microbiota-attine-ants-gardens-visualizing-microbial-landscape

Microbiota of Attine Ants' Gardens: Visualizing a Microbial Landscape by Scanning Electron Microscopy

In macroscale ecosystems, such as rainforests or coral reefs, the spatial localization of organisms is the basis of our understanding of community ...

São Paulo State University (UNESP)

Some lineages of ants, termites, and beetles independently evolved a symbiotic association with lignocellulolytic fungi cultivated for food, in a lifestyle known as fungiculture. Fungus-growing insects' symbiosis also hosts a bacterial community thought to integrate their physiology. Similarities in taxonomic composition support the microbiota of fungus-growing insects as convergent, despite differences in fungus-rearing by these insects. Here, by comparing fungus-growing insects to several hosts ranging diverse dietary patterns, we investigate whether the microbiota taxonomic and functional profiles are characteristic of the fungiculture environment. Compared to other hosts, the microbiota associated with fungus-growing insects presents a distinctive taxonomic profile, dominated by Gammaproteobacteria at class level and by Pseudomonas at genera level. Even with a functional profile presenting similarities with the gut microbiota of herbivorous and omnivorous hosts, some differentially abundant features codified by the microbiota of fungus-growing insects suggest these communities occupying microhabitats that are characteristic of fungiculture. These features include metabolic pathways involved in lignocellulose breakdown, detoxification of plant secondary metabolites, metabolism of simple sugars, fungal cell wall deconstruction, biofilm formation, antimicrobials biosynthesis, and metabolism of diverse nutrients. Our results suggest that the microbiota could be functionally adapted to the fungiculture environment, codifying metabolic pathways potentially relevant to the fungus-growing insects' ecosystems functioning.

Fungus-growing insects host a distinctive microbiota apparently adapted to the fungiculture environment.

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.

Uncovering the Yeast Communities in Fungus-Growing Ant Colonies.

In varied environments, microorganisms search for partners or nutritional resources using chemical signals. Microbes are drawn (chemotaxis) or grow directionally (chemotropism) towards the chemical source, enabling them to establish and maintain symbiosis. The hypocrealean fungi Escovopsis enhance their growth towards the basidiomycete fungus Leucoagaricus gongylophorus, which is cultivated by leaf-cutting attine ants for food. Although directional growth is well documented in this symbiosis, it is unclear whether non-volatile or volatile organic compounds participate in the interaction between cultivar and Escovopsis, and which specific chemical compounds might attract and induce chemotropism. In this study, we examined the growth responses of Escovopsis isolates to non-volatile and volatile organic compounds produced by fungal cultivars of higher attine ants. We also isolated and identified molecules released by the ant-cultivar and assessed the chemotropism of Escovopsis towards them. Our results indicate that the growth of Escovopsis is stimulated in the presence of both non-volatile and volatile compounds from fungal cultivars. We also identified three isomeric diketopiperazines molecules from crude extracts of the ant cultivar, suggesting that these might play a role in Escovopsis chemotropism. Our findings provide insights into the complex chemical interactions that govern the association between Escovopsis and fungal cultivars.

Fungal Cultivars of Higher Attine Ants Promote Escovopsis Chemotropism.

Endophytic fungi are a diverse group of microorganisms that reside within plant tissues and play a crucial ecological role in the development of their hosts. Psidium cattleianum (Myrtales: Myrtaceae: 'Cattley guava') is a Brazilian native species with economic potential due to the diverse applications of its fruits, wood, and essential oils. Despite their significance, the diversity of endophytic fungi associated with P. cattleianum remains unexplored. Here, we investigated the diversity of endophytic fungi in the leaves of this plant using cultivation-dependent isolation methods, analysis of the macroscopic characters of the isolates, and phylogenetic analyses employing the ITS barcode marker. A total of 396 isolates, classified into 25 fungal taxa, were obtained, namely, Alternaria, Aspergillus, Cladosporium, Colletotrichum, Coprinellus, Coriolopsis, Diaporthe, Induratia, Mycosphaerella, Muyocoprom, Myrmecridium, Neofusicoccum, Pantospora, Paracamarosporium, Parapallidocercospora, Paraphaeosphaeria, Penicillium, Perenniporia, Phaeophleospora, Phyllosticta, Pseudofusicoccum, Talaromyces, Xylaria, Sordariomycetes, and Xylariomycetes. Our findings reveal a significant diversity of fungi associated with P. cattleianum leaves; however, our study suggests an even greater diversity of fungi associated with this plant species. Interestingly, although P. cattleianum shares endophytic fungi with other plants in the Myrtaceae family, this plant species harbors a unique fungal community. This distinction is evidenced by certain fungal genera and seven potentially new phylogenetic species, isolated in this study.

Article	Year
Fungus-growing insects host a distinctive microbiota apparently adapted to the fungiculture environment. Scientific reports\| PubMed ID: 32709946	2020
Uncovering the Yeast Communities in Fungus-Growing Ant Colonies. Microbial ecology\| PubMed ID: 35962280	2023
Fungal Cultivars of Higher Attine Ants Promote Escovopsis Chemotropism. Current microbiology\| PubMed ID: 38063979	2023
Culture-dependent methods revel the diversity of endophytic fungi of Psidium cattleianum leaves (Myrtales: Myrtaceae). Brazilian journal of microbiology : [publication of the Brazilian Society for Microbiology]\| PubMed ID: 39155340	2024

Andre Rodrigues

Biography

JoVE Journal Publications

Other Publications