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Project Progress

Using insect-associated bacteria as model systems, we are exploring the genomic and functional basis of endosymbiotic associations in which prokaryotes replicate within multicellular hosts. This project has important implications for understanding genome-genome interactions among disparate life forms, the evolution of complex life, and the molecular forces that shape beneficial and parasitic associations in endosymbionts. This year, we investigated the molecular evolution and functional genomics of two model systems: Wolbachia, an endosymbiont estimated to infect millions of species worldwide (Fig.1), and Blochmannia, a long-term mutualist of ants that offers of model for highly integrated symbioses.

Using phylogenomic analyses of 22 Wolbachia lineages that vary in symbiotic associations, we determined that parasitic strains arose earlier in the endosymbiosis than the mutualistic strains. This analysis validates a long-standing view that mutualism is typically derived from parasitism and has implications to the origins of organelles and complex life. The evolution of endosymbiotic mutualism is coupled with strict vertical transmission in new host taxa and a complete loss of mobile DNA in the genome. By contrast, parasites still contain active bacteriophages and transposable elements. We determined that transposon insertions can negatively impact the Wolbachia physiology by disrupting essential surface protein genes. Other sequence analyses led to the identification of the origin of replication and a multi-locus sequence typing system to study this dynamic endosymbiont’s transmission, function, and global distribution.

Building upon our completion of the small genome of Blochmannia, we are examing how this nutritional symbiont responds to the dynamic environment of its animal host. The distinct castes of Hymenopteran insects (which include ants) represent the most extreme morphological and biochemical variation ever documented among genetically identical organisms. Thus, this bacterial-ant mutualism offers an ideal system to study symbiont plasticity across genetically identical hosts. Results to date point to differences in symbiont densities and expression patterns across host stages with distinct nutritional requirements. We discovered that expression of key symbiont biosynthetic genes varies in predictable ways. For example, relatively high expression of an essential amino acid gene (trpE) in host pupae matches the severe metabolic demands of this developmental stage. Likewise, we found that symbiont genome copies vary significantly among host stages (p<0.0131, Wilcoxon test), with particularly high densities (30 symbiont genomes per host genome) in reproductive females. Combined, these results point to mechanisms for plasticity in long-term mutualisms. In addition, our comparisons of gene contents across mutualist groups are distinguishing convergent patterns of gene loss in response to an intracellular lifestyle versus genomic differences that catalyze specific host interactions.

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