RESUMO

Bacteria can live in a variety of interkingdom communities playing key ecological roles. The microbiome of leaf-cutting attine ant colonies are a remarkable example of such communities, as they support ants' metabolic processes and the maintenance of ant-fungus gardens. Studies on this topic have explored the bacterial community of the whole fungus garden, without discerning bacterial groups associated with the nutrient storage structures (gongylidia) of ant fungal cultivars. Here we studied bacteria isolated from the surface of gongylidia in the cultivars of Atta sexdens and Acromyrmex coronatus, to assess whether the bacterial community influences the biology of the fungus. A total of 10 bacterial strains were isolated from gongylidia (Bacillus sp., Lysinibacillus sp., Niallia sp., Staphylococcus sp., Paenibacillus sp., Pantoea sp., Staphylococcus sp., and one Actinobacteria). Some bacterial isolates increased gongylidia production and fungal biomass while others had inhibitory effects. Eight bacterial strains were confirmed to form biofilm-like structures on the fungal cultivar hyphae. They also showed auxiliary metabolic functions useful for the development of the fungal garden such as phosphate solubilization, siderophore production, cellulose and chitin degradation, and antifungal activity against antagonists of the fungal cultivar. Bacteria-bacteria interaction assays revealed heterogeneous behaviors including synergism and competition, which might contribute to regulate the community structure inside the garden. Our results suggest that bacteria and the ant fungal cultivar interact directly, across a continuum of positive and negative interactions within the community. These complex relationships could ultimately contribute to the stability of the ant-fungus mutualism.

Assuntos

RESUMO

Yeast-insect interactions are compelling models to study the evolution, ecology, and diversification of yeasts. Fungus-growing (attine) ants are prominent insects in the Neotropics that evolved an ancient fungiculture of basidiomycete fungi over 55-65 million years, supplying an environment for a hidden yeast diversity. Here we assessed the yeast diversity in the attine ant environment by thoroughly sampling fungus gardens across four out of five ant fungiculture systems: Acromyrmex coronatus and Mycetomoellerius tucumanus standing for leaf-cutting and higher-attine fungicultures, respectively; Apterostigma sp., Mycetophylax sp., and Mycocepurus goeldii as ants from the lower-attine fungiculture. Among the fungus gardens of all fungus-growing ants examined, we found taxonomically unique and diverse microbial yeast communities across the different fungicultures. Ascomycete yeasts were the core taxa in fungus garden samples, with Saccharomycetales as the most frequent order. The genera Aureobasidium, Candida, Papiliotrema, Starmerella, and Sugiyamaella had the highest incidence in fungus gardens. Despite the expected similarity within the same fungiculture system, colonies of the same ant species differed in community structure. Among Saccharomycotina yeasts, few were distinguishable as killer yeasts, with a classical inhibition pattern for the killer phenotype, differing from earlier observations in this environment, which should be further investigated. Yeast mycobiome in fungus gardens is distinct between colonies of the same fungiculture and each ant colony harbors a distinguished and unique yeast community. Fungus gardens of attine ants are emergent environments to study the diversity and ecology of yeasts associated with insects.

Assuntos

RESUMO

The leaf-cutter ant Acromyrmex balzani is responsible for causing important losses in reforestation areas, crops, and pastures, and is frequently found in the Brazilian savanna (Cerrado). So far, there is no information regarding the yeast communities that occur in their nests. Here, we evaluated the diversity, composition, and structure of yeast communities in both fungus gardens (FG) and external refuse dump (RD) of this ant species (Palmas, Tocantins, northern Brazil). A total of 720 yeasts were isolated, comprising 52 species distributed in 29 genera. The RDs have significantly richer and more diverse yeast communities than the fungus gardens, regardless of the season and the level of preservation in the area. The isolates produced a wide range of carbon polymer-degrading enzymes and were able to assimilate carbon-sources present in plant materials. We observed a different proportion of enzyme-producers and carbon-assimilation found in external refuse dump and fungus gardens from preserved and disturbed areas, suggesting that this interaction may vary depending on the environmental conditions. A. balzani nests in the savanna biome are a hotspot of yeast species with ecological, clinical, and biotechnological implications.

