From Plants to Ants: Fungal Modification of Leaf Lipids for Nutrition and Communication in the Leaf-Cutter Ant Fungal Garden Ecosystem

Khadempour, Lily; Kyle, Jennifer E.; Webb-Robertson, Bobbie-Jo M.; Nicora, Carrie D.; Smith, Francesca B.; Smith, Richard D.; Lipton, Mary S.; Currie, Cameron R.; Baker, Erin S.; Burnum-Johnson, Kristin E.; Shank, ed., Elizabeth Anne

doi:10.1128/msystems.01307-20

Title: From Plants to Ants: Fungal Modification of Leaf Lipids for Nutrition and Communication in the Leaf-Cutter Ant Fungal Garden Ecosystem

Journal Article · Tue Apr 27 04:00:00 UTC 2021 · mSystems

DOI: https://doi.org/10.1128/msystems.01307-20 · OSTI ID:1772265

^[1]; Kyle, Jennifer E. ^[2]; Webb-Robertson, Bobbie-Jo M. ^[2]; Nicora, Carrie D. ^[2]; Smith, Francesca B. ^[2]; Smith, Richard D. ^[2]; Lipton, Mary S. ^[3]; Currie, Cameron R. ^[1]; Baker, Erin S. ^[4];

^[3]; Shank, ed., Elizabeth Anne

Department of Bacteriology, University of Wisconsin—Madison, Madison, Wisconsin, USA
Biological Sciences Division, Pacific Northwest National Laboratory, Richland, Washington, USA
The Environmental Molecular Sciences Laboratory, Pacific Northwest National Laboratory, Richland, Washington, USA
Department of Chemistry, North Carolina State University, Raleigh, North Carolina, USA

In this work, we examined the role of lipids in the mutualism between leaf-cutter ants and fungus. These ants cut fresh leaf material, which they provide to their fungal cultivar, that converts energy and nutrients from the plants and provides it to the ants in specialized hyphal swellings called gongylidia.

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Sponsoring Organization:: USDOE

OSTI ID:: 1772265

Journal Information:: mSystems, Journal Name: mSystems Journal Issue: 2 Vol. 6; ISSN 2379-5077

Publisher:: American Society for MicrobiologyCopyright Statement

Country of Publication:: United States

Language:: English

References (43)

