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The evolution of abdominal microbiomes in fungus-growing ants.

ABSTRACT: The attine ants are a monophyletic lineage that switched to fungus farming ca. 55-60 MYA. They have become a model for the study of complex symbioses after additional fungal and bacterial symbionts were discovered, but their abdominal endosymbiotic bacteria remain largely unknown. Here, we present a comparative microbiome analysis of endosymbiotic bacteria spanning the entire phylogenetic tree. We show that, across 17 representative sympatric species from eight genera sampled in Panama, abdominal microbiomes are dominated by Mollicutes, ?- and ?-Proteobacteria, and Actinobacteria. Bacterial abundances increase from basal to crown branches in the phylogeny reflecting a shift towards putative specialized and abundant abdominal microbiota after the ants domesticated gongylidia-bearing cultivars, but before the origin of industrial-scale farming based on leaf-cutting herbivory. This transition coincided with the ancestral single colonization event of Central/North America ca. 20 MYA, documented in a recent phylogenomic study showing that almost the entire crown group of the higher attine ants, including the leaf-cutting ants, evolved there and not in South America. Several bacterial species are located in gut tissues or abdominal organs of the evolutionarily derived, but not the basal attine ants. The composition of abdominal microbiomes appears to be affected by the presence/absence of defensive antibiotic-producing actinobacterial biofilms on the worker ants' cuticle, but the significance of this association remains unclear. The patterns of diversity, abundance and sensitivity of the abdominal microbiomes that we obtained explore novel territory in the comparative analysis of attine fungus farming symbioses and raise new questions for further in-depth research.

SUBMITTER: Sapountzis P

PROVIDER: S-EPMC6446810 | biostudies-literature | 2019 Feb

REPOSITORIES: biostudies-literature

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The evolution of abdominal microbiomes in fungus-growing ants.

Sapountzis Panagiotis P Nash David R DR Schiøtt Morten M Boomsma Jacobus J JJ

Molecular ecology 20181210 4

The attine ants are a monophyletic lineage that switched to fungus farming ca. 55-60 MYA. They have become a model for the study of complex symbioses after additional fungal and bacterial symbionts were discovered, but their abdominal endosymbiotic bacteria remain largely unknown. Here, we present a comparative microbiome analysis of endosymbiotic bacteria spanning the entire phylogenetic tree. We show that, across 17 representative sympatric species from eight genera sampled in Panama, abdomina ...[more]

PMID: 30411820

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Project description:BackgroundCooperative benefits of mutualistic interactions are affected by genetic variation among the interacting partners, which may have consequences for interaction-specificities across guilds of sympatric species with similar mutualistic life histories. The gardens of fungus-growing (attine) ants produce carbohydrate active enzymes that degrade plant material collected by the ants and offer them food in exchange. The spectrum of these enzyme activities is an important symbiont service to the host but may vary among cultivar genotypes. The sympatric occurrence of several Trachymyrmex and Sericomyrmex higher attine ants in Gamboa, Panama provided the opportunity to do a quantitative study of species-level interaction-specificity.ResultsWe genotyped the ants for Cytochrome Oxidase and their Leucoagaricus fungal cultivars for ITS rDNA. Combined with activity measurements for 12 carbohydrate active enzymes, these data allowed us to test whether garden enzyme activity was affected by fungal strain, farming ants or combinations of the two. We detected two cryptic ant species, raising ant species number from four to six, and we show that the 38 sampled colonies reared a total of seven fungal haplotypes that were different enough to represent separate Leucoagaricus species. The Sericomyrmex species and one of the Trachymyrmex species reared the same fungal cultivar in all sampled colonies, but the remaining four Trachymyrmex species largely shared the other cultivars. Fungal enzyme activity spectra were significantly affected by both cultivar species and farming ant species, and more so for certain ant-cultivar combinations than others. However, relative changes in activity of single enzymes only depended on cultivar genotype and not on the ant species farming a cultivar.ConclusionsAnt cultivar symbiont-specificity varied from almost full symbiont sharing to one-to-one specialization, suggesting that trade-offs between enzyme activity spectra and life-history traits such as desiccation tolerance, disease susceptibility and temperature sensitivity may apply in some combinations but not in others. We hypothesize that this may be related to ecological specialization in general, but this awaits further testing. Our finding of both cryptic ant species and extensive cultivar diversity underlines the importance of identifying all species-level variation before embarking on estimates of interaction specificity.

Project description: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.

Project description:Symbiotic Actinobacteria help fungus-growing ants suppress fungal pathogens through the production of antifungal compounds. Trachymyrmex ants of the southwest desert of the United States inhabit a unique niche far from the tropical rainforests in which most fungus-growing ant species are found. These ants may not encounter the specialist fungal pathogen Escovopsis known to threaten colonies of other fungus-growing ants. It is unknown whether Actinobacteria associated with these ants antagonize contaminant fungi and, if so, what the chemical basis of such antagonism is. We find that Pseudonocardia and Amycolatopsis strains isolated from three desert specialist Trachymyrmex species do antagonize diverse contaminant fungi isolated from field-collected ant colonies. We did not isolate the specialist fungal pathogen Escovopsis in our sampling. We trace strong antifungal activity from Amycolatopsis isolates to the molecule ECO-0501, an antibiotic that was previously under preclinical development as an antibacterial agent. In addition to suppression of contaminant fungi, we find that this molecule has strong activity against ant-associated Actinobacteria and may also play a role in bacterial competition in this niche. By studying interspecies interactions in a previously unexplored niche, we have uncovered novel bioactivity for a structurally unique antibiotic. IMPORTANCE Animal hosts often benefit from chemical defenses provided by microbes. These molecular defenses are a potential source of novel antibiotics and offer opportunities for understanding how antibiotics are used in ecological contexts with defined interspecies interactions. Here, we recover contaminant fungi from nests of Trachymyrmex fungus-growing ants of the southwest desert of the United States and find that they are suppressed by Actinobacteria isolated from these ants. The antibiotic ECO-0501 is an antifungal agent used by some of these Amycolatopsis bacterial isolates. This antibiotic was previously investigated in preclinical studies and known only for antibacterial activity.

Dataset Information

The evolution of abdominal microbiomes in fungus-growing ants.

Publications

The evolution of abdominal microbiomes in fungus-growing ants.

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