Assuntos

RESUMO

Fungus-growing ants share a complex symbiosis with microbes, including fungal mutualists, antibiotic-producing bacteria, and fungal pathogens. The bacterial communities associated with this symbiosis are poorly understood but likely play important roles in maintaining the health and function of fungal gardens. We studied bacterial communities in gardens of two Apterostigma species, A. dentigerum, and A. pilosum, using next-generation sequencing to evaluate differences between the two ant species, their veiled and no-veiled fungal garden types, and across three collection locations. We also compared different parts of nests to test for homogeneity within nests. Enterobacteriaceae dominated gardens of both species and common OTUs were shared across both species and nest types. However, differences in community diversity were detected between ant species, and in the communities of A. dentigerum veiled and no-veiled nests within sites. Apterostigma pilosum had a higher proportion of Phyllobacteriaceae and differed from A. dentigerum in the proportions of members of the order Clostridiales. Within A. dentigerum, nests with veiled and no-veiled fungus gardens had similar taxonomic profiles but differed in the relative abundance of some groups, with veiled gardens having more Rhodospirillaceae and Hyphomicrobiaceae, and no-veiled having more Xanthomonadaceae and certain genera in the Enterobacteriaceae C. However, bacterial communities in Apterostigma fungal gardens are highly conserved and resemble those of the nests of other attine ants with dominant taxa likely playing a role in biomass degradation and defense. Further work is required to understand and explain how bacterial community composition of fungus-growing nests is maintained.

Assuntos

RESUMO

BACKGROUND: Fungus gardens of fungus-growing (attine) ants harbor complex microbiomes in addition to the mutualistic fungus they cultivate for food. Fungi in the genus Escovopsioides were recently described as members of this microbiome but their role in the ant-fungus symbiosis is poorly known. In this study, we assessed the phylogenetic diversity of 21 Escovopsioides isolates obtained from fungus gardens of leafcutter ants (genera Atta and Acromyrmex) and non-leafcutter ants (genera Trachymyrmex and Apterostigma) sampled from several regions in Brazil. RESULTS: Regardless of the sample locality or ant genera, phylogenetic analysis showed low genetic diversity among the 20 Escovopsisoides isolates examined, which prompted the identification as Escovopsioides nivea (the only described species in the genus). In contrast, one Escovopsioides isolate obtained from a fungus garden of Apterostigma megacephala was considered a new phylogenetic species. Dual-culture plate assays showed that Escovopsioides isolates inhibited the mycelium growth of Leucoagaricus gongylophorus, the mutualistic fungus cultivated by somes species of leafcutter ants. In addition, Escovopsioides growth experiments in fungus gardens with and without ant workers showed this fungus is detrimental to the ant-fungus symbiosis. CONCLUSIONS: Here, we provide clues for the antagonism of Escovopsioides towards the mutualistic fungus of leafcutter ants.

Assuntos

RESUMO

Leafcutter ants are the ultimate insect superorganisms, with up to millions of physiologically specialized workers cooperating to cut and transport vegetation and then convert it into compost used to cultivate co-evolved fungi, domesticated over millions of years. We tested hypotheses about the nutrient-processing dynamics governing this functional integration, tracing 15 N- and 13 C-enriched substrates through colonies of the leafcutter ant Atta colombica. Our results highlight striking performance efficiencies, including rapid conversion (within 2 d) of harvested nutrients into edible fungal tissue (swollen hyphal tips called gongylidia) in the center of fungus gardens, while also highlighting that much of each colony's foraging effort resulted in substrate placed directly in the trash. We also find nutrient-specific processing dynamics both within and across layers of the fungus garden, and in ant consumers. Larvae exhibited higher overall levels of 15 N and 13 C enrichment than adult workers, supporting that the majority of fungal productivity is allocated to colony growth. Foragers assimilated 13 C-labeled glucose during its ingestion, but required several days to metabolically process ingested 15 N-labeled ammonium nitrate. This processing timeline helps resolve a 40-yr old hypothesis, that foragers (but apparently not gardeners or larvae) bypass their fungal crops to directly assimilate some of the nutrients they ingest outside the nest. Tracing these nutritional pathways with stable isotopes helps visualize how physiological integration within symbiotic networks gives rise to the ecologically dominant herbivory of leafcutter ants in habitats ranging from Argentina to the southern United States.

