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. Most of the organic carbon in land plants is stocked as lignocellulose 1 , a recalcitrant mesh constituted by biopolymers including cellulose, hemicellulose, pectin, and lignin 2,3. For feeding on recalcitrant and indigestible lignocellulosic plant tissues, herbivorous animals rely largely on the association with symbiotic microorganisms, which mediates the use of otherwise non-accessible resources 4-7. Besides metabolizing plant biomass components by hydrolysis and fermentation, the host-associated microbiota also assists the detoxification of plant-derived defensive secondary compounds 4,7,8. A fascinating example of insect-microbial symbiosis for exploring recalcitrant plant biomass is observed in fungus-growing insects (FGI), which maintain lignocellulolytic fungi as crops 9. The active maintenance of fungus crops, also known as fungiculture, evolved independently in three insect lineages 9 : ants in the subtribe Attina (Hymenoptera: Formicidae: Myrmicinae, "the attines"), which are strict to the New World 10,11 ; beetles in the subfamilies Scolytinae and Platypodinae (Coleoptera: Curculionidae), which are predominantly found in tropical and subtropical ecosystems 12 ; and termites in the subfamily Macrotermitinae (Isoptera: Termitidae), which occur in the Old-World tropics, mainly in Africa and Asia 13. The fungal lignocellulose-degrading capacity has been fundamental for the evolutionary succes...

Leaf-cutting ants employ diverse behavioral strategies for promoting the growth of fungal cultivars in a structure known as fungus garden. As a nutritionally rich resource for the ants, the fungal crop is threatened by microbial antagonists and pathogens. Strategies for protecting the garden against harmful microbes have been described in detail, although the process of microbial threat recognition is not fully understood. Here, we review the literature on leaf-cutting ants' social immunity traits, in search of possibilities by which workers recognize harmful microbes in their system. Based on current data, we suggest mechanisms regarding (1) chemical recognition, where discrimination could be related to chemical cues from the antagonistic microbe or semiochemicals released by the fungus garden during harmful interactions, or (2) through associative learning when workers would connect the microbe cues with a damage in the fungus garden, developing a "colony-level memory" toward this threat. We also discuss evidence supporting ant-fungus communication as key for maintaining the health of the fungus garden, as well as experimental setups for future evaluation of threat detection and recognition by leaf-cutting ants.

Syncephalastrum sp. treatment resulted in progressive damage in subcolonies. The interactions among Syncephalastrum sp., fungus garden and ants offer new opportunities in integrated pest management of leaf-cutter ants. © 2016 Society of Chemical Industry.

Health and disease emerge from intricate interactions between genotypes, phenotypes, and environmental features. The outcomes of such interactions are context-dependent, existing as a dynamic continuum ranging from benefits to damage. In host-microbial interactions, both the host and environmental conditions modulate the pathogenic potential of a microorganism. Microbial interactions are the core of the agricultural systems of ants in the subtribe Attina, which cultivate basidiomycete fungi for food. The fungiculture environment harbors a diverse microbial community, including fungi in the genus Escovopsis that has been studied as damage-causing agent. Here, we consider the ant colony as a host and investigate to what extent its health impacts the dynamics and outcomes of host-Escovopsis interactions. We found that different ant fungal cultivars vary in susceptibility to the same Escovopsis strains in plate-assays interactions. In subcolony-Escovopsis interactions, while healthy subcolonies gradually recover from infection with different concentrations of Escovopsis conidia, insecticide-treated subcolonies evidenced traits of infection and died within 7 days. The opportunistic nature of Escovopsis infections indicates that diseases in attine fungiculture are a consequence of host susceptibility, rather than the effect of a single microbial agent. By addressing the host susceptibility as a major modulator of Escovopsis pathogenesis, our findings expand the understanding of disease dynamics within attine colonies.

Anthropogenic activities have extensively transformed the biosphere by extracting and disposing of resources, crossing boundaries of planetary threat while causing a global crisis of waste overload. Despite fundamental differences regarding structure and recalcitrance, lignocellulose and plastic polymers share physical-chemical properties to some extent, that include carbon skeletons with similar chemical bonds, hydrophobic properties, amorphous and crystalline regions. Microbial strategies for metabolizing recalcitrant polymers have been selected and optimized through evolution, thus understanding natural processes for lignocellulose modification could aid the challenge of dealing with the recalcitrant human-made polymers spread worldwide. We propose to look for inspiration in the charismatic fungal-growing insects to understand multipartite degradation of plant polymers. Independently evolved in diverse insect lineages, fungiculture embraces passive or active fungal cultivation for food, protection, and structural purposes. We consider there is much to learn from these symbioses, in special from the community-level degradation of recalcitrant biomass and defensive metabolites. Microbial plant-degrading systems at the core of insect fungicultures could be promising candidates for degrading synthetic plastics. Here, we first compare the degradation of lignocellulose and plastic polymers, with emphasis in the overlapping microbial players and enzymatic activities between these processes. Second, we review the literature on diverse insect fungiculture systems, focusing on features that, while supporting insects’ ecology and evolution, could also be applied in biotechnological processes. Third, taking lessons from these microbial communities, we suggest multidisciplinary strategies to identify microbial degraders, degrading enzymes and pathways, as well as microbial interactions and interdependencies. Spanning from multiomics to spectroscopy, microscopy, stable isotopes probing, enrichment microcosmos, and synthetic communities, these strategies would allow for a systemic understanding of the fungiculture ecology, driving to application possibilities. Detailing how the metabolic landscape is entangled to achieve ecological success could inspire sustainable efforts for mitigating the current environmental crisis.