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Collaborative Research: Dimensions US-São Paulo: Integrating phylogeny, genetics, and chemical ecology to unravel the tangled bank of the multipartite fungus-farming ant symbiosis

Grant number:19/03746-0
Support Opportunities:BIOTA-FAPESP Program - Thematic Grants
Start date: September 01, 2019
End date: August 31, 2026
Field of knowledge:Biological Sciences - Microbiology
Agreement: NSF - Dimensions of Biodiversity and BIOTA
Principal Investigator:André Rodrigues
Grantee:André Rodrigues
Principal researcher abroad:Bryn Dentinger
Institution abroad: University of Utah (U) , United States
Host Institution: Instituto de Biociências (IB). Universidade Estadual Paulista (UNESP). Campus de Rio Claro. Rio Claro , SP, Brazil
City of the host institution:Rio Claro
Principal investigatorsCameron Robert Currie ; Eric Schmidt ; Mauricio Bacci Junior ; Nicole Marie Gerardo ; Theodore Robert Schultz
Associated researchers:Fábio Santos do Nascimento ; Mauricio Bacci Junior ; Milene Ferro ; Pepijn Wilhelmus Kooij ; Simon Luke Elliot
Associated scholarship(s):25/25835-5 - Freeze-drying Escovopsis fungal cultures, BP.TT
25/15773-2 - Curating the collection of microorganisms associated with fungus-growing attine ants, BP.TT
24/16911-7 - Yeast diversity and screening for killer-toxin phenotypes in the Apterostigma ant fungiculture, BP.MS
+ associated scholarships 24/15045-4 - Taxonomy and systematics of Escovopsis symbionts of Apterostigma, BP.IC
24/16915-2 - Curating the collection of microorganisms associated with fungus-growing attine ants, BP.TT
24/06694-9 - Curating the microbial collection derived from attine ants, BP.TT
24/00461-2 - Farming connections: assessing the symbiosis between fungus-growing ants, their gardens and associated microorganisms, BP.JC
24/00463-5 - Farming connections: assessing the symbiosis between fungus-growing ants, their gardens and associated microorganisms, BP.JC
23/11414-2 - Biodegradation of PET by fungi associated with leaf-cutting ants, BP.IC
22/16087-7 - Ecology and systematic of hypocrealean fungi associated with attine ants, BP.DR
23/05135-3 - Impacts of Syncephalastrum on leaf-cutting ant colonies, BP.MS
23/05457-0 - Curating the microbial collection derived from attine ants., BP.TT
21/08013-0 - Fungus gardens of leaf-cutting ants: Functional flexibility, metabolic complementarity, and biotechnological applications, BP.DR
20/12423-7 - Polyols and volatile compounds in ant fungus gardens: ecology, evolution and biotechnological applications, BP.PD
21/05895-2 - Lyophilization of fungal cultures of the genus Escovopsis, BP.TT
21/04706-1 - Unraveling the origin of the parasitic fungus Escovopsis, BP.PD
21/04112-4 - The superorganism immunology: detection, response, and memory in leaf-cutting ants, BP.MS
21/01072-1 - Curating the microbial collection derived from attine ants., BP.TT
20/04639-0 - Lyophilization of cultures of fungi in the genus Escovopsis, BP.TT
19/24412-2 - Diversity and functional roles of yeasts in fungus-growing insects, BP.DR
19/23391-1 - Mycoparasitism in the attine ant fungiculture: host competition in multiple infections, BP.IC - associated scholarships

Abstract

