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, 2025
• 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
• Pesquisadores principais: Cameron 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): 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; + associated scholarships 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 and genetic diversity as organisms respond to each over microevolutionary timescales. Furthermore, such evolutionary coupling can lead to taxonomic diversification, as one or more partners track one another over macroevolutionary time scales. While this is widely recognized, much of the underlying diversity in such systems may be obscured without extensive sampling and taxonomic investigation. This research takes a comprehensive approach to uncover suspected hidden diversity within an iconic example of symbiotic coevolution, the fungus-growing ant symbiosis. Through broad geographic sampling, targeting taxa in which we expect to encounter cryptic species, the research team will uncover phylogenetic and taxonomic diversity of the over two hundred species of ants, their cultivated fungi, parasites that attack these fungi, and bacteria that function in garden defense and metabolic processes. Coupling metatranscriptomic and metabolomic approaches, they will characterize genetic diversity, assessing whether and how the functions of the ants' garden microbiomes complement those of the core symbionts within 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 functional chemistry underlying symbiont communication, pathogen suppression, and mutualistic facilitation. This project benefits from the wide-ranging expertise of the US-Brazil investigative team, whose researchs pans 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 study of two-way interactions between predators and prey, between hosts and parasites, and between mutualistic partners, there is increasing recognition that such coevolutionary processes are embedded within complex ecological communities that involve other species, many of which are microbes. This complexity may lead to diffuse coevolution, where interacting species do not evolve in response only to one another but to multiple potential partners and antagonists. Assessing whether coevolution and specialization can be strictly maintained in such a context requires extensive sampling and understanding of the taxonomic, phylogenetic, and functional diversity within a system. Building on previous research in the fungus-growing ant symbiosis, this research will leverage the diversity of this tractable symbiosis to address this central question. Broader Impacts: As a textbook example of symbiosis and coevolution, the fungus-growing ant system has an extensive history of research and captivates the public. The team will take a unique approach to collaborate with a historian to document their international research and how it builds on previous research. Video interviews stemming from this collaboration will serve as the backbone of a multimedia video installation, which will be displayed at two museums and a public science festival. In Brazil, the researchers will lead a workshop for graduate and undergraduate students on microbial isolation. The project will train post docs, graduate students, and undergraduates, who will be recruited through a targeted approach to reach candidates from backgrounds underrepresented in STEM. (AU)

Scientific publications

(19)

(References retrieved automatically from Web of Science and SciELO through information on FAPESP grants and their corresponding numbers as mentioned in the publications by the authors)

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., 2022-04-01. (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, MAY 5 2020. (12/25299-6, 19/03087-6, 19/03746-0)

BIZARRIA, RODOLFO; KOOIJ, PEPIJN W.; RODRIGUES, ANDRE. Climate Change Influences Basidiome Emergence of Leaf-Cutting Ant Cultivars. JOURNAL OF FUNGI, v. 7, n. 11, NOV 2021. (19/24412-2, 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., 2022-07-01. (12/25299-6, 19/03746-0, 19/03087-6)

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., 2022-08-12. (19/03746-0, 19/24412-2)

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, JUN 14 2021. (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., 2023-02-16. (19/03746-0)

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., 2023-12-01. (14/24298-1, 16/04955-3, 17/12689-4, 21/04706-1, 18/07931-3, 19/03746-0)

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., 2024-08-19. (21/04706-1, 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., 2024-01-01. (12/25299-6, 18/12481-7, 19/03746-0)

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., 2023-09-01. (17/12689-4, 17/10631-9, 19/03746-0)

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, JUL 24 2020. (12/25299-6, 15/16415-0, 19/03746-0, 16/02767-5, 13/50954-0, 17/04824-9)

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, SEP 2021. (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, SEP 2021. (19/24412-2, 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, AUG 24 2021. (19/03746-0, 14/24298-1, 18/07931-3, 17/12689-4, 16/04955-3)

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., 2023-02-09. (21/04706-1, 19/03746-0, 17/12689-4, 14/24298-1)

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, DEC 2021. (17/04824-9, 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., 2024-06-21. (21/04706-1, 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., 2024-10-01. (21/08013-0, 19/03746-0)