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Project Progress

This project aims to elucidate genetic changes that catalyze the establishment and diversification of genome-genome interactions. Using insect-associated endosymbionts as model systems, we are examining the molecular and evolutionary forces that shape associations between bacteria and eukaryotic hosts. Our studies target Proteobacterial species that represent both long-term, stable mutualisms and transient parasitic interactions.

This year we completed the 792 kb genome sequence of Blochmannia pennsylvanicus, an intracellular mutualist of carpenter ants. This genome was sequenced in house at the MBL. Comparisons with related bacterial species revealed mechanisms driving severe genome reduction in microbes engaged in long-term host associations. For example, the ant mutualist retains numerous biosynthetic pathways due to host-level selection for nutritional functions, but has lost many genes to utilize diverse substrates in the environment. Its small genome also exhibits exceptionally fast rates of amino acid substitutions, yet shows remarkable genome stability with no gene acquisitions, inversions, or translocations for ~20 MY of its host association. This discovery illustrates that an intracellular lifestyle can alter fundamental mechanisms for genetic change in bacteria. Along with our primary genome publication (Degnan et al., 2005), broader comparisons across intracellular bacteria are described in an upcoming review (Wernegreen, submitted) and a collaborative study of mutualist genomes (Schaber et al., 2005). We also completed molecular evolution analyses that demonstrated strong mutational pressure and genetic drift in obligate endosymbionts (Wernegreen and Funk, 2004; Fry and Wernegreen, 2005) and developed new phylogenetic approaches to better resolve bacterial phylogenies and identify the origins of intracellular groups (Herbeck et al., 2005).

Our research progress on Wolbachia genome evolution and viruses went farther than expected this year. Wolbachia are a genus of obligate intracellular α—Proteobacteria that are closely related to the bacterial ancestor of mitochondria. These bacteria show moderate rates of host-switching and have largely formed parasitic associations with a wide arthropod host range. Our comprehensive review article on mobile DNA in intracellular bacteria (to be featured in a Nature Reviews special issue on horizontal gene transfer, Bordenstein and Reznikoff, 2005) highlights the extraordinary phage and transposon colonization of the Wolbachia genome relative to other obligate and facultative intracellular species. Bioinformatic and molecular phylogenetic studies this past year determined that a Wolbachia temperate phage is the only element known to frequently laterally transfer between obligate, intracellular bacteria (Bordenstein and Wernegreen, 2004) as well as vector transposable elements into the tiny genomes of Wolbachia (Reznikoff et al., 2004). Of the 1271 genes annotated in Wolbachia, our comparative genomic hybridizations using DNA microarrays (performed in collaboration with TIGR) indicate that the largest fraction of divergent genes between strains tends to be prophage, a finding that is unique among bacterial endosymbionts, yet typical for other free-living bacterial systems in which mobile and repetitive DNA are significant diversifying agents. We also completed molecular evolutionary analyses that specified novel genetic lineages of Wolbachia (Bordenstein and Rosengaus, 2005), the molecular phylogeny of this endosymbiont (Casiraghi et al., submitted), and extensive recombination among housekeeping genes (Baldo et al., in preparation).

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