Overview:Species interactions can drive diversification. This is particularly true in cases of coevolved symbioses,where coevolutionary processes can lead to the generation and maintenance of novel functional andgenetic diversity as organisms respond to each over microevolutionary timescales. Furthermore, suchevolutionary coupling can lead to taxonomic diversification, as one or more partners track one anotherover macroevolutionary time scales. While this is widely recognized, much of the underlying diversity insuch systems may be obscured without extensive sampling and taxonomic investigation. This researchtakes a comprehensive approach to uncover suspected hidden diversity within an iconic example ofsymbiotic coevolution, the fungus-growing ant symbiosis. Through broad geographic sampling, targetingtaxa in which we expect to encounter cryptic species, the research team will uncover phylogenetic andtaxonomic diversity of the over two hundred species of ants, their cultivated fungi, parasites that attackthese fungi, and bacteria that function in garden defense and metabolic processes. Couplingmetatranscriptomic and metabolomic approaches, they will characterize genetic diversity, assessingwhether and how the functions of the ants' garden microbiomes complement those of the core symbiontswithin the system. Finally, recognizing that chemical interactions are key drivers of most species'interactions, they will use cutting-edge techniques in natural products research to discover the functionalchemistry underlying symbiont communication, pathogen suppression, and mutualistic facilitation. Thisproject benefits from the wide-ranging expertise of the US-Brazil investigative team, whose researchspans insect and fungal taxonomy, phylogenetics, genomics, and natural products chemistry.Intellectual Merit:While profound insights into organismal evolution and diversification have been gained through the studyof two-way interactions between predators and prey, between hosts and parasites, and betweenmutualistic partners, there is increasing recognition that such coevolutionary processes are embeddedwithin complex ecological communities that involve other species, many of which are microbes. Thiscomplexity may lead to diffuse coevolution, where interacting species do not evolve in response only toone another but to multiple potential partners and antagonists. Assessing whether coevolution andspecialization can be strictly maintained in such a context requires extensive sampling and understandingof the taxonomic, phylogenetic, and functional diversity within a system. Building on previous research inthe fungus-growing ant symbiosis, this research will leverage the diversity of this tractable symbiosis toaddress this central question.Broader Impacts:As a textbook example of symbiosis and coevolution, the fungus-growing ant system has an extensivehistory of research and captivates the public. The team will take a unique approach to collaborate with ahistorian to document their international research and how it builds on previous research. Videointerviews stemming from this collaboration will serve as the backbone of a multimedia videoinstallation, which will be displayed at two museums and a public science festival. In Brazil, theresearchers will lead a workshop for graduate and undergraduate students on microbial isolation. Theproject will train postdocs, graduate students, and undergraduates, who will be recruited through atargeted approach to reach candidates from backgrounds underrepresented in STEM. (AU)

Articles published in Agência FAPESP Newsletter about the research grant:
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Scientific publications (23)
