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Open Access Highly Accessed Research article

The fungal symbiont of Acromyrmex leaf-cutting ants expresses the full spectrum of genes to degrade cellulose and other plant cell wall polysaccharides

Morten N Grell1*, Tore Linde13, Sanne Nygaard3, Kåre L Nielsen2, Jacobus J Boomsma3 and Lene Lange1

Author Affiliations

1 Department of Biotechnology, Chemistry and Environmental Engineering, Aalborg University, A.C. Meyers Vænge 15, DK-2450, Copenhagen, Denmark

2 Department of Biotechnology, Chemistry and Environmental Engineering, Aalborg University, Sohngårdsholmsvej 49, DK-9000, Aalborg, Denmark

3 Centre for Social Evolution, Department of Biology, University of Copenhagen, Universitetsparken 15, DK-2100, Copenhagen, Denmark

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BMC Genomics 2013, 14:928  doi:10.1186/1471-2164-14-928

Published: 28 December 2013

Abstract

Background

The fungus gardens of leaf-cutting ants are natural biomass conversion systems that turn fresh plant forage into fungal biomass to feed the farming ants. However, the decomposition potential of the symbiont Leucocoprinus gongylophorus for processing polysaccharides has remained controversial. We therefore used quantifiable DeepSAGE technology to obtain mRNA expression patterns of genes coding for secreted enzymes from top, middle, and bottom sections of a laboratory fungus-garden of Acromyrmex echinatior leaf-cutting ants.

Results

A broad spectrum of biomass-conversion-relevant enzyme genes was found to be expressed in situ: cellulases (GH3, GH5, GH6, GH7, AA9 [formerly GH61]), hemicellulases (GH5, GH10, CE1, GH12, GH74), pectinolytic enzymes (CE8, GH28, GH43, PL1, PL3, PL4), glucoamylase (GH15), α-galactosidase (GH27), and various cutinases, esterases, and lipases. In general, expression of these genes reached maximal values in the bottom section of the garden, particularly for an AA9 lytic polysaccharide monooxygenase and for a GH5 (endocellulase), a GH7 (reducing end-acting cellobiohydrolase), and a GH10 (xylanase), all containing a carbohydrate binding module that specifically binds cellulose (CBM1). Although we did not directly quantify enzyme abundance, the profile of expressed cellulase genes indicates that both hydrolytic and oxidative degradation is taking place.

Conclusions

The fungal symbiont of Acromyrmex leaf-cutting ants can degrade a large range of plant polymers, but the conversion of cellulose, hemicellulose, and part of the pectin occurs primarily towards the end of the decomposition process, i.e. in the bottom section of the fungus garden. These conversions are likely to provide nutrients for the fungus itself rather than for the ants, whose colony growth and reproductive success are limited by proteins obtained from ingesting fungal gongylidia. These specialized hyphal tips are hardly produced in the bottom section of fungus gardens, consistent with the ants discarding old fungal biomass from this part of the garden. The transcripts that we found suggest that actively growing mycelium in the bottom of gardens helps to maintain an optimal water balance to avoid hyphal disintegration, so the ants can ultimately discard healthy rather than decaying and diseased garden material, and to buffer negative effects of varying availability and quality of substrate across the seasons.

Keywords:
Acromyrmex echinatior; Attine ants; Biomass conversion; Carbohydrate-active enzymes (CAZymes); DeepSAGE; Fungus garden; Leucocoprinus gongylophorus; Symbiosis; Transcript profiling