Leaf-cutting ant fungi produce cell wall degrading pectinase complexes reminiscent of phytopathogenic fungi - PubMed (original) (raw)

Leaf-cutting ant fungi produce cell wall degrading pectinase complexes reminiscent of phytopathogenic fungi

Morten Schiøtt et al. BMC Biol. 2010.

Abstract

Background: Leaf-cutting (attine) ants use their own fecal material to manure fungus gardens, which consist of leaf material overgrown by hyphal threads of the basidiomycete fungus Leucocoprinus gongylophorus that lives in symbiosis with the ants. Previous studies have suggested that the fecal droplets contain proteins that are produced by the fungal symbiont to pass unharmed through the digestive system of the ants, so they can enhance new fungus garden growth.

Results: We tested this hypothesis by using proteomics methods to determine the gene sequences of fecal proteins in Acromyrmex echinatior leaf-cutting ants. Seven (21%) of the 33 identified proteins were pectinolytic enzymes that originated from the fungal symbiont and which were still active in the fecal droplets produced by the ants. We show that these enzymes are found in the fecal material only when the ants had access to fungus garden food, and we used quantitative polymerase chain reaction analysis to show that the expression of six of these enzyme genes was substantially upregulated in the fungal gongylidia. These unique structures serve as food for the ants and are produced only by the evolutionarily advanced garden symbionts of higher attine ants, but not by the fungi reared by the basal lineages of this ant clade.

Conclusions: Pectinolytic enzymes produced in the gongylidia of the fungal symbiont are ingested but not digested by Acromyrmex leaf-cutting ants so that they end up in the fecal fluid and become mixed with new garden substrate. Substantial quantities of pectinolytic enzymes are typically found in pathogenic fungi that attack live plant tissue, where they are known to breach the cell walls to allow the fungal mycelium access to the cell contents. As the leaf-cutting ant symbionts are derived from fungal clades that decompose dead plant material, our results suggest that their pectinolytic enzymes represent secondarily evolved adaptations that are convergent to those normally found in phytopathogens.

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Figures

Figure 1

Figure 1

The life cycle of fecal droplet proteins. (a) Degradation enzymes produced in the gongylidia are passed through the ant alimentary system to end up in the fecal fluid, fecal droplets of which are mixed with the new plant substrate to form leaf pulp that the ants add to the fungus garden. (b) Sodium dodecyl sulfate-polyacrylamide gel electrophoresis (SDS-PAGE) of ant fecal fluid. M, molecular size marker. F, fecal fluid. Excised bands are indicated by numbered boxes in the right-hand version of duplicated lane F.

Figure 2

Figure 2

Pectinolytic enzyme activities in fecal material from ants with access to fungal symbiont food compared to ants deprived of their fungus garden material for 2 weeks. Bars are means ± SE (n = 9).

Figure 3

Figure 3

Expression levels of pectinolytic enzyme genes in gongylidia relative to gongylidia-free mycelium measured with quantitative real-time polymerase chain reaction (qPCR). Bars are means ± SE (n = 4). Statistically significant results are marked with an asterisk. An equal level of gene expression between the two tissues gives a fold change of one (dotted horizontal line).

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