The fungus gardens of leaf‐cutter ants undergo a distinct physiological transition during biomass degradation

Abstract

Leaf-cutter ants are dominant herbivores in ecosystems throughout the Neotropics that feed on fungus gardens cultivated on fresh foliar biomass. Although recent investigations have shed light on how plant biomass is degraded in fungus gardens, the cycling of nutrients that takes place in these specialized microbial ecosystems is still not well understood. Here, using metabolomic and metaproteomic techniques, we examine the dynamics of nutrient turnover in these gardens. Our results reveal that numerous free amino acids and sugars are depleted throughout the process of biomass degradation, indicating that easily accessible nutrients from plant material are readily consumed by microbes in these ecosystems. Accumulation of cellobiose and lignin derivatives near the end of the degradation process is consistent with previous characterization of lignocellulases produced by the fungal cultivar of the ants. Our results also suggest that ureides may be an important source of nitrogen in fungus gardens, especially during nitrogen-limiting conditions. No free arginine was detected in our metabolomic experiments despite evidence that the host ants cannot produce this amino acid, suggesting that biosynthesis of this metabolite may be tightly regulated in fungus gardens. These results provide new insights into microbial community-level processes that underlie this important ant-fungus symbiosis.

The good, the bad and the tasty: The many roles of mushrooms

“…In the middle section of the garden, L. gongylophorus produces the gongylidia that contain laccases, proteases, pectinases, hemicelluloses, cellulases and xylanases for digestion of plant tissues and are ingested by the ants and their larvae. The top of the garden contains limited fungal biomass and it is here that the ants add new plant material, masticating it into smaller fragments and depositing faecal fluid containing the fungal-derived digestive enzymes from the ingested gongylidia to facilitate degradation (Grell et al., 2013, Huang et al., 2014). The ants also inoculate new plant material with fragments of mycelium from the older, lower part of the garden to expedite digestion.…”

Active Site and Laminarin Binding in Glycoside Hydrolase Family 55

“…In addition to the well documented cellulolytic activity of microbes that inhabit the digestive tracks of termites (3), newer paradigms for insect/microbe symbiotic interactions have been recently described in leaf cutter ants (1,2,4,5), pine beetles (6), and wood wasps (7). For example, the highly invasive pinewood-boring wasp Sirex noctilio deposits a fungal/bacterial community into the pine tree when it lays eggs (8).…”

The MPLEx Protocol for Multi-omic Analyses of Soil Samples

“…While the MPLEx protocol has been well-established for general extraction of lipids and metabolites 12,13,14,15,16,17,18,19,20,21,22,23,24,25,26,27,28,29,30,34, its comparison to common soil protein extraction methods for microbial analyses, such as soil protein extraction kits (see Table of Materials ) and SDS (sodium dodecyl sulfate) extractions 35 , is further evaluated here. To assess these techniques, Kansas native prairie soil proteins were extracted with each approach and analyzed directly with reversed-phase LC-MS/MS using a UPLC system coupled with a hybrid quadrupole/Orbitrap mass spectrometer.…”

“…This method was originally developed for total lipid extractions 9,11 and more recently was amended for the simultaneous extraction of metabolites, proteins, and lipids from a single sample 12,13,14,15,16,17,18,19,20,21,22,23,24,25,26,27,28,29,30, enabling less sample quantity and experimental variability 10 . In the MPLEx protocol, chloroform is not miscible with water, which provides the basis for the triphasic chemical separation of sample constituents into distinct fractions.…”