Proteomics reveals synergy between biomass degrading enzymes and inorganic Fenton chemistry in leaf-cutting ant colonies.

Morten Schiøtt,Jacobus J Boomsma

doi:10.7554/elife.61816

Abstract

The symbiotic partnership between leaf-cutting ants and fungal cultivars processes plant biomass via ant fecal fluid mixed with chewed plant substrate before fungal degradation. Here we present a full proteome of the fecal fluid of Acromyrmex leaf-cutting ants, showing that most proteins function as biomass degrading enzymes and that ca. 85% are produced by the fungus and ingested, but not digested, by the ants. Hydrogen peroxide producing oxidoreductases were remarkably common in the proteome, inspiring us to test a scenario in which hydrogen peroxide reacts with iron to form reactive oxygen radicals after which oxidized iron is reduced by other fecal-fluid enzymes. Our biochemical assays confirmed that these so-called Fenton reactions do indeed take place in special substrate pellets, presumably to degrade plant cell wall polymers. This implies that the symbiotic partnership manages a combination of oxidative and enzymatic biomass degradation, an achievement that surpasses current human bioconversion technology.

Highlights

The symbiotic partnership between leaf-cutting ants and fungal cultivars processes plant biomass via ant fecal fluid mixed with chewed plant substrate before fungal degradation
The deep ancestors of the attine ants and their fungal cultivars were hunter-gatherers and saprotrophs, respectively, which implies that none of them were adapted for efficiently degrading fresh plant material
Most of the leaves that the ants harvest are heavily protected against herbivory by recalcitrant cell walls and toxic substances (Chen 2008), defences that needed to be overcome for obtaining net nutrition

Summary

Introduction

The symbiotic partnership between leaf-cutting ants and fungal cultivars processes plant biomass via ant fecal fluid mixed with chewed plant substrate before fungal degradation. Our biochemical assays confirmed that these so-called Fenton reactions do take place in special substrate pellets, presumably to degrade plant cell wall polymers. This implies that the symbiotic partnership manages a combination of oxidative and enzymatic biomass degradation, an achievement that surpasses current human bioconversion technology. The ants cut leaf fragments from the canopy and understory and bring them back to their nest to be processed as growth substrate for the cultivar This involves chewing forage material into smaller pieces, which are mixed with fecal fluid and deposited as new substrate on the actively growing parts of the garden (Weber 1966). The crown group of the attine ants underwent significant changes in their gut microbiota that likely facilitated the conversion efficiency of fungal diet substrate into ant biomass (Sapountzis et al 2015; 2019)

Methods

Results

Conclusion