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

Abstract

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...

The coevolutionary history of the microbial planet

“…Remarkably, these farming ants and their cultivar form the crux of a multi‐partite symbiosis that involves several other fungi and bacteria, and new members continue to be discovered (Poulsen and Currie, 2006). Interactions in the leaf‐cutter ant symbiosis vary in their strength and the degree to which members have co‐evolved; some are cases of clear co‐evolution in that they exhibit reciprocal adaptation, while other interactions are more transient or may lack specificity (Pinto‐Tomás et al ., 2009; Aylward et al ., 2014; Barcoto et al ., 2020). What I find most remarkable about this symbiosis is how the evolutionary trajectories of all of the partners are intertwined to varying degrees, forming a complex co‐evolutionary web in which each member uniquely shapes the ecology and selective pressures on the others.…”

Pseudomonascan prevent the parasitic fungus, while keeping the crop fungus unaffected, in the gardens ofOdontotermes obesus

“…This multi-level convergent evolution suggests the importance of such secondary microbes in maintaining successful nutritional symbiosis across all fungus-growing insects [18,19]. The evolutionary logic for the presence of such mutualistic microbes within these symbioses is inescapable.…”

“…The presence of fungicide-producing mutualistic microbes in fungus-growing ants, which arguably suppresses the growth of parasitic fungi in their colonies [12][13][14][15], points to a similar role of secondary bacterial symbionts in fungus-growing termites as well [16,17]. This conjecture is strengthened by the fact that even after cultivating very divergent crop fungi, the microbiota across all insect-fungal systems shows a remarkable phylogenetic and compositional similarity [18,19]. This multi-level convergent evolution suggests the importance of such secondary microbes in maintaining successful nutritional symbiosis across all fungus-growing insects [18,19].…”

Pseudomonas Can Prevent the Parasitic Fungus, While Keeping the Crop Fungus Unaffected, in the Gardens of Odontotermes Obesus.

“…The presence of fungicide-producing mutualistic microbes in fungus-growing ants, which arguably suppresses the growth of parasitic fungi in their colonies [12][13][14][15], points to a similar role of secondary bacterial symbionts in fungus-growing termites as well [16,17]. This conjecture is strengthened by the fact that even after cultivating very divergent crop fungi, the microbiota across all insect-fungal systems shows a remarkable phylogenetic and compositional similarity [18,19]. This multi-level convergent evolution suggests the importance of such secondary microbes in maintaining successful nutritional symbiosis across all fungusgrowing insects [18,19].…”

“…This conjecture is strengthened by the fact that even after cultivating very divergent crop fungi, the microbiota across all insect-fungal systems shows a remarkable phylogenetic and compositional similarity [18,19]. This multi-level convergent evolution suggests the importance of such secondary microbes in maintaining successful nutritional symbiosis across all fungusgrowing insects [18,19]. The evolutionary logic for the presence of such mutualistic microbes within these symbioses is inescapable.…”