Symbiont-Mediated Protection of Acromyrmex Leaf-Cutter Ants from the Entomopathogenic Fungus Metarhizium anisopliae

Bruner-Montero, Gaspar; Wood, Matthew; Horn, Heidi A.; Gemperline, Erin; Li, Lingjun; Currie, Cameron R.

doi:10.1128/mbio.01885-21

Title: Symbiont-Mediated Protection of Acromyrmex Leaf-Cutter Ants from the Entomopathogenic Fungus Metarhizium anisopliae

Journal Article · 20 December 2021 · mBio (Online)

DOI: https://doi.org/10.1128/mbio.01885-21 · OSTI ID:1903820

Bruner-Montero, Gaspar ^[1]; Wood, Matthew ^[2]; Horn, Heidi A. ^[2]; Gemperline, Erin ^[2]; Li, Lingjun ^[2];

^[2]

University of Wisconsin, Madison, WI (United States); University of Cambridge (United Kingdom); OSTI
University of Wisconsin, Madison, WI (United States)

Many fungus-growing ants engage in a defensive symbiosis with antibiotic-producing ectosymbiotic bacteria in the genus Pseudonocardia, which help protect the ants’ fungal mutualist from a specialized mycoparasite, Escovopsis. Here, using germfree ant rearing and experimental pathogen infection treatments, we evaluate if Acromyrmex ants derive higher immunity to the entomopathogenic fungus Metarhizium anisopliae from their Pseudonocardia symbionts. We further examine the ecological dynamics and defensive capacities of Pseudonocardia against M. anisopliae across seven different Acromyrmex species by controlling Pseudonocardia acquisition using ant-nonnative Pseudonocardia switches, in vitro challenges, and in situ mass spectrometry imaging (MSI). We show that Pseudonocardia protects the ants against M. anisopliae across different Acromyrmex species and appears to afford higher protection than metapleural gland (MG) secretions. Although Acromyrmex echinatior ants with nonnative Pseudonocardia symbionts receive protection from M. anisopliae regardless of the strain acquired compared with Pseudonocardia-free conditions, we find significant variation in the degree of protection conferred by different Pseudonocardia strains. Additionally, when ants were reared in Pseudonocardia-free conditions, some species exhibit more susceptibility to M. anisopliae than others, indicating that some ant species depend more on defensive symbionts than others. In vitro challenge experiments indicate that Pseudonocardia reduces Metarhizium conidiospore germination area. Our chemometric analysis using matrix-assisted laser desorption/ionization mass spectrometry imaging (MALDI-MSI) reveals that Pseudonocardia-carrying ants produce more chemical signals than Pseudonocardia-free treatments, indicating that Pseudonocardia produces bioactive metabolites on the Acromyrmex cuticle. Our results indicate that Pseudonocardia can serve as a dual-purpose defensive symbiont, conferring increased immunity for both the obligate fungal mutualist and the ants themselves.

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Research Organization:: Great Lakes Bioenergy Research Center (GLBRC), Madison, WI (United States); University of Wisconsin, Madison, WI (United States)

Sponsoring Organization:: National Institutes of Health (NIH); National Science Foundation (NSF); USDOE

OSTI ID:: 1903820

Journal Information:: mBio (Online), Journal Name: mBio (Online) Journal Issue: 6 Vol. 12; ISSN 2150-7511

Publisher:: American Society for Microbiology (ASM)Copyright Statement

Country of Publication:: United States

Language:: English

References (82)