Disentangling nutritional pathways linking leafcutter ants and their co-evolved fungal symbionts using stable isotopes Shik, Jonathan Z.; Rytter, Winnie; Arnan, Xavier Ecology, Vol. 99, Issue 9 https://doi.org/10.1002/ecy.2431	journal	August 2018
Dependence of necrophoric response to oleic acid on social context in the ant,Pogonomyrmex badius Gordon, Deborah M. Journal of Chemical Ecology, Vol. 9, Issue 1 https://doi.org/10.1007/BF00987774	journal	January 1983
The role of chemical signalling in maintenance of the fungus garden by leaf-cutting ants Green, P. W. C.; Kooij, P. W. Chemoecology, Vol. 28, Issue 3 https://doi.org/10.1007/s00049-018-0260-x	journal	May 2018
Fungal allelochemicals in insect pest management Holighaus, Gerrit; Rohlfs, Marko Applied Microbiology and Biotechnology, Vol. 100, Issue 13 https://doi.org/10.1007/s00253-016-7573-x	journal	May 2016
Role of membrane glycerolipids in photosynthesis, thylakoid biogenesis and chloroplast development Kobayashi, Koichi Journal of Plant Research, Vol. 129, Issue 4 https://doi.org/10.1007/s10265-016-0827-y	journal	April 2016
Fungal Volatiles as Olfactory Cues for Female Fungus Gnat, Lycoriella ingenua in the Avoidance of Mycelia Colonized Compost Kecskeméti, Sándor; Szelényi, Magdolna Olívia; Erdei, Anna Laura Journal of Chemical Ecology, Vol. 46, Issue 10 https://doi.org/10.1007/s10886-020-01210-5	journal	October 2020
A Simple Method for the Isolation and Purification of Total Lipides from Animal Tissues Folch, Jordi; Lees, M.; Stanley, G. H. Sloane Journal of Biological Chemistry, Vol. 226, Issue 1 https://doi.org/10.1016/S0021-9258(18)64849-5	journal	May 1957
Desert Ants Locate Food by Combining High Sensitivity to Food Odors with Extensive Crosswind Runs Buehlmann, Cornelia; Graham, Paul; Hansson, Bill S. Current Biology, Vol. 24, Issue 9 https://doi.org/10.1016/j.cub.2014.02.056	journal	May 2014
Nestmate recognition signals of the leaf-cutting ant Atta laevigata Hernández, J. V.; López, H.; Jaffe, K. Journal of Insect Physiology, Vol. 48, Issue 3 https://doi.org/10.1016/s0022-1910(01)00173-1	journal	March 2002
Lipid chemotaxis and signal transduction in Myxococcus xanthus Kearns, Daniel B.; Shimkets, Lawrence J. Trends in Microbiology, Vol. 9, Issue 3 https://doi.org/10.1016/s0966-842x(01)01948-5	journal	March 2001
Combined Statistical Analyses of Peptide Intensities and Peptide Occurrences Improves Identification of Significant Peptides from MS-Based Proteomics Data Webb-Robertson, Bobbie-Jo M.; McCue, Lee Ann; Waters, Katrina M. Journal of Proteome Research, Vol. 9, Issue 11 https://doi.org/10.1021/pr1005247	journal	November 2010
Metagenomic and metaproteomic insights into bacterial communities in leaf-cutter ant fungus gardens Aylward, Frank O.; Burnum, Kristin E.; Scott, Jarrod J. The ISME Journal, Vol. 6, Issue 9 https://doi.org/10.1038/ismej.2012.10	journal	March 2012
Reciprocal genomic evolution in the ant–fungus agricultural symbiosis Nygaard, Sanne; Hu, Haofu; Li, Cai Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms12233	journal	July 2016
Symbiotic adaptations in the fungal cultivar of leaf-cutting ants De Fine Licht, Henrik H.; Boomsma, Jacobus J.; Tunlid, Anders Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms6675	journal	December 2014
Host interactions of probiotic bacterial surface molecules: comparison with commensals and pathogens Lebeer, Sarah; Vanderleyden, Jos; De Keersmaecker, Sigrid C. J. Nature Reviews Microbiology, Vol. 8, Issue 3 https://doi.org/10.1038/nrmicro2297	journal	March 2010
Uncovering biologically significant lipid isomers with liquid chromatography, ion mobility spectrometry and mass spectrometry Kyle, Jennifer E.; Zhang, Xing; Weitz, Karl K. The Analyst, Vol. 141, Issue 5 https://doi.org/10.1039/c5an02062j	journal	January 2016
Communication between the fungus garden and workers of the leaf‐cutting ant, Atta sexdens rubropilosa , regarding choice of substrate for the fungus North, R. D.; Jackson, C. W.; Howse, P. E. Physiological Entomology, Vol. 24, Issue 2 https://doi.org/10.1046/j.1365-3032.1999.00122.x	journal	June 1999
Major evolutionary transitions in ant agriculture Schultz, T. R.; Brady, S. G. Proceedings of the National Academy of Sciences, Vol. 105, Issue 14 https://doi.org/10.1073/pnas.0711024105	journal	March 2008
Laccase detoxification mediates the nutritional alliance between leaf-cutting ants and fungus-garden symbionts De Fine Licht, H. H.; Schiott, M.; Rogowska-Wrzesinska, A. Proceedings of the National Academy of Sciences, Vol. 110, Issue 2 https://doi.org/10.1073/pnas.1212709110	journal	December 2012
Predator lipids induce paralytic shellfish toxins in bloom-forming algae Selander, Erik; Kubanek, Julia; Hamberg, Mats Proceedings of the National Academy of Sciences, Vol. 112, Issue 20 https://doi.org/10.1073/pnas.1420154112	journal	April 2015
Improved quality control processing of peptide-centric LC-MS proteomics data Matzke, Melissa M.; Waters, Katrina M.; Metz, Thomas O. Bioinformatics, Vol. 27, Issue 20 https://doi.org/10.1093/bioinformatics/btr479	journal	August 2011
LC-IMS-MS Feature Finder: detecting multidimensional liquid chromatography, ion mobility and mass spectrometry features in complex datasets Crowell, Kevin L.; Slysz, Gordon W.; Baker, Erin S. Bioinformatics, Vol. 29, Issue 21 https://doi.org/10.1093/bioinformatics/btt465	journal	September 2013
