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| Research Overview |
We use an integrative approach to study the dynamics of host-microbe ecology and evolution. Our goal is to gain a broader understanding of how host and microbe responses shape the evolution of both beneficial and harmful associations by developing study systems in which we can manipulate species interactions in order to elucidate adaptive mechanisms and the genetics behind those mechanisms. To address such questions, we utilize insect–microbe associations amenable to long-term laboratory maintenance and experimental manipulation.PUBLICATIONS |
| Aphid-Microbe Interactions |
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 work is of increasing interest as many animals must be able to keep beneficial bacteria while eliminating harmful ones. Emory News Article of the Publication of the Pea Aphid Genome Paper Daily Mail Article on the Publication of the Pea Aphid Genome Paper |
| The 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. We have established that highly-specific host and parasite adaptations shape the ability of Escovopsis lineages to switch to novel hosts over evolutionary time. Specifically, we demonstrated that, in in vitro bioassays, 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 genomics 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. Scientific American Blog on the Sequencing of the Atta cephalotes genome |
| The Invasion of a Symbiosis: Megacopta Stinkbugs |
| Megacopta Cribraria 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. |
| Monarch Butterflies and Immunity |
Monarch butterflies (Danaus plexippus) occur in populations worldwide and are often infected with a protozoan parasite (Ophryocystis elektroscirrha). This system, which is well-studied in Jaap de Roode’s lab, provides all ingredients necessary to investigate the effect of parasite pressure on the evolution of host immunity. First, the parasite has a large detrimental effect on the fitness of the host by reducing its survival. Second, parasite prevalence differs dramatically between populations, ranging from 5% of monarchs infected in some populations to over 80% in others. Third, monarch populations differ in the species of milkweed that they utilize as a host plant; because consumption of some plant species can reduce parasite infection, these populations differ in their ability to reduce parasite risk. Fourth, monarchs and parasites from all populations can be kept in the lab to carry out experiments on infection and immunity. Despite the suitability of this host-parasite system, there is one serious shortcoming, which is that we currently have no knowledge of the monarch’s immune responses nor of the genes that underlie these responses. The Gerardo and De Roode Labs, therefore, are currently sequencing RNA transcripts in infected and uninfected monarchs using 454 sequencing technology. Because RNA transcripts are the molecules used to translate activated genes into functional proteins, the presence of a particular RNA transcript indicates gene activation and protein production. Hence, by comparing the transcripts of infected and uninfected monarchs, we will be able to tell which genes are specifically activated during parasite infection. We plan to follow up this preliminary work with investigation of how immunological responses are altered by alternative protective host plants and by the butterflies' microbial gut community. |
| Selected Publications |
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Barribeau, S. and N.M. Gerardo. An evolutionarily and ecologically based strategy for genome sequencing efforts. Heredity, in press. Altincicek, B., Kovacs, J.L. and N.M. Gerardo. 2011. Horizontally-transferred fungal carotenoid genes in the two-spotted spider mite Tetranychus urticae. Biology Letters, in press. Altincicek, B., ter Braak, B., Laughton, A.M., Udekwi, K.I. and N.M. Gerardo. 2011. Escherichia coli K-12 pathogenicity in the pea aphid, Acyrthosiphon pisum, reveals reduced antibacterial defense in aphids. Developmental and Comparative Immunology 35(10): 1091-1097. Laughton, A.L., Hall, J.R., Strand, M., Altincicek, B. and N.M. Gerardo. 2011. Characterisation of immune responses in the pea aphid, Acyrthosiphon pisum. Journal of Insect Physiology 57(6): 830-839. Parker, B.J., Barribeau, S.M., Laughton, A.L., de Roode, J.C. and N.M. Gerardo. 2011. Non-immunological defense in an evolutionary framework. Trends in Ecology and Evolution 26(5): 242-8. De Roode, J., Rarick, R., Mongue. A., Gerardo, N.M., Hunter, M. 2011. Aphids indirectly increase virulence and transmission potential of a monarch butterfly parasite by reducing defensive chemistry of a shared food plant. Ecology Letters. Cafaro, M.J., Poulsen, M., Little, A.E.F., Price, S.L., Gerardo, N.M., Wong, B., Stuart, A.E., Larget, B., Abbot, P. and C.R. Currie. Specificity in the symbiotic association between fungus-growing ants and protective Pseudonocardia bacteria. Accepted, Proceedings of the Royal Society of London, B. Barribeau, S., Sok, D. and N.M. Gerardo. 2010. Bacterial symbionts alter aphid reproductive investment in response to mortality risk. BMC Evolutionary Biology. 10:article 251. Gerardo, N.M., Altincicek, B., Anselme C., Atamian, H., Barribeau, S.B., de Vos, M, Duncan, E.J., Evans, J.D., Gabaldon, T., Ghanim, M., Heddi, A., Kaloshian, I., Latorre, A., Moya, A., Nakabachi, A., Parker, B.J.**, Perez-Brocal, V., Pignatelli, M., Rahbe, Y., Ramsey, J., Spragg, C., Tamames, J., Tamarit, D., Tamborindeguy, C., Vincent-Montegat, C. and A. Vilcinskas. Immunity and defense in pea aphids, Acyrthrosiphon pisum..Genome Biology 11(2):R21 The International Aphid Genomics Consortium. 2010. The genome of the pea aphid, Acyrthosiphon pisum. PLOS Biology 8(2):e1000313.(Project Leader) Poulsen M, Erhardt D, Little AEF, Gerardo NM, Tebbets B, Klein B, Currie CR. 2010. Variation in Pseudonocardia antibiotic defense helps govern parasite-induced morbidity in Acromyrmex leaf-cutting ants. Environmental Microbiology Reports 2(10):534-540. Gerardo, N.M. & E.J. Caldera. 2007. Labile associations between fungus-growing ant cultivars and their garden pathogens. International Society for Microbial Ecology Journal (ISME). Gerardo, N.M., U.G. Mueller & C.R. Currie. 2006. Complex host-pathogen coevolution in the Apterostigma fungus-growing ant-microbe symbiosis. BMC Evolutionary Biology 6(88). Gerardo, N.M., Jacobs, S., Currie, C.R.. & U.G. Mueller. 2006. Ancient host-pathogen associations maintained by specificity of chemotaxis and antibiosis. Public Library of Science - Biology (PLOS Biology) 4(8): 1358-1363. Moran, N. A., P. Tran , & N. M. Gerardo. 2005. Symbiosis and insect diversification: an ancient symbiont of sap-feeding insects from the bacterial phylum Bacteroidetes. Applied and Environmental Microbiology 71(12): 8802-8810. Mueller, U.G., N.M. Gerardo, D. Aanen, D. Six & T. Schultz. 2005. The evolution of agriculture in insects. Annual Review of Ecology, Evolution and Systematics 36: 563-595. Gerardo, N.M., U.G. Mueller, S. Price & C.R. Currie. 2004. Exploiting a mutualism: parasite specialization on cultivars within the fungus-growing ant symbiosis. Proceedings of the Royal Society B 271: 1791-1798.
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