Abstract
The degradation of live plant biomass in fungus gardens of leaf-cutting ants is poorly characterised but fundamental for understanding the mutual advantages and efficiency of this obligate nutritional symbiosis. Controversies about the extent to which the garden-symbiont Leucocoprinus gongylophorus degrades cellulose have hampered our understanding of the selection forces that induced large scale herbivory and of the ensuing ecological footprint of these ants. Here we use a recently established technique, based on polysaccharide microarrays probed with antibodies and carbohydrate binding modules, to map the occurrence of cell wall polymers in consecutive sections of the fungus garden of the leaf-cutting ant Acromyrmex echinatior. We show that pectin, xyloglucan and some xylan epitopes are degraded, whereas more highly substituted xylan and cellulose epitopes remain as residuals in the waste material that the ants remove from their fungus garden. These results demonstrate that biomass entering leaf-cutting ant fungus gardens is only partially utilized and explain why disproportionally large amounts of plant material are needed to sustain colony growth. They also explain why substantial communities of microbial and invertebrate symbionts have evolved associations with the dump material from leaf-cutting ant nests, to exploit decomposition niches that the ant garden-fungus does not utilize. Our approach thus provides detailed insight into the nutritional benefits and shortcomings associated with fungus-farming in ants.
Highlights
Leaf-cutting ants are conspicuous New-World herbivores comprised of ca. 45 species divided into two genera, Atta and Acromyrmex
The three major classes of cell wall polysaccharides, pectins, hemicelluloses and cellulose are held together in walls with increasing degrees of firmness by different chemical bonds and supramolecular associations. These were sequentially extracted from the fungus garden using three solvents CDTA, NaOH and cadoxen, respectively, so that our results provide information not just about the relative abundance of polymers per se, and about the disassembly of higher order cell wall architectures
Combining these data across the three extractions provided an overview of the changes in cell wall epitope levels as plant material is processed through the fungus garden (Figure 3) and of the overall fold changes in polysaccharides relative to levels in the starting leaf material (Figure S1)
Summary
Leaf-cutting ants are conspicuous New-World herbivores comprised of ca. 45 species divided into two genera, Atta and Acromyrmex. 45 species divided into two genera, Atta and Acromyrmex They form the monophyletic crown group of the attine fungus-growing ants, capable of harvesting over half a ton per year of live vegetation per colony and playing a significant role in nutrient transport and (sub)tropical ecosystems [1,2]. In order to deconstruct plant biomass into usable nutrients such as simpler sugars, leaf-cutting ants rely on an obligate symbiosis with fungus gardens that are assemblies of microbes dominated by the basidiomycete fungus Leucocoprinus gongylophorus (Agaricales: Agaricaceae) [1,4]. While leaf-cutting ants provide their fungus gardens with plant material to sustain its growth, the fungus provides food for the ants and their brood in the form of specialized inflated hyphal tips (gongylidia) which the ants excise, consume and feed to their larvae [5,6]. The unique characteristics of these multipartite ant-symbiont relationships have led this mutualism to become a model system for studying social evolution at multiple levels [8,9,10,11]
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