Assuntos

RESUMO

The attine ant system is a remarkable example of symbiosis. An antagonistic partner within this system is the fungal parasite Escovopsis, a genus specific to the fungal gardens of the Attini. Escovopsis parasitizes the Leucoagaricus symbiont that leaf-cutting ants (Acromyrmex, Atta) have been farming over the past 8-12 Myr. However, it has been a puzzle how Escovopsis reaches its host. During a seasonal survey of nests of Acromyrmex subterraneus subterraneus in Atlantic rainforest in Brazil, Escovopsis was detected in all the sampled fungal garden waste tips or middens (n = 111). Middens were built strategically; always below the nest entrances. Here, we report the first evidence of a putative mechanism for horizontal transmission of Escovopsis between attine colonies. It is posited that leaf-cutting ants pick up the spores from soil and litter during foraging and vector the mycoparasite between attine colonies. Field and laboratory experiments, using At. laevigata and Ac. subterraneus subterraneus, confirm that Escovopsis spores are phoretic, and have an inbuilt dormancy, broken by the presence of their Leucoagaricus host. However, in the coevolutionary arms race, Atta ants may lose out-despite most species in the genus investing in a more advanced waste disposal system-due to the insanitary habits of their Acromyrmex neighbours.

RESUMO

The evolution of ant agriculture, as practised by the fungus-farming 'attine' ants, is thought to have arisen in the wet rainforests of South America about 55-65 Ma. Most subsequent attine agricultural evolution, including the domestication event that produced the ancestor of higher attine cultivars, is likewise hypothesized to have occurred in South American rainforests. The 'out-of-the-rainforest' hypothesis, while generally accepted, has never been tested in a phylogenetic context. It also presents a problem for explaining how fungal domestication might have occurred, given that isolation from free-living populations is required. Here, we use phylogenomic data from ultra-conserved element (UCE) loci to reconstruct the evolutionary history of fungus-farming ants, reduce topological uncertainty, and identify the closest non-fungus-growing ant relative. Using the phylogeny we infer the history of attine agricultural systems, habitat preference and biogeography. Our results show that the out-of-the-rainforest hypothesis is correct with regard to the origin of attine ant agriculture; however, contrary to expectation, we find that the transition from lower to higher agriculture is very likely to have occurred in a seasonally dry habitat, inhospitable to the growth of free-living populations of attine fungal cultivars. We suggest that dry habitats favoured the isolation of attine cultivars over the evolutionary time spans necessary for domestication to occur.

Assuntos

RESUMO

Microbiome surveys provide clues for the functional roles of symbiotic microbial communities and their hosts. In this study, we elucidated bacterial microbiomes associated with the vertically transmitted fungal inocula (pellets) used by foundress queens of the leaf-cutting ant Atta texana as starter-cultures for new gardens. As reference microbiomes, we also surveyed bacterial microbiomes of foundress queens, gardens and brood of incipient nests. Pseudomonas, Acinetobacter, Propionibacterium and Corynebacterium were consistently present in high abundance in microbiomes. Some pellet and ant samples contained abundant bacteria from an Entomoplasmatales-clade, and a separate PCR-based survey of Entomoplasmatales bacteria in eight attine ant-genera from Brazil placed these bacteria in a monophyletic clade within the bacterial genus Mesoplasma. The attine ant-Mesoplasma association parallels a similar association between a closely related, monophyletic Entomoplasmatales-clade and army ants. Of thirteen A. texana nests surveyed, three nests with exceptionally high Mesoplasma abundance died, whereas the other nests survived. It is unclear whether Mesoplasma was the primary cause of mortality, or Mesoplasma became abundant in moribund nests for non-pathogenic reasons. However, the consistent and geographically widespread presence of Mesoplasma suggests an important functional role in the association with attine ants.