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

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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.

Data availability

The mass spectrometry data generated in this project as well as the amino acid sequences used for protein identification have been submitted to the PRIDE Archive with accession number PXD016395. All other data is provided in the Supplementary Table S1 and the source data files provided for Figures 3 and 4.

The following data sets were generated

1. Schiøtt M
2. Boomsma
3. JJ
(2020) Leaf-cutting ant feces LC-MS/MS
PRIDE, PXD016395.

https://www.ebi.ac.uk/pride/archive/projects/PXD016395

Article and author information

Author details

Morten Schiøtt

Centre for Social Evolution, Department of Biology, University of Copenhagen, Copenhagen, Denmark

For correspondence
mosch@aqua.dtu.dk

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-4309-8090
Jacobus J Boomsma

Centre for Social Evolution, Department of Biology, University of Copenhagen, Copenhagen, Denmark

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-3598-1609

Funding

Danmarks Grundforskningsfond (DNRF57)

Jacobus J Boomsma

H2020 European Research Council (Advanced Grant 323085)

Jacobus J Boomsma

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.