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Title: 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. Rather than directly consuming the fresh foliar biomass they harvest, these ants use it to cultivate specialized fungus gardens. 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 metametabolomics and metaproteomics techniques, we examine the dynamics of nutrient turnover and biosynthesis 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 findings of cellulases and laccases produced by Leucoagaricus gongylophorus, the fungus cultivated by leaf-cutter 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 metametabolomics experiments despite evidence that the host ants cannot produce this amino acid, suggesting that biosynthesis of this metabolite may be tightly regulated in the fungus garden. Thesemore » results provide new insights into the dynamics of nutrient cycling that underlie this important ant-fungus symbiosis.« less

Authors:
; ; ; ; ; ; ; ; ; ;
Publication Date:
Research Org.:
Pacific Northwest National Laboratory (PNNL), Richland, WA (US), Environmental Molecular Sciences Laboratory (EMSL)
Sponsoring Org.:
USDOE
OSTI Identifier:
1170464
Report Number(s):
PNNL-SA-96938
34708; KP1601010
DOE Contract Number:
AC05-76RL01830
Resource Type:
Journal Article
Resource Relation:
Journal Name: Environmental Microbiology Reports, 6(4):389-95
Country of Publication:
United States
Language:
English
Subject:
Environmental Molecular Sciences Laboratory

Citation Formats

Huang, Eric L., Aylward, Frank O., Kim, Young-Mo, Webb-Robertson, Bobbie-Jo M., Nicora, Carrie D., Hu, Zeping, Metz, Thomas O., Lipton, Mary S., Smith, Richard D., Currie, Cameron R., and Burnum-Johnson, Kristin E.. The fungus gardens of leaf-cutter ants undergo a distinct physiological transition during biomass degradation. United States: N. p., 2014. Web. doi:10.1111/1758-2229.12163.
Huang, Eric L., Aylward, Frank O., Kim, Young-Mo, Webb-Robertson, Bobbie-Jo M., Nicora, Carrie D., Hu, Zeping, Metz, Thomas O., Lipton, Mary S., Smith, Richard D., Currie, Cameron R., & Burnum-Johnson, Kristin E.. The fungus gardens of leaf-cutter ants undergo a distinct physiological transition during biomass degradation. United States. doi:10.1111/1758-2229.12163.
Huang, Eric L., Aylward, Frank O., Kim, Young-Mo, Webb-Robertson, Bobbie-Jo M., Nicora, Carrie D., Hu, Zeping, Metz, Thomas O., Lipton, Mary S., Smith, Richard D., Currie, Cameron R., and Burnum-Johnson, Kristin E.. Fri . "The fungus gardens of leaf-cutter ants undergo a distinct physiological transition during biomass degradation". United States. doi:10.1111/1758-2229.12163.
@article{osti_1170464,
title = {The fungus gardens of leaf-cutter ants undergo a distinct physiological transition during biomass degradation},
author = {Huang, Eric L. and Aylward, Frank O. and Kim, Young-Mo and Webb-Robertson, Bobbie-Jo M. and Nicora, Carrie D. and Hu, Zeping and Metz, Thomas O. and Lipton, Mary S. and Smith, Richard D. and Currie, Cameron R. and Burnum-Johnson, Kristin E.},
abstractNote = {Leaf-cutter ants are dominant herbivores in ecosystems throughout the Neotropics. Rather than directly consuming the fresh foliar biomass they harvest, these ants use it to cultivate specialized fungus gardens. 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 metametabolomics and metaproteomics techniques, we examine the dynamics of nutrient turnover and biosynthesis 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 findings of cellulases and laccases produced by Leucoagaricus gongylophorus, the fungus cultivated by leaf-cutter 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 metametabolomics experiments despite evidence that the host ants cannot produce this amino acid, suggesting that biosynthesis of this metabolite may be tightly regulated in the fungus garden. These results provide new insights into the dynamics of nutrient cycling that underlie this important ant-fungus symbiosis.},
doi = {10.1111/1758-2229.12163},
journal = {Environmental Microbiology Reports, 6(4):389-95},
number = ,
volume = ,
place = {United States},
year = {Fri Aug 01 00:00:00 EDT 2014},
month = {Fri Aug 01 00:00:00 EDT 2014}
}