ArticleProceedings of the National Academy of Sciences of the United States of America2013
Laccase detoxification mediates the nutritional alliance between leaf-cutting ants and fungus-garden symbionts.
Article in Proceedings of the National Academy of Sciences of the United States of America, 2013. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 58 papers.
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Who cites it
58 citing papers in PubMed, 135 citations in OpenAlex.
- Leafcutter Ant Farmers Prevent Loss of Edible Symbiotic Structures by Maintaining Allelic Diversity in Their Multinucleate Fungal Crop.Molecular ecology · 2026Article
- The multifaceted physiological roles of fungal laccases.Communications biology · 2026Review
- You are what your fungus eats: diet shapes the microbial garden of a fungus-growing ant.NPJ biofilms and microbiomes · 2025Article
- Evidence of cellular adaptations in a fungal cultivar promoting resource exchange with leafcutter ant farmers.Biology letters · 2025Article
- Examining the Assembly of the Bacterial Community Associated with the Fungus Garden of Atta mexicana (Hymenoptera: Formicidae): Does Queen Origin Matter?Current microbiology · 2025Article
- Ambrosia gall midges (Diptera: Cecidomyiidae) and their microbial symbionts as a neglected model of fungus-farming evolution.FEMS microbiology reviews · 2025Review
- On the Origins of Symbiotic Fungi in Carmine Cochineals and Their Function in the Digestion of Plant Polysaccharides.Insects · 2024Article
- Genomic Signatures of Domestication in a Fungus Obligately Farmed by Leafcutter Ants.Molecular biology and evolution · 2024Article
- Two +ssRNA mycoviruses cohabiting the fungal cultivar of leafcutter ants.Virology journal · 2024Article
- An at-leg pellet and associated Penicillium sp. provide multiple protections to mealybugs.Communications biology · 2024Article
- Phylogenomics of the Ecdysteroid Kinase-like (EcKL) Gene Family in Insects Highlights Roles in Both Steroid Hormone Metabolism and Detoxification.Genome biology and evolution · 2024Article
- The fungusFrontiers in fungal biology · 2024Review
- Article
- Nutritional challenges of feeding a mutualist: Testing for a nutrient-toxin tradeoff in fungus-farming leafcutter ants.Ecology · 2022Article
- The Symbiotic FungusInsects · 2022Review
- A fungal symbiont converts provisioned cellulose into edible yield for its leafcutter ant farmers.Biology letters · 2022Article
- Lessons From Insect Fungiculture: From Microbial Ecology to Plastics Degradation.Frontiers in microbiology · 2022Article
- Demonstrating the role of symbionts in mediating detoxification in herbivores.Symbiosis (Philadelphia, Pa.) · 2022Article
- Molecular Rationale of Insect-Microbes Symbiosis-From Insect Behaviour to Mechanism.Microorganisms · 2021Review
- The multidimensional nutritional niche of fungus-cultivar provisioning in free-ranging colonies of a neotropical leafcutter ant.Ecology letters · 2021Article
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Authors and funding
6 authors at 2 institutions in 1 country.
Funding
No grant is acknowledged in the PubMed record.
Abstract
Leaf-cutting ants combine large-scale herbivory with fungus farming to sustain advanced societies. Their stratified colonies are major evolutionary achievements and serious agricultural pests, but the crucial adaptations that allowed this mutualism to become the prime herbivorous component of neotropical ecosystems has remained elusive. Here we show how coevolutionary adaptation of a specific enzyme in the fungal symbiont has helped leaf-cutting ants overcome plant defensive phenolic compounds. We identify nine putative laccase-coding genes in the fungal genome of Leucocoprinus gongylophorus cultivated by the leaf-cutting ant Acromyrmex echinatior. One of these laccases (LgLcc1) is highly expressed in the specialized hyphal tips (gongylidia) that the ants preferentially eat, and we confirm that these ingested laccase molecules pass through the ant guts and remain active when defecated on the leaf pulp that the ants add to their gardens. This accurate deposition ensures that laccase activity is highest where new leaf material enters the fungus garden, but where fungal mycelium is too sparse to produce extracellular enzymes in sufficient quantities to detoxify phenolic compounds. Phylogenetic analysis of LgLcc1 ortholog sequences from symbiotic and free-living fungi revealed significant positive selection in the ancestral lineage that gave rise to the gongylidia-producing symbionts of leaf-cutting ants and their non-leaf-cutting ant sister group. Our results are consistent with fungal preadaptation and subsequent modification of a particular laccase enzyme for the detoxification of secondary plant compounds during the transition to active herbivory in the ancestor of leaf-cutting ants between 8 and 12 Mya.
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