LIQUID: an-open source software for identifying lipids in LC-MS/MS-based lipidomics data Kyle, Jennifer E.; Crowell, Kevin L.; Casey, Cameron P. Bioinformatics, Vol. 33, Issue 11 https://doi.org/10.1093/bioinformatics/btx046	journal	January 2017
Anthonomus grandis aggregation pheromone induces cotton indirect defence and attracts the parasitic wasp Bracon vulgaris Magalhães, Diego Martins; Da Silva, Izabela Thaís Fidelis Alves; Borges, Miguel Journal of Experimental Botany, Vol. 70, Issue 6 https://doi.org/10.1093/jxb/erz040	journal	February 2019
Lipid regulation of cell membrane structure and function Yèagle, Philip L. The FASEB Journal, Vol. 3, Issue 7 https://doi.org/10.1096/fasebj.3.7.2469614	journal	May 1989
Ultrastructural and microbial analyses of cellulose degradation in leaf-cutter ant colonies Moreira-Soto, Rolando Daniel; Sanchez, Ethel; Currie, Cameron R. Microbiology, Vol. 163, Issue 11 https://doi.org/10.1099/mic.0.000546	journal	November 2017
Intracellular Levels of Free Linolenic and Linoleic Acids Increase in Tomato Leaves in Response to Wounding Conconi, A.; Miquel, M.; Browse, J. A. Plant Physiology, Vol. 111, Issue 3 https://doi.org/10.1104/pp.111.3.797	journal	July 1996
BORIS : a free, versatile open‐source event‐logging software for video/audio coding and live observations Friard, Olivier; Gamba, Marco Methods in Ecology and Evolution, Vol. 7, Issue 11 https://doi.org/10.1111/2041-210X.12584	journal	May 2016
Ecosystem engineering by leaf-cutting ants: nests of Atta cephalotes drastically alter forest structure and microclimate Meyer, Sebastian T.; Leal, Inara R.; Tabarelli, Marcelo Ecological Entomology, Vol. 36, Issue 1 https://doi.org/10.1111/j.1365-2311.2010.01241.x	journal	November 2010
Fungal hyphae as a source of nutrients for the leaf-cutting ant Atta sexdens Bass, M.; Cherrett, J. M. Physiological Entomology, Vol. 20, Issue 1 https://doi.org/10.1111/j.1365-3032.1995.tb00793.x	journal	March 1995
Antennal olfactory sensitivity in response to task-related odours of three castes of the ant Atta mexicana (hymenoptera: formicidae) LÓPez-Riquelme, GermÁN Octavio; Malo, Edi A.; Cruz-LÓPez, Leopoldo Physiological Entomology, Vol. 31, Issue 4 https://doi.org/10.1111/j.1365-3032.2006.00526.x	journal	November 2006
The Importance of Where to Dump the Refuse: Seed Banks and Fine Roots in Nests of the Leaf-Cutting Ants Atta cephalotes and A. colombica1 Farji-Brener, Alejandro G.; Medina, Claudia A. Biotropica, Vol. 32, Issue 1 https://doi.org/10.1111/j.1744-7429.2000.tb00454.x	journal	March 2000
The fungal cultivar of leaf-cutter ants produces specific enzymes in response to different plant substrates Khadempour, Lily; Burnum-Johnson, Kristin E.; Baker, Erin S. Molecular Ecology, Vol. 25, Issue 22 https://doi.org/10.1111/mec.13872	journal	October 2016
Leucoagaricus gongylophorus Produces Diverse Enzymes for the Degradation of Recalcitrant Plant Polymers in Leaf-Cutter Ant Fungus Gardens Aylward, Frank O.; Burnum-Johnson, Kristin E.; Tringe, Susannah G. Applied and Environmental Microbiology, Vol. 79, Issue 12 https://doi.org/10.1128/AEM.03833-12	journal	April 2013
Virus Impact on Lipids and Membranes Ketter, Ellen; Randall, Glenn Annual Review of Virology, Vol. 6, Issue 1 https://doi.org/10.1146/annurev-virology-092818-015748	journal	September 2019
QUORUM SENSING: Cell-to-Cell Communication in Bacteria Waters, Christopher M.; Bassler, Bonnie L. Annual Review of Cell and Developmental Biology, Vol. 21, Issue 1 https://doi.org/10.1146/annurev.cellbio.21.012704.131001	journal	November 2005
Chemical Releaser of Necrophoric Behavior in Ants Wilson, E. O.; Durlach, N. I.; Roth, L. M. Psyche: A Journal of Entomology, Vol. 65, Issue 4 https://doi.org/10.1155/1958/69391	journal	January 1958
MZmine 2: Modular framework for processing, visualizing, and analyzing mass spectrometry-based molecular profile data Pluskal, Tomáš; Castillo, Sandra; Villar-Briones, Alejandro BMC Bioinformatics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2105-11-395	journal	July 2010
Update on LIPID MAPS classification, nomenclature, and shorthand notation for MS-derived lipid structures Liebisch, Gerhard; Fahy, Eoin; Aoki, Junken Journal of Lipid Research, Vol. 61, Issue 12 https://doi.org/10.1194/jlr.S120001025	journal	December 2020
The Genome Sequence of the Leaf-Cutter Ant Atta cephalotes Reveals Insights into Its Obligate Symbiotic Lifestyle Suen, Garret; Teiling, Clotilde; Li, Lewyn PLoS Genetics, Vol. 7, Issue 2 https://doi.org/10.1371/journal.pgen.1002007	journal	February 2011
Enrichment and Broad Representation of Plant Biomass-Degrading Enzymes in the Specialized Hyphal Swellings of Leucoagaricus gongylophorus, the Fungal Symbiont of Leaf-Cutter Ants Aylward, Frank O.; Khadempour, Lily; Tremmel, Daniel M. PLOS ONE, Vol. 10, Issue 8 https://doi.org/10.1371/journal.pone.0134752	journal	August 2015
A Volatile Semiochemical Released by the Fungus Garden of Leaf-Cutting Ants Sousa, K. K. A.; Catalani, G. C.; Gianeti, T. M. R. Florida Entomologist, Vol. 103, Issue 1 https://doi.org/10.1653/024.103.0401	journal	March 2020
Do herbivores exert top‐down effects in Neotropical savannas? Estimates of biomass consumption by leaf‐cutter ants Costa, Alan N.; Vasconcelos, Heraldo L.; Vieira‐Neto, Ernane H. M. Journal of Vegetation Science, Vol. 19, Issue 6 https://doi.org/10.3170/2008-8-18461	journal	January 2008

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