(The scientific publications listed on this page originate from the Web of Science or SciELO databases. Their authors have cited FAPESP grant or fellowship project numbers awarded to Principal Investigators or Fellowship Recipients, whether or not they are among the authors. This information is collected automatically and retrieved directly from those bibliometric databases.)
BARCOTO, MARIANA O.; CARLOS-SHANLEY, CAMILA; FAN, HUAN; FERRO, MILENE; NAGAMOTO, NILSON S.; BACCI, JR., MAURICIO; CURRIE, CAMERON R.; RODRIGUES, ANDRE. Fungus-growing insects host a distinctive microbiota apparently adapted to the fungiculture environment. SCIENTIFIC REPORTS, v. 10, n. 1, . (12/25299-6, 15/16415-0, 19/03746-0, 16/02767-5, 13/50954-0, 17/04824-9)
BIZARRIA, RODOLFO; KOOIJ, PEPIJN W.; RODRIGUES, ANDRE. Climate Change Influences Basidiome Emergence of Leaf-Cutting Ant Cultivars. JOURNAL OF FUNGI, v. 7, n. 11, . (19/24412-2, 19/03746-0)
DE OLIVEIRA, KARINA B.; GOES, ARYEL C.; SILVA, AIRTON D.; VIEIRA, PAULO C.; RODRIGUES, ANDRE. Fungal Cultivars of Higher Attine Ants Promote Escovopsis Chemotropism. Current Microbiology, v. 81, n. 1, p. 12-pg., . (12/25299-6, 18/12481-7, 19/03746-0)
BIZARRIA JR, RODOLFO; PIETROBON, TATIANE DE CASTRO; RODRIGUES, ANDRE. Uncovering the Yeast Communities in Fungus-Growing Ant Colonies. MICROBIAL ECOLOGY, v. N/A, p. 12-pg., . (19/03746-0, 19/24412-2)
MONTOYA, Q. V.; MARTIARENA, M. J. S.; RODRIGUES, A.. Taxonomy and systematics of the fungus-growing ant associate Escovopsis (Hypocreaceae). STUDIES IN MYCOLOGY, v. 106, p. 50-pg., . (14/24298-1, 16/04955-3, 17/12689-4, 21/04706-1, 18/07931-3, 19/03746-0)
GOES, ARYEL C.; KOOIJ, PEPIJN W.; CULOT, LAURENCE; BUENO, ODAIR C.; RODRIGUES, ANDRE. Distinct and enhanced hygienic responses of a leaf-cutting ant toward repeated fungi exposures. ECOLOGY AND EVOLUTION, v. 12, n. 7, p. 13-pg., . (12/25299-6, 19/03746-0, 19/03087-6)
URREA-VALENCIA, SALOME; BIZARRIA JR, RODOLFO; KOOIJ, PEPIJN W.; MONTOYA, QUIMI VIDAURRE; RODRIGUES, ANDRE. Unraveling fungal species cultivated by lower attine ants. MYCOLOGICAL PROGRESS, v. 22, n. 9, p. 19-pg., . (17/12689-4, 17/10631-9, 19/03746-0)
GOES, ARYEL C.; BARCOTO, MARIANA O.; KOOIJ, PEPIJN W.; BUENO, ODAIR C.; RODRIGUES, ANDRE. How Do Leaf-Cutting Ants Recognize Antagonistic Microbes in Their Fungal Crops?. FRONTIERS IN ECOLOGY AND EVOLUTION, v. 8, . (12/25299-6, 19/03087-6, 19/03746-0)
JIMENEZ-GOMEZ, IRINA; BARCOTO, MARIANA O.; MONTOYA, QUIMI V.; GOES, ARYEL C.; MONTEIRO, LANA S. V. E.; BUENO, ODAIR C.; RODRIGUES, ANDRE. Host Susceptibility Modulates Escovopsis Pathogenic Potential in the Fungiculture of Higher Attine Ants. FRONTIERS IN MICROBIOLOGY, v. 12, . (17/12689-4, 19/03746-0)
BAUTZ, KEMINY R.; CAIXETA, MARCELA C. S.; DEL PUPPO, NATHALIA P.; RODRIGUES, ANDRE; KLOSS, THIAGO G.; ELLIOT, SIMON L.. Limited impacts of the fungus Syncephalastrum on nests of leaf-cutting ants. Fungal Ecology, v. 62, p. 7-pg., . (19/03746-0)
PIETROBON, TATIANE DE CASTRO; KOOIJ, PEPIJN WILHELMUS; MONTOYA, QUIMI VIDAURRE; RODRIGUES, ANDRE. Escovopsioides nivea is a non-specific antagonistic symbiont of ant-fungal crops. Fungal Ecology, v. 56, p. 9-pg., . (19/03746-0)
MONTOYA, QUIMI VIDAURRE; GERARDO, NICOLE MARIE; MARTIARENA, MARIA JESUS SUTTA; SOLIS-LEMUS, CLAUDIA; KRIEBEL, RICARDO; SCHULTZ, TED R.; SOSA-CALVO, JEFFREY; RODRIGUES, ANDRE. Digging into the evolutionary history of the fungus-growing-ant symbiont, Escovopsis (Hypocreaceae). COMMUNICATIONS BIOLOGY, v. 8, n. 1, p. 11-pg., . (17/12689-4, 21/04706-1, 18/07931-3, 16/04955-3, 14/24298-1, 19/03746-0)
