin of the fungus-growing ants whose gardens they parasitize. We reveal that genome reduction, determined by both genomic sequencing and flow cytometry, is a consistent feature across the genus Escovopsis, largely occurring in coding regions, specifically in the form of gene loss and reductions in copy numbers of genes. All functional gene categories have reduced copy numbers, but resistance and virulence genes maintain functional diversity. Biosynthetic gene clusters (BGCs) contribute to phylogenetic differences among Escovopsis spp., and sister taxa in the Hypocreaceae. The phylogenetic patterns of co-diversification among BGCs are similarly exhibited across mass spectrometry analyses of the metabolomes of Escovopsis and their sister taxa. Taken together, our results indicate that Escovopsis spp. evolved unique genomic repertoires to specialize on the fungus-growing ant-microbe symbiosis. 
    more » « less
  3. ; ; ; ; (, Sociobiology)
    The ability to recognize nestmates is critical to the ecological success of social insects. Fungus-farming “attine” ants (Formicidae: Myrmicinae: Attini: Attina) can recognize their nestmates and symbiotic fungi via chemoreception. Although it has been shown that mutualistic fungi release volatile compounds that elicit responses in fungus-farming ants, the compounds and the sensory mechanisms involved remain little studied. Here, we characterize compounds found in attine fungus gardens and explore the correlations between those compounds, fungal substrates, and the laboratory environment. We also characterize ant cuticular hydrocarbons from Atta cephalotes colonies of the same species maintained in the same laboratory conditions for two or more years. Using gas chromatography associated with mass spectrometry, we verified that both substrate (i.e., the food on which fungus gardens grow) and environmental origin may influence the volatiles the fungus releases. We found compounds related to the environment, including naphthalene. We show that the volatile profiles of fungal strains grown by Atta cephalotes are most similar to each other, whereas the profile of the fungus grown by ants in the genus Cyphomyrmex is more similar to that of their substrate than to the profiles of other cultivated fungi. Regarding cuticular hydrocarbons, we found that ants collected in the same location have more similar hydrocarbon profiles than ants of the same species collected in a different location, even if all the colonies had been maintained under the same conditions (temperature, substrate) for extended periods. Our results provide strong evidence that a combination of species genetics and environmental factors shape variations in the volatile chemical profiles of cultivated fungi. After long homogenization, ants still demonstrate a solid difference among the cuticular profiles. 
    more » « less
  4. ; ; ; ; (, IMA Fungus)
    Abstract Escovopsisis a diverse group of fungi, which are considered specialized parasites of the fungal cultivars of fungus-growing ants. The lack of a suitable taxonomic framework and phylogenetic inconsistencies have long hamperedEscovopsisresearch. The aim of this study is to reassess the genusEscovopsisusing a taxonomic approach and a comprehensive multilocus phylogenetic analysis, in order to set the basis of the genus systematics and the stage for futureEscovopsisresearch. Our results support the separation ofEscovopsisinto three distinct genera. In light of this, we redefineEscovopsisas a monophyletic clade whose main feature is to form terminal vesicles on conidiophores. Consequently,E. kreiseliiandE. trichodermoideswere recombined into two new genera,SympodioroseaandLuteomyces, asS.kreiseliiandL.trichodermoides, respectively. This study expands our understanding of the systematics ofEscovopsisand related genera, thereby facilitating future research on the evolutionary history, taxonomic diversity, and ecological roles of these inhabitants of the attine ant colonies. 
    more » « less
  5. ; ; ; ; ; ; ; (, Proceedings of the National Academy of Sciences)
    Evolutionary adaptations for maintaining beneficial microbes are hallmarks of mutualistic evolution. Fungus-farming “attine” ant species have complex cuticular modifications and specialized glands that house and nourish antibiotic-producing Actinobacteria symbionts, which in turn protect their hosts’ fungus gardens from pathogens. Here we reconstruct ant–Actinobacteria evolutionary history across the full range of variation within subtribe Attina by combining dated phylogenomic and ultramorphological analyses. Ancestral-state analyses indicate the ant–Actinobacteria symbiosis arose early in attine-ant evolution, a conclusion consistent with direct observations of Actinobacteria on fossil ants in Oligo-Miocene amber. qPCR indicates that the dominant ant-associated Actinobacteria belong to the genus Pseudonocardia . Tracing the evolutionary trajectories of Pseudonocardia -maintaining mechanisms across attine ants reveals a continuum of adaptations. In Myrmicocrypta species, which retain many ancestral morphological and behavioral traits, Pseudonocardia occur in specific locations on the legs and antennae, unassociated with any specialized structures. In contrast, specialized cuticular structures, including crypts and tubercles, evolved at least three times in derived attine-ant lineages. Conspicuous caste differences in Pseudonocardia -maintaining structures, in which specialized structures are present in worker ants and queens but reduced or lost in males, are consistent with vertical Pseudonocardia transmission. Although the majority of attine ants are associated with Pseudonocardia , there have been multiple losses of bacterial symbionts and bacteria-maintaining structures in different lineages over evolutionary time. The early origin of ant– Pseudonocardia mutualism and the multiple evolutionary convergences on strikingly similar anatomical adaptations for maintaining bacterial symbionts indicate that Pseudonocardia have played a critical role in the evolution of ant fungiculture. 
    more » « less
  • Citation Formats
  • MLA
  • APA
  • Chicago
  • BibTeX
  • Save / Share this Record
  • Send to Email