Variable sensitivity of fungi and bacteria to compounds produced by the metapleural glands of leaf-cutting ants Bot, A. N. M.; Ortius-Lechner, D.; Finster, K. Insectes Sociaux, Vol. 49, Issue 4 https://doi.org/10.1007/PL00012660	journal	November 2002
Prudent inquilines and proactive hosts: behavioral dynamics between an ant social parasite, Megalomyrmex symmetochus and its fungus-growing ant host, Sericomyrmex amabilis Bruner, G.; Wcislo, W. T.; Fernández-Marín, H. Insectes Sociaux, Vol. 61, Issue 1 https://doi.org/10.1007/s00040-013-0331-5	journal	December 2013
Variation in subterranean termite susceptibility to fatal infections by local Metarhizium soil isolates Denier, D.; Bulmer, M. S. Insectes Sociaux, Vol. 62, Issue 2 https://doi.org/10.1007/s00040-015-0394-6	journal	March 2015
The effect of metapleural gland secretion on the growth of a mutualistic bacterium on the cuticle of leaf-cutting ants Poulsen, Michael; Bot, Adrianne N. M.; Boomsma, Jacobus J. Naturwissenschaften, Vol. 90, Issue 9 https://doi.org/10.1007/s00114-003-0450-3	journal	September 2003
Experimental evidence for the costs and hygienic significance of the antibiotic metapleural gland secretion in leaf-cutting ants Poulsen, Michael; Bot, Adrianne; Nielsen, Mogens Behavioral Ecology and Sociobiology, Vol. 52, Issue 2 https://doi.org/10.1007/s00265-002-0489-8	journal	July 2002
Sanitizing the fortress: protection of ant brood and nest material by worker antibiotics Tranter, C.; Graystock, P.; Shaw, C. Behavioral Ecology and Sociobiology, Vol. 68, Issue 3 https://doi.org/10.1007/s00265-013-1664-9	journal	December 2013
Social Prophylaxis: Group Interaction Promotes Collective Immunity in Ant Colonies Ugelvig, Line V.; Cremer, Sylvia Current Biology, Vol. 17, Issue 22 https://doi.org/10.1016/j.cub.2007.10.029	journal	November 2007
Actinobacteria as mutualists: general healthcare for insects? Kaltenpoth, Martin Trends in Microbiology, Vol. 17, Issue 12 https://doi.org/10.1016/j.tim.2009.09.006	journal	December 2009
A taxonomic revision of Metarhizium based on a phylogenetic analysis of rDNA sequence data Driver, Felice; Milner, Richard J.; Trueman, John W. H. Mycological Research, Vol. 104, Issue 2 https://doi.org/10.1017/S0953756299001756	journal	February 2000
Imaging with Mass Spectrometry of Bacteria on the Exoskeleton of Fungus-Growing Ants Gemperline, Erin; Horn, Heidi A.; DeLaney, Kellen ACS Chemical Biology, Vol. 12, Issue 8 https://doi.org/10.1021/acschembio.7b00038	journal	June 2017
Experimental evidence of a tripartite mutualism: bacteria protect ant fungus gardens from specialized parasites Currie, C. R.; Bot, A. N. M.; Boomsma, J. J. Oikos, Vol. 101, Issue 1 https://doi.org/10.1034/j.1600-0706.2003.12036.x	journal	April 2003
Fungus-growing ants use antibiotic-producing bacteria to control garden parasites Currie, Cameron R.; Scott, James A.; Summerbell, Richard C. Nature, Vol. 398, Issue 6729 https://doi.org/10.1038/19519	journal	April 1999
Feast or famine: the global regulator DasR links nutrient stress to antibiotic production by Streptomyces Rigali, Sébastien; Titgemeyer, Fritz; Barends, Sharief EMBO reports, Vol. 9, Issue 7 https://doi.org/10.1038/embor.2008.83	journal	May 2008
Dentigerumycin: a bacterial mediator of an ant-fungus symbiosis Oh, Dong-Chan; Poulsen, Michael; Currie, Cameron R. Nature Chemical Biology, Vol. 5, Issue 6 https://doi.org/10.1038/nchembio.159	journal	March 2009