ASSIS, DIEGO SANTANA; KAKAZU, SERGIO; DA CRUZ, MATEUS OLIVEIRA; DA SILVA, RAPHAEL AFFONSO PEREIRA; MARIN, VITOR RODRIGUES; FERRO, MILENE; SASS, DAIANE CRISTINA; RODRIGUES, ANDRE; BACCI JR, MAURICIO. Ants manage polyol production to fight fungal antagonists. MICROBIOLOGY SPECTRUM, v. 13, n. 6, p. 14-pg., . (21/10639-5, 22/16087-7, 19/03746-0, 20/12423-7)
ANDRE, BIANCA LARIZA OLIVEIRA; MONTOYA, QUIMI VIDAURRE; MARTIARENA, MARIA JESUS SUTTA; RODRIGUES, ANDRE. Culture-dependent methods revel the diversity of endophytic fungi of Psidium cattleianum leaves (Myrtales: Myrtaceae). Brazilian Journal of Microbiology, v. N/A, p. 12-pg., . (21/04706-1, 19/03746-0)
BIZARRIA JR, RODOLFO; PIETROBON, TATIANE DE CASTRO; KOOIJ, PEPIJN W.; RODRIGUES, ANDRE. When Two Species Meet: A Potential Beetle-Yeast Facultative Mutualism. ENVIRONMENTAL MICROBIOLOGY REPORTS, v. 17, n. 4, p. 14-pg., . (19/03746-0, 19/24412-2, 22/16087-7)
AQUINO ZANI, RENATA DE OLIVEIRA; FERRO, MILENE; BACCI JR, MAURICIO. hree phylogenetically distinct and culturable diazotrophs are perennial symbionts of leaf-cutting ant. ECOLOGY AND EVOLUTION, v. 11, n. 24, . (17/04824-9, 19/03746-0)
MONTOYA, QUIMI VIDAURRE; SUTTA MARTIARENA, MARIA JESUS; BIZARRIA JR, RODOLFO; GERARDO, NICOLE MARIE; RODRIGUES, ANDRE. Fungi inhabiting attine ant colonies: reassessment of the genus Escovopsis and description of Luteomyces and Sympodiorosea gens. nov.. IMA FUNGUS, v. 12, n. 1, . (19/03746-0, 14/24298-1, 18/07931-3, 17/12689-4, 16/04955-3)
BARRERA, CORINA A.; SOSA-CALVO, JEFFREY; SCHULTZ, TED R.; RABELING, CHRISTIAN; BACCI, MAURICIO. hylogenomic reconstruction reveals new insights into the evolution and biogeography of Atta leaf-cutting ants (Hymenoptera: Formicidae. Systematic Entomology, v. 47, n. 1, . (19/03746-0, 19/24470-2)
BIZARRIA, JR., RODOLFO; PAGNOCCA, FERNANDO CARLOS; RODRIGUES, ANDRE. easts in the attine ant-fungus mutualism: Diversity, functional roles, and putative biotechnological application. YEAST, v. 39, n. 1-2, SI, . (19/24412-2, 19/03746-0)
MARTIARENA, MARIA JESUS SUTTA; DEVEAU, AURELIE; MONTOYA, QUIMI VIDAURRE; FLOREZ, LAURA V.; RODRIGUES, ANDRE. The Hyphosphere of Leaf-Cutting Ant Cultivars Is Enriched with Helper Bacteria. MICROBIAL ECOLOGY, v. N/A, p. 16-pg., . (21/04706-1, 19/03746-0, 17/12689-4, 14/24298-1)
CROUS, P. W.; CATCHESIDE, D. E. A.; CATCHESIDE, P. S.; ALFENAS, A. C.; ALFENAS, R. F.; BARRETO, R. W.; LEBEL, T.; BALASHOV, S.; BROADBRIDGE, J.; JURJEVIC, Z.; et al. Fungal Planet description sheets: 1781-1866. PERSOONIA, v. 54, n. 1, p. 261-pg., . (22/16087-7, 19/03746-0)
BARCOTO, MARIANA OLIVEIRA; SILVA, RAPHAEL AFFONSO PEREIRA; KITAJIMA, ELLIOT WATANABE; RODRIGUES, ANDRE. Microbiota of Attine Ants' Gardens: Visualizing a Microbial Landscape by Scanning Electron Microscopy. JOVE-JOURNAL OF VISUALIZED EXPERIMENTS, v. N/A, n. 212, p. 24-pg., . (21/08013-0, 19/03746-0)
BERASATEGUI, AILEEN; SALEM, HASSAN; MOLLER, ABRAHAM G.; CHRISTOPHER, YULIANA; VIDAURRE MONTOYA, QUIMI; CONN, CAITLIN; READ, TIMOTHY D.; RODRIGUES, ANDRE; ZIEMERT, NADINE; GERARDO, NICOLE. Genomic insights into the evolution of secondary metabolism of Escovopsis and its allies, specialized fungal symbionts of fungus-farming ants. MSYSTEMS, v. 9, n. 7, p. 23-pg., . (21/04706-1, 19/03746-0)