Certain ants cultivate fungi as their major food source. The ants collect and transport vegetable substrate to a "garden," usually a sheltered chamber excavated in the ground, then plant fungus on this new substrate. Gardens of fungus-growing ants are foci of interactions within a community of ants, the cultivated fungus, and a great diversity of additional microbes. Specifically, pathogens attacking the ants or the fungal gardens can cause the death of the nest community, but a variety of auxiliary microbes contribute disease-suppressing properties that control such pathogens. Disease resistance to pathogens is shaped by the genetic identity of both the ant and the fungus and the interaction of these two dominant community members with the auxiliary microbes. This research will elucidate how these nest community members interact and co-evolve in response to pathogen presence. To understand disease dynamics, the research will (a) characterize the inheritance of assemblages of auxiliary microbes from maternal to offspring ant nest; (b) determine the importance of co-inheritance of ant-fungus-microbe combinations to disease resistance of the community; and (c) evaluate the relative contribution to disease-resistance by ant, fungus, and auxiliary microbes. The research integrates a variety of experimental approaches within an ecological-genetics and quantitative-genetics framework, contributing towards a unification of ecology and evolutionary biology.

Inheritance of auxiliary microbes between generations occurs in diverse hosts, including humans, but the importance of communities of auxiliary microbes in their contribution to the health of a host is incompletely understood. This research develops novel experimental approaches to elucidate the role of auxiliary microbe communities in disease suppression. Because microbial communities also confer disease resistance for humans (e.g., the microbiome of human skin or gut) and for crops (e.g., the microbiome of roots), this research on fungus-growing ants will contribute to the understanding of general microbial principles with applications to human and agricultural disease management. Fungus-growing ants and their microbes will also be used to promote education of students and the public on the importance of ecological, evolutionary, and all biological processes. A postdoctoral researcher and multiple undergraduates will be trained and mentored in this research project.

Project Report

Most organisms depend on beneficial microbiomes (e.g., humans depend on beneficial gut-microbiomes), and microbiomes can provide diverse benefits, including protection of a host organism against disease. In such host organisms, disease resistance to pathogens is an emergent community property that is shaped by complex interactions between host genotype and genotypes of associated microbes. These complex interactions are difficult to elucidate experimentally in vertebrate hosts, but can be manipulated readily in insect hosts that depend on complex microbiomes, for example in fungus-growing ants that engineer microbiomes in their cultivated gardens. The research used a variety of experimental, ecological-genetic, and quantitative-genetics approaches to elucidate how fungus-growing ants manipulate microbiomes benefitting growth and health. Fungus-growing ants propagate their cultivars as clonal monocultures within their nests, and inherit fungi clonally across many ant generations. Crop clonality generates problems for disease control, but fungus-growing ants employ complex strategies to manage crop diseases. Most importantly, fungus-growing ants engineer communities of "auxiliary" microbiomes (e.g., bacteria, yeasts) in their gardens in addition to the primary fungal cultivars, and these auxiliary microbiomes provide disease-suppressing antibiotics, enzymes, or other services. Rather than cultivating a single cultivar solely for nutrition, fungus-growing ants engineer integrated and co-propagated crop-microbe consortia. In a first phase of the project, to understand disease dynamics in ant fungiculture, the research characterized the inheritance of assemblages of auxiliary microbes from maternal to offspring ant nests; determined the importance of strict co-inheritance of ant-fungus-microbe combinations to disease resistance of the community; and evaluated the relative contribution to disease-resistance by the ant host, the cultivated fungus, and the auxiliary microbiomes. Two postdoctoral researchers, two technicians, three graduate students, and twelve undergraduate research assistants were trained during the project. In a second phase of the project, exceeding the original research goals, the research adapted the microbiome-engineering principles observed in ants to develop a method of plant-bacterial-community co-propagation that enhances plant growth. Root-associated (rhizosphere) bacterial communities rapidly evolved differences between microbiome selection-lines that were selected for either growth-enhancing versus growth-attenuating effects on plants, documenting that artificial selection on microbiomes through plant-microbiome co-propagation can engineer rhizosphere bacterial-communities benefitting plant growth. Because these plant-microbiome co-propagation methods were bio-inspired by fungus-growing ants, research on organismal adaptations (i.e., the microbiome-engineering methods of ants) therefore can generate innovative ideas with economic applications. Experimental host-microbiome co-propagation protocols developed to engineer beneficial microbiomes in agriculture and animal-welfare were disseminated to the general research community.

Agency
National Science Foundation (NSF)
Institute
Division of Environmental Biology (DEB)
Type
Standard Grant (Standard)
Application #
0919519
Program Officer
Alan James Tessier
Project Start
Project End
Budget Start
2009-08-15
Budget End
2014-07-31
Support Year
Fiscal Year
2009
Total Cost
$513,611
Indirect Cost
Name
University of Texas Austin
Department
Type
DUNS #
City
Austin
State
TX
Country
United States
Zip Code
78712