Evidence that the Domesticated Fungus Leucoagaricus gongylophorus Recycles its Cytoplasmic Contents as Nutritional Rewards to Feed its Leafcutter Ant Farmers

Summary

This research reveals how a fungus farmed by leafcutter ants produces specialized food structures for the ants by recycling its own cellular contents through a process called autophagy. This finding helps explain how this ancient farming partnership between ants and fungi has remained stable for millions of years. Impacts on everyday life: – Provides insights into how organisms can form stable, mutually beneficial partnerships – Advances our understanding of cellular recycling processes that are important across biology – Offers potential applications for improving agricultural crop development – Demonstrates how microscopic processes can maintain large-scale ecological relationships – Could inform development of sustainable farming practices based on natural systems

Background

Leafcutter ants farm a fungal cultivar (Leucoagaricus gongylophorus) that converts inedible vegetation into food that sustains colonies with up to millions of workers. The fungus has evolved specialized nutritional rewards called gongylidia – swollen hyphal cells that package metabolites and are consumed by ant farmers. However, little is known about how gongylidia form and how fungal physiology and ant provisioning collectively govern farming performance.

Objective

To explore the process of gongylidium formation using advanced microscopy to image the cultivar at nanometer scales, and both in vitro experiments and in silico analyses to examine the mechanisms of gongylidia formation when isolated from ant farmers. The study aimed to test whether autophagy and plant-fragment provisioning by ants provide alternative and/or complementary pathways for gongylidium formation.

Results

The imaging showed that the cultivar uses autophagy to recycle its own cellular material and shuttles resulting metabolites into a vacuole whose expansion creates the gongylidium’s bulging appearance. In vitro experiments demonstrated that autophagy inhibitors significantly reduced gongylidia formation. Transcriptomic analyses revealed upregulation of multiple autophagy gene isoforms in gongylidia compared to undifferentiated hyphae. The study found that gongylidia contain thin cell walls (120-220nm) and use complex branching patterns mediated by nuclear distributions.

Conclusion

The study reveals that autophagy drives the morphogenesis of nutritional rewards produced by L. gongylophorus for leafcutter ant farmers. This autophagic mechanism provides a way to maintain higher level homeostasis in the farming symbiosis. The distinctive morphology, ontogeny and physiology of gongylidia make them unique within the fungal kingdom and exemplify true crop domestication, as the nutrients are not recycled back into fungal metabolism but are dedicated solely to feeding the ant farmers.
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