Trachymyrmex septentrionalis ants promote fungus garden hygiene using Trichoderma-derived metabolite cues
Por:
Kyle, Kathleen E., Puckett, Sara P., Caraballo-Rodriguez, Andres Mauricio, Rivera-Chavez, Jose, Samples, Robert M., Earp, Cody E., Raja, Huzefa A., Pearce, Cedric J., Ernst, Madeleine, van der Hooft J.J.J., Adams, Madison E., Oberlies, Nicholas H., Dorrestein, Pieter C., Klassen, Jonathan L., Balunas, Marcy J.
Publicada:
1 ene 2023
Categoría:
Multidisciplinary
Resumen:
Fungus-growing ants depend on a fungal mutualist that can fall prey to fungal pathogens. This mutualist is cultivated by these ants in structures called fungus gardens. Ants exhibit weeding behaviors that keep their fungus gardens healthy by physically removing compromised pieces. However, how ants detect diseases of their fungus gardens is unknown. Here, we applied the logic of Koch's postulates using environmental fungal community gene sequencing, fungal isolation, and laboratory infection experiments to establish that Trichoderma spp. can act as previously unrecognized pathogens of Trachymyrmex septentrionalis fungus gardens. Our environmental data showed that Trichoderma are the most abundant noncultivar fungi in wild T. septentrionalis fungus gardens. We further determined that metabolites produced by Trichoderma induce an ant weeding response that mirrors their response to live Trichoderma. Combining ant behavioral experiments with bioactivity-guided fractionation and statistical prioritization of metabolites in Trichoderma extracts demonstrated that T. septentrionalis ants weed in response to peptaibols, a specific class of secondary metabolites known to be produced by Trichoderma fungi. Similar assays conducted using purified peptaibols, including the two previously undescribed peptaibols trichokindins VIII and IX, suggested that weeding is likely induced by peptaibols as a class rather than by a single peptaibol metabolite. In addition to their presence in laboratory experiments, we detected peptaibols in wild fungus gardens. Our combination of environmental data and laboratory infection experiments strongly support that peptaibols act as chemical cues of Trichoderma pathogenesis in T. septentrionalis fungus gardens.
Filiaciones:
Kyle, Kathleen E.:
Department of Molecular and Cell Biology, University of Connecticut, Storrs, CT 06269, United States
Puckett, Sara P.:
Division of Medicinal Chemistry, Department of Pharmaceutical Sciences, University of Connecticut, Storrs, CT 06269, United States
Caraballo-Rodriguez, Andres Mauricio:
Collaborative Mass Spectrometry Innovation Center, Skaggs School of Pharmacy and Pharmaceutical Sciences, University of California San Diego, La Jolla, CA 92093-0657
Rivera-Chavez, Jose:
Department of Chemistry and Biochemistry, University of North Carolina at Greensboro, Greensboro, United States
Department of Natural Products, Instituto de Química, Universidad Nacional Autónoma de México, Coyoacán, Mexico City 04510, Mexico
Samples, Robert M.:
Division of Medicinal Chemistry, Department of Pharmaceutical Sciences, University of Connecticut, Storrs, CT 06269, United States
Department of Chemistry, University of Connecticut, Storrs, CT 06269, United States
Earp, Cody E.:
Department of Chemistry and Biochemistry, University of North Carolina at Greensboro, Greensboro, United States
Raja, Huzefa A.:
Department of Chemistry and Biochemistry, University of North Carolina at Greensboro, Greensboro, United States
Pearce, Cedric J.:
Mycosynthetix, Inc., Hillsborough, United Kingdom
Ernst, Madeleine:
Department of Congenital Disorders, Section for Clinical Mass Spectrometry, Danish Center for Neonatal Screening, Statens Serum Institut, Copenhagen, 2300, Denmark
van der Hooft J.J.J.:
Bioinformatics Group, Wageningen University & Research, PB Wageningen, 6708, Netherlands
Department of Biochemistry, University of Johannesburg, Auckland Park, Johannesburg, 2006, South Africa
Adams, Madison E.:
Department of Molecular and Cell Biology, University of Connecticut, Storrs, CT 06269, United States
Oberlies, Nicholas H.:
Department of Chemistry and Biochemistry, University of North Carolina at Greensboro, Greensboro, United States
Dorrestein, Pieter C.:
Collaborative Mass Spectrometry Innovation Center, Skaggs School of Pharmacy and Pharmaceutical Sciences, University of California San Diego, La Jolla, CA 92093-0657
Department of Pharmacology, University of California San Diego, La Jolla, CA 92093-0657
Department of Pediatrics, University of California San Diego, La Jolla, CA 92093-0657
Klassen, Jonathan L.:
Department of Molecular and Cell Biology, University of Connecticut, Storrs, CT 06269, United States
Balunas, Marcy J.:
Division of Medicinal Chemistry, Department of Pharmaceutical Sciences, University of Connecticut, Storrs, CT 06269, United States
Department of Microbiology and Immunology, University of Michigan, Ann Arbor, MI 48109, United States
Department of Medicinal Chemistry, University of Michigan, Ann Arbor, MI 48109, United States
Green Submitted, hybrid, Hybrid Gold
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