Stolen genes, a shortcut to success : Evolution of metabolic and detoxification capacities in Diplomonads

Parasites do not represent a single evolutionary lineage meaning that they have evolved several times. The changes that parasites have undergone to adapt to such a lifestyle are not entirely understood. This thesis focuses on the study of diplomonads (Fornicata, Metamonada), a group of host-associated or free-living protists, to better understand how they adapted to different environments and hosts. Diplomonads, and close relatives, are found in low-oxygen environments. However, some species can withstand fluctuating levels of oxygen. In a first study, we reconstructed the oxygen detoxification pathway of Fornicata and study its evolution. Comparative genomics showed that Fornicata shares a common pathway with lineage-specific modifications. Phylogenetic analyses showed a pathway in a constant change where proteins have been gained and lost. In a second study, the Giardia muris genome was sequenced and compared to the genome of G. intestinalis WB. We reconstructed the metabolic capacities of both species. Our analyses showed that the observed differences are the result of gene acquisitions or differential losses that can be explained based on differences