Aphids are host to both beneficial and harmful microbes. Of benefit, aphids harbor, Buchnera aphidicola, an obligate bacterial symbiont, which provides amino acids not available in the aphid diet. Aphids frequently also harbor facultative, symbiotic bacteria that provide protection against heat stress, fungal pathogens and parasitic wasps. Aphid pathogens include a number of viruses, fungi and bacteria.
One goal is to understand how the aphids’ own immune defenses are coupled with protection conferred by symbionts to mediate the outcome and evolution of disease. We are currently working to annotate and functionally characterize the immune capacity of aphids, focusuing on Acyrthosiphon pisum (the pea aphid). Part of this work is in collaboration with members of the International Aphid Genomics Consortium, including Boran Altincicek and Alex Wilson.
We are also interested in how aphids respond to the establishment of symbiotic versus pathogenic microbes. This question is of increasing interest as many animals must be able to keep beneficial bacteria while eliminating harmful ones. Our work on aphid immunity is funded by the National Science Foundation.
Fungus-Growing Ant Symbiosis
The fungus-growing ant–microbe symbiosis consists of coevolving microbial mutualists and pathogens. The diverse fungal lineages that the ants cultivate are attacked by parasitic microfungi in the genus Escovopsis. Highly specific host and parasite adaptations shape the ability of Escovopsis lineages to switch to novel hosts over evolutionary time. Specifically, Escovopsis spp. are attracted to their hosts via chemotaxis. This response is host-specific; Escovopsis spp. grow toward their natural host-cultivars more rapidly than toward other closely-related fungi. Moreover, the cultivated fungi secrete compounds that can suppress Escovopsis growth. These antibiotic defenses are likewise specific; in most interactions, cultivars can inhibit growth of Escovopsis spp. not known to infect them in nature but cannot inhibit isolates of their naturally-infecting pathogens. Targeted chemotactic and antibiotic responses therefore explain why Escovopsis pathogens do not readily switch to novel hosts, consequently constraining long-term dynamics of host–parasite coevolution within this ancient association.
As a next step in this research, we have established collaborations with chemists to begin to understand a) what chemical signals Escovopsis uses to recognize its hosts, and b) what antibiotics the host cultivars use to suppress Escovopsis. We will couple this work with laboratory infections of colonies to determine whether the attraction and inhibition that we see in vitro correlates with infectivity in vivo.
With a team of collaborators, we received funding from Roche 454 to complete 10GB of 454 sequencing to explore the genomes and transcriptomes of the ants, their fungi, and associated mutualistic and parasitic players in the symbiosis. These genomic resources will serve as tools for researchers exploring broad aspects of the fungus-growing ant symbiosis. Thus far, we have published the genome of one fungus-growing ant species and we are currently working on genomes of one strain of cultivated fungus and one strain of fungal pathogen.
Invasion of a Symbiosis: Megacopta cribraria and its Bacteria
Megacopta Cribraria, the Kudzu Bug, is a pest of soybeans in Asia. In Japan, the ability of these stinkbugs to utilize soybeans is dictated by what strain of bacterial symbiont the bugs carry. In Fall 2009, these bugs were first found in the United States. They have since spread onto soybeans in several states in the Southeastern United States. In collaboration with Tracie Jenkins (U. of Georgia, Griffin Campus), Paul Smith (U. of Georgia), Meg Allen (USDA) and John McCutcheon (U. Montana), and with funding from the United States Department of Agriculture, we are exploring how symbionts impact the invasion of this pest insect in the United States. We will sequence the genome of the bacteria in the North American population, and we will monitor the spread of both insect and symbiont diversity. We will couple this work with studies of the host plant range of these insects, both with and without their bacteria.
Broad-Headed Bugs and their Symbionts
For many insects, including aphids, beneficial symbionts are maternally inherited by offspring before birth, ensuring infection. While beneficial to the insect, this makes experimentation on host and microbe responses during symbiont establishment more challenging. Many true bug species have obligate associations with symbiotic bacteria that are transmitted externally. These systems allow us to introduce the symbiont through the natural route of infection and then monitor immunological and genetic responses. We are currently interested in determining host and symbiont traits that mediate establishment and maintenance of environmentally-acquired symbionts in four local broad-headed bug species. We are characterizing specificity of the association between these sympatric broad-headed bug species and Burkholderia bacteria by comparing the Burkholderia community in these bugs to the diversity of Burkholderia found in root nodules of the bugs’ leguminous host plants, and in soil near host plants. We are using these cultivable isolates in controlled infection experiments to determine the role that bacterial-conferred benefits, bacterial genotype, bacterial gene expression, host behavior, and host immune responses play in establishing and maintaining the symbiosis.