Abstract
BackgroundThe 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.ResultsA 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.ConclusionsThe 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.
Highlights
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
Some full-length coding sequences were obtained from the Expressed sequence tag (EST) library, but all selected genes were subsequently retrieved from the low coverage genome, which confirmed the selected EST library hits to be of L. gongylophorus origin
After analyzing genes expressed by the fungusgarden symbiont in situ, we conclude that L. gongylophorus is producing all enzymes necessary for degrading the major plant-cell-wall polysaccharides: cellulose, hemicellulose, and pectin
Summary
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. To accelerate the subsequent decomposition process, the ants chew the leaf fragments into small pieces and mix the leaf-pulp with fecal droplets [7,8] This fluid contains substantial quantities of enzymes that the ants ingested with fungal material but without digesting them [7,8,9], so that new hyphal growth can quickly access the most valuable resources inside the plant cells [10]. Studies by Schiøtt et al [7] and De Fine Licht et al [8] have shown that expression of these enzymes tends to be upregulated in the fungal gongylidia, the unique inflated hyphal tips that are harvested by the ants [11,12]. Most notable among these ant-vectored enzymes are proteases, cellulases acting on amorphous cellulose, laccases, and pectinases [7,8,9,13,14]
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