A fungal symbiont converts provisioned cellulose into edible yield for its leafcutter ant farmers

Abstract

While ants are dominant consumers in terrestrial habitats, only the leafcutters practice herbivory. Leafcutters do this by provisioning a fungal cultivar (Leucoagaricus gongylophorus) with freshly cut plant fragments and harnessing its metabolic machinery to convert plant mulch into edible fungal tissue (hyphae and swollen hyphal cells called gongylidia). The cultivar is known to degrade cellulose, but whether it assimilates this ubiquitous but recalcitrant molecule into its nutritional reward structures is unknown. We use in vitro experiments with isotopically labelled cellulose to show that fungal cultures from an Atta colombica leafcutter colony convert cellulose-derived carbon into gongylidia, even when potential bacterial symbionts are excluded. A laboratory feeding experiment showed that cellulose assimilation also occurs in vivo in A. colombica colonies. Analyses of publicly available transcriptomic data further identified a complete, constitutively expressed, cellulose-degradation pathway in the fungal cultivar. Confirming leafcutters use cellulose as a food source sheds light on the eco-evolutionary success of these important herbivores.

Keywords: Atta; Leucoagaricus; gongylidia; herbivory; nutrition; stable isotope.

Figure 1.

Isotopic evidence that the fungal cultivar assimilates carbon (C) from cellulose molecules. (a) An in vitro experiment detected significant overall ¹³C enrichment in fungal hyphae and staphylae on ¹³C-enriched media compared to the control. Levels of ¹³C enrichment for staphylae and hyphae did not differ between isotopic enrichment treatments but staphylae were more enriched than hyphae. Letters show groupings based on pairwise tests (p_adj < 0.05). (b) An in vivo experiment showed that staphylae and hyphae were significantly ¹³C-enriched after 2 days compared to baseline natural abundance with no significant differences between fungal tissues. Z-scores relative to control/baseline, diamonds indicate means.

Figure 2.

The fungal cultivar can directly metabolise and assimilate cellulose. (a) A complete cellulose-degradation pathway was identified from transcriptomic data. (b) The in vitro cultivar remained significantly ¹³C-enriched relative to the baseline natural abundance (control) when bacteria were specifically excluded using antibiotics. Z-scores relative to control, diamonds indicate means, letters show groupings based on pairwise tests (p_adj < 0.05).