EVOLUTION OF WOLBACHIA SYMBIOSIS IN ARTHOPODS AND NEMATODES: INSIGTHS FROM PHYLOGENETICS AND COMPARATIVE GENOMICS

Wolbachia is a bacterium observed in relationship with a wide array of arthropod and nematode species. This is an obligate intracellular symbiont, maternally transferred through the host oocytes. In arthropods Wolbachia is able to manipulate reproduction, using multiple strategies to increase the fitness of infected females. In nematodes the bacterium has a fundamental, and not completely understood, role in larvae development. Wolbachia infects ~50% of all the arthropod species worldwide, and in some of them it can be considered the most important sex determination factor. In contrast, Wolbachia presence is much more limited in nematodes, being present in a limited number of filarial species. The taxonomic status within the Wolbachia genus is highly debated, with the current classification dividing all strains in 14 'supergroups'. During my Ph.D. I studied the evolution of the symbiotic relationship between Wolbachia and its arthropod and nematode hosts, using genomic approaches. Indeed, during the evolution of the Wolbachia-host relationship, genetic signs have been left in the Wolbachia genomes. I worked to identify these genomic signs and to evaluate them within an evolutionary frame, in order to obtain a better understanding of how the Wolbachia-host symbiosis evolved. The work here presented can be organized in three major sections: i) the sequencing and analysis of the genome of the filarial nematode Dirofilaria immitis and of its symbiotic Wolbachia strain, wDi; ii) the sequencing of the genome of Wolbachia endosymbiont of Litomosoides sigmodontis, and the phylogenomic reconstruction of the Wolbachia supergroups A-D; iii) a comparison of the genomes of 26 Wolbachia strains spanning the A to F supergroups. Here a schematic summary of the results is reported: 1. Dirofilaria immitis and the Wolbachia symbiont wDi show metabolic complementarity for fundamental pathways 2. The metabolic pathway for the synthesis of wDi membrane proteins is one evolving the fastest in the genome of the bacterium 3. Nematode Wolbachia belonging to supergroups C and D are monophyletic, indicating that a single transition to mutualism likely occurred during the evolution of Wolbachia 4. Wolbachia strains of the C supergroup show genomic features that are unique in the genus, such as a much higher level of synteny compared to the rest of Wolbachia supergroups, and a newly generated pattern of GC skew curves, typically observed in free-living bacteria genomes 5. Wolbachia supergroups show conserved genomic features, which suggest genomic isolation among them.