Antibiotic-producing symbionts dynamically transition between plant pathogenicity and insect-defensive mutualism Flórez, Laura V.; Scherlach, Kirstin; Gaube, Paul Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/ncomms15172	journal	April 2017
Defensive symbioses of animals with prokaryotic and eukaryotic microorganisms Flórez, Laura V.; Biedermann, Peter H. W.; Engl, Tobias Natural Product Reports, Vol. 32, Issue 7 https://doi.org/10.1039/c5np00010f	journal	January 2015
Within-colony transmission and the cost of a mutualistic bacterium in the leaf-cutting ant Acromyrmex octospinosus Poulsen, M.; Bot, A. N. M.; Currie, C. R. Functional Ecology, Vol. 17, Issue 2 https://doi.org/10.1046/j.1365-2435.2003.00726.x	journal	April 2003
Facultative bacterial symbionts in aphids confer resistance to parasitic wasps Oliver, K. M.; Russell, J. A.; Moran, N. A. Proceedings of the National Academy of Sciences, Vol. 100, Issue 4 https://doi.org/10.1073/pnas.0335320100	journal	January 2003
Variation in resistance to parasitism in aphids is due to symbionts not host genotype Oliver, K. M.; Moran, N. A.; Hunter, M. S. Proceedings of the National Academy of Sciences, Vol. 102, Issue 36 https://doi.org/10.1073/pnas.0506131102	journal	August 2005
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
Candicidin-producing Streptomyces support leaf-cutting ants to protect their fungus garden against the pathogenic fungus Escovopsis Haeder, S.; Wirth, R.; Herz, H. Proceedings of the National Academy of Sciences, Vol. 106, Issue 12 https://doi.org/10.1073/pnas.0812082106	journal	March 2009
Socially transmitted gut microbiota protect bumble bees against an intestinal parasite Koch, H.; Schmid-Hempel, P. Proceedings of the National Academy of Sciences, Vol. 108, Issue 48 https://doi.org/10.1073/pnas.1110474108	journal	November 2011
Microbes are trophic analogs of animals Steffan, Shawn A.; Chikaraishi, Yoshito; Currie, Cameron R. Proceedings of the National Academy of Sciences, Vol. 112, Issue 49 https://doi.org/10.1073/pnas.1508782112	journal	November 2015
Convergent evolution of complex structures for ant–bacterial defensive symbiosis in fungus-farming ants Li, Hongjie; Sosa-Calvo, Jeffrey; Horn, Heidi A. Proceedings of the National Academy of Sciences, Vol. 115, Issue 42 https://doi.org/10.1073/pnas.1809332115	journal	October 2018
The agricultural pathology of ant fungus gardens Currie, C. R.; Mueller, U. G.; Malloch, D. Proceedings of the National Academy of Sciences, Vol. 96, Issue 14 https://doi.org/10.1073/pnas.96.14.7998	journal	July 1999
Recruitment of minor workers for defense against a specialized parasite ofAttaleaf-cutting ant fungus gardens Gerstner, A. T.; Poulsen, M.; Currie, C. R. Ethology Ecology & Evolution, Vol. 23, Issue 1 https://doi.org/10.1080/03949370.2010.529828	journal	January 2011
Modeling the Ecology of Symbiont-Mediated Protection against Parasites Kwiatkowski, Marek; Vorburger, Christoph The American Naturalist, Vol. 179, Issue 5 https://doi.org/10.1086/665003	journal	May 2012
The Population Structure of Antibiotic-Producing Bacterial Symbionts of Apterostigma dentigerum Ants: Impacts of Coevolution and Multipartite Symbiosis Caldera, Eric J.; Currie, Cameron R. The American Naturalist, Vol. 180, Issue 5 https://doi.org/10.1086/667886	journal	November 2012
Dynamic Disease Management inTrachymyrmexFungus-Growing Ants (Attini: Formicidae) Fernández-Marín, Hermógenes; Bruner, Gaspar; Gomez, Ernesto B. The American Naturalist, Vol. 181, Issue 4 https://doi.org/10.1086/669664	journal	April 2013
Rapid spread of the defensive endosymbiont Spiroplasma in Drosophila hydei under high parasitoid wasp pressure Xie, Jialei; Winter, Caitlyn; Winter, Lauryn FEMS Microbiology Ecology, Vol. 91, Issue 2 https://doi.org/10.1093/femsec/fiu017	journal	December 2014
Chemical ecology of antibiotic production by actinomycetes van der Meij, Anne; Worsley, Sarah F.; Hutchings, Matthew I. FEMS Microbiology Reviews, Vol. 41, Issue 3 https://doi.org/10.1093/femsre/fux005	journal	May 2017
MetaboAnalyst 3.0—making metabolomics more meaningful Xia, Jianguo; Sinelnikov, Igor V.; Han, Beomsoo Nucleic Acids Research, Vol. 43, Issue W1 https://doi.org/10.1093/nar/gkv380	journal	April 2015
Symbiotic bacteria on the cuticle of the leaf-cutting ant Acromyrmex subterraneus subterraneus protect workers from attack by entomopathogenic fungi Mattoso, Thalles C.; Moreira, Denise D. O.; Samuels, Richard I. Biology Letters, Vol. 8, Issue 3 https://doi.org/10.1098/rsbl.2011.0963	journal	November 2011
Weeding and grooming of pathogens in agriculture by ants Currie, Cameron R.; Stuart, Alison E. Proceedings of the Royal Society of London. Series B: Biological Sciences, Vol. 268, Issue 1471 https://doi.org/10.1098/rspb.2001.1605	journal	May 2001
Active use of the metapleural glands by ants in controlling fungal infection Fernández-Marín, Hermógenes; Zimmerman, Jess K.; Rehner, Stephen A. Proceedings of the Royal Society B: Biological Sciences, Vol. 273, Issue 1594 https://doi.org/10.1098/rspb.2006.3492	journal	March 2006
Symbiont-mediated protection Haine, Eleanor R. Proceedings of the Royal Society B: Biological Sciences, Vol. 275, Issue 1633 https://doi.org/10.1098/rspb.2007.1211	journal	December 2007
Reduced biological control and enhanced chemical pest management in the evolution of fungus farming in ants Fernández-Marín, Hermógenes; Zimmerman, Jess K.; Nash, David R. Proceedings of the Royal Society B: Biological Sciences, Vol. 276, Issue 1665 https://doi.org/10.1098/rspb.2009.0184	journal	March 2009
Specificity in the symbiotic association between fungus-growing ants and protective Pseudonocardia bacteria Cafaro, Matías J.; Poulsen, Michael; Little, Ainslie E. F. Proceedings of the Royal Society B: Biological Sciences, Vol. 278, Issue 1713 https://doi.org/10.1098/rspb.2010.2118	journal	November 2010
Regulation and specificity of antifungal metapleural gland secretion in leaf-cutting ants Yek, Sze Huei; Nash, David R.; Jensen, Annette B. Proceedings of the Royal Society B: Biological Sciences, Vol. 279, Issue 1745 https://doi.org/10.1098/rspb.2012.1458	journal	August 2012
Extended disease resistance emerging from the faecal nest of a subterranean termite Chouvenc, Thomas; Efstathion, Caroline A.; Elliott, Monica L. Proceedings of the Royal Society B: Biological Sciences, Vol. 280, Issue 1770 https://doi.org/10.1098/rspb.2013.1885	journal	November 2013
A carbohydrate-rich diet increases social immunity in ants Kay, Adam D.; Bruning, Abbie J.; van Alst, Andy Proceedings of the Royal Society B: Biological Sciences, Vol. 281, Issue 1778 https://doi.org/10.1098/rspb.2013.2374	journal	March 2014
Virus evolution in Wolbachia- infected Drosophila Martinez, Julien; Bruner-Montero, Gaspar; Arunkumar, Ramesh Proceedings of the Royal Society B: Biological Sciences, Vol. 286, Issue 1914 https://doi.org/10.1098/rspb.2019.2117	journal	October 2019
Defensive microbial symbionts in Hymenoptera Kaltenpoth, Martin; Engl, Tobias Functional Ecology, Vol. 28, Issue 2 https://doi.org/10.1111/1365-2435.12089	journal	April 2013
BroadEscovopsis-inhibition activity ofPseudonocardiaassociated withTrachymyrmexants Meirelles, Lucas A.; Mendes, Thaís D.; Solomon, Scott E. Environmental Microbiology Reports, Vol. 6, Issue 4 https://doi.org/10.1111/1758-2229.12132	journal	January 2014
INFECTIOUS ADAPTATION: POTENTIAL HOST RANGE OF A DEFENSIVE ENDOSYMBIONT INDROSOPHILA Haselkorn, Tamara S.; Cockburn, Sarah N.; Hamilton, Phineas T. Evolution, Vol. 67, Issue 4 https://doi.org/10.1111/evo.12020	journal	December 2012
Specificity of the mutualistic association between actinomycete bacteria and two sympatric species of Acromyrmex leaf-cutting ants Poulsen, M.; Cafaro, M.; Boomsma, J. J. Molecular Ecology, Vol. 14, Issue 11 https://doi.org/10.1111/j.1365-294X.2005.02695.x	journal	October 2005
Evolutionary genetics of a defensive facultative symbiont of insects: exchange of toxin-encoding bacteriophage: MULTILOCUS ANALYSIS OF PROTECTIVE INSECT SYMBIONT AND ITS PHAGE Degnan, Patrick H.; Moran, Nancy A. Molecular Ecology, Vol. 17, Issue 3 https://doi.org/10.1111/j.1365-294X.2007.03616.x	journal	December 2007
Defensive endosymbionts: a cryptic trophic level in community ecology Jaenike, John; Brekke, Thomas D. Ecology Letters, Vol. 14, Issue 2 https://doi.org/10.1111/j.1461-0248.2010.01564.x	journal	December 2010
The metapleural gland of ants Yek, Sze Huei; Mueller, Ulrich G. Biological Reviews, Vol. 86, Issue 4 https://doi.org/10.1111/j.1469-185X.2010.00170.x	journal	December 2010
Genotypic Variation and the role of Defensive Endosymbionts in an All-Parthenogenetic Host-Parasitoid Interaction Vorburger, Christoph; Sandrock, Christoph; Gouskov, Alexandre Evolution, Vol. 63, Issue 6 https://doi.org/10.1111/j.1558-5646.2009.00660.x	journal	June 2009
Immune Defense in Leaf-Cutting Ants: a Cross-Fostering Approach Armitage, Sophie A. O.; Broch, Jens F.; Marín, Hermogenes Fernández Evolution, Vol. 65, Issue 6 https://doi.org/10.1111/j.1558-5646.2011.01241.x	journal	February 2011
Common trends in mutualism revealed by model associations between invertebrates and bacteria: Table 1 Chaston, John; Goodrich-Blair, Heidi FEMS Microbiology Reviews, Vol. 34, Issue 1 https://doi.org/10.1111/j.1574-6976.2009.00193.x	journal	January 2010
Variation in Pseudonocardia antibiotic defence helps govern parasite-induced morbidity in Acromyrmex leaf-cutting ants: Parasite-defence interactions in leaf-cutting ants Poulsen, Michael; Cafaro, Matías J.; Erhardt, Daniel P. Environmental Microbiology Reports, Vol. 2, Issue 4 https://doi.org/10.1111/j.1758-2229.2009.00098.x	journal	November 2009
Specificity and stability of the Acromyrmex -Pseudonocardia symbiosis Andersen, S. B.; Hansen, L. H.; Sapountzis, P. Molecular Ecology, Vol. 22, Issue 16 https://doi.org/10.1111/mec.12380	journal	July 2013
Immune system stimulation by the gut symbiont Frischella perrara in the honey bee ( Apis mellifera ) Emery, Olivier; Schmidt, Konstantin; Engel, Philipp Molecular Ecology, Vol. 26, Issue 9 https://doi.org/10.1111/mec.14058	journal	March 2017
Intertwining nutrient-sensory networks and the control of antibiotic production in Streptomyces: Intertwining nutrient-sensory networks Urem, Mia; Świątek-Połatyńska, Magdalena A.; Rigali, Sébastien Molecular Microbiology, Vol. 102, Issue 2 https://doi.org/10.1111/mmi.13464	journal	August 2016
Coevolved Crypts and Exocrine Glands Support Mutualistic Bacteria in Fungus-Growing Ants Currie, C. R. Science, Vol. 311, Issue 5757 https://doi.org/10.1126/science.1119744	journal	January 2006
Aphid Protected from Pathogen by Endosymbiont Scarborough, C. L. Science, Vol. 310, Issue 5755 https://doi.org/10.1126/science.1120180	journal	December 2005
Bacterial Protection of Beetle-Fungus Mutualism Scott, J. J.; Oh, D. -C.; Yuceer, M. C. Science, Vol. 322, Issue 5898 https://doi.org/10.1126/science.1160423	journal	October 2008
Wolbachia and Virus Protection in Insects Hedges, L. M.; Brownlie, J. C.; O'Neill, S. L. Science, Vol. 322, Issue 5902 https://doi.org/10.1126/science.1162418	journal	October 2008
Bacteriophages Encode Factors Required for Protection in a Symbiotic Mutualism Oliver, Kerry M.; Degnan, Patrick H.; Hunter, Martha S. Science, Vol. 325, Issue 5943 https://doi.org/10.1126/science.1174463	journal	August 2009
Phylogenetic analysis of mutualistic filamentous bacteria associated with fungus-growing ants Cafaro, Matías J.; Currie, Cameron R. Canadian Journal of Microbiology, Vol. 51, Issue 6 https://doi.org/10.1139/w05-023	journal	June 2005
A Community of Ants, Fungi, and Bacteria: A Multilateral Approach to Studying Symbiosis Currie, Cameron R. Annual Review of Microbiology, Vol. 55, Issue 1 https://doi.org/10.1146/annurev.micro.55.1.357	journal	October 2001
Towards a Better Understanding of the Evolution of Specialized Parasites of Fungus-Growing Ant Crops Yek, Sze Huei; Boomsma, Jacobus J.; Poulsen, Michael Psyche: A Journal of Entomology, Vol. 2012 https://doi.org/10.1155/2012/239392	journal	January 2012
Filtering for increased power for microarray data analysis Hackstadt, Amber J.; Hess, Ann M. BMC Bioinformatics, Vol. 10, Issue 1 https://doi.org/10.1186/1471-2105-10-11	journal	January 2009
A mixed community of actinomycetes produce multiple antibiotics for the fungus farming ant Acromyrmex octospinosus Barke, Jörg; Seipke, Ryan F.; Grüschow, Sabine BMC Biology, Vol. 8, Issue 1 https://doi.org/10.1186/1741-7007-8-109	journal	January 2010
Interaction specificity between leaf-cutting ants and vertically transmitted Pseudonocardia bacteria Andersen, Sandra B.; Yek, Sze Huei; Nash, David R. BMC Evolutionary Biology, Vol. 15, Issue 1 https://doi.org/10.1186/s12862-015-0308-2	journal	February 2015
Social Transfer of Pathogenic Fungus Promotes Active Immunisation in Ant Colonies Konrad, Matthias; Vyleta, Meghan L.; Theis, Fabian J. PLoS Biology, Vol. 10, Issue 4 https://doi.org/10.1371/journal.pbio.1001300	journal	April 2012
Antagonistic Bacterial Interactions Help Shape Host-Symbiont Dynamics within the Fungus-Growing Ant-Microbe Mutualism Poulsen, Michael; Erhardt, Daniel P.; Molinaro, Daniel J. PLoS ONE, Vol. 2, Issue 9 https://doi.org/10.1371/journal.pone.0000960	journal	September 2007
Chemical Analyses of Wasp-Associated Streptomyces Bacteria Reveal a Prolific Potential for Natural Products Discovery Poulsen, Michael; Oh, Dong-Chan; Clardy, Jon PLoS ONE, Vol. 6, Issue 2 https://doi.org/10.1371/journal.pone.0016763	journal	February 2011
Interaction between Workers during a Short Time Window Is Required for Bacterial Symbiont Transmission in Acromyrmex Leaf-Cutting Ants Marsh, Sarah E.; Poulsen, Michael; Pinto-Tomás, Adrián PLoS ONE, Vol. 9, Issue 7 https://doi.org/10.1371/journal.pone.0103269	journal	July 2014
Variation in Antiviral Protection Mediated by Different Wolbachia Strains in Drosophila simulans Osborne, Sheree E.; Leong, Yi San; O'Neill, Scott L. PLoS Pathogens, Vol. 5, Issue 11 https://doi.org/10.1371/journal.ppat.1000656	journal	November 2009
Midgut Microbiota of the Malaria Mosquito Vector Anopheles gambiae and Interactions with Plasmodium falciparum Infection Boissière, Anne; Tchioffo, Majoline T.; Bachar, Dipankar PLoS Pathogens, Vol. 8, Issue 5 https://doi.org/10.1371/journal.ppat.1002742	journal	May 2012
Symbionts Commonly Provide Broad Spectrum Resistance to Viruses in Insects: A Comparative Analysis of Wolbachia Strains Martinez, Julien; Longdon, Ben; Bauer, Simone PLoS Pathogens, Vol. 10, Issue 9 https://doi.org/10.1371/journal.ppat.1004369	journal	September 2014
Generality of toxins in defensive symbiosis: Ribosome-inactivating proteins and defense against parasitic wasps in Drosophila Ballinger, Matthew J.; Perlman, Steve J. PLOS Pathogens, Vol. 13, Issue 7 https://doi.org/10.1371/journal.ppat.1006431	journal	July 2017
Behavioral betrayal: How select fungal parasites enlist living insects to do their bidding Lovett, Brian; Macias, Angie; Stajich, Jason E. PLOS Pathogens, Vol. 16, Issue 6 https://doi.org/10.1371/journal.ppat.1008598	journal	June 2020
Genetic Diversity and Disease Resistance in Leaf-Cutting ant Societies Hughes, William O. H.; Boomsma, Jacobus J. Evolution, Vol. 58, Issue 6 https://doi.org/10.1554/03-546	journal	January 2004
Leaf-Cutting Ant Herbivory in Successional and Agricultural Tropical Ecosystems Blanton, Chantal M.; Ewel, John J. Ecology, Vol. 66, Issue 3 https://doi.org/10.2307/1940548	journal	June 1985
Pathogenicity of Escovopsis weberi: The Parasite of the Attine Ant-Microbe Symbiosis Directly Consumes the Ant-Cultivated Fungus Reynolds, Hannah T.; Currie, Cameron R. Mycologia, Vol. 96, Issue 5 https://doi.org/10.2307/3762079	journal	September 2004
Pseudonocardia Symbionts of Fungus-Growing Ants and the Evolution of Defensive Secondary Metabolism Goldstein, Sarah L.; Klassen, Jonathan L. Frontiers in Microbiology, Vol. 11 https://doi.org/10.3389/fmicb.2020.621041	journal	December 2020
The Evolutionary Innovation of Nutritional Symbioses in Leaf-Cutter Ants Aylward, Frank O.; Currie, Cameron R.; Suen, Garret Insects, Vol. 3, Issue 1 https://doi.org/10.3390/insects3010041	journal	January 2012
Intracellular Metabolite Pool Changes in Response to Nutrient Depletion Induced Metabolic Switching in Streptomyces coelicolor Wentzel, Alexander; Sletta, Havard; Consortium, Stream Metabolites, Vol. 2, Issue 1 https://doi.org/10.3390/metabo2010178	journal	February 2012

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59 BASIC BIOLOGICAL SCIENCES
antifunga
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hostparasite interactions
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Title: Symbiont-Mediated Protection of Acromyrmex Leaf-Cutter Ants from the Entomopathogenic Fungus Metarhizium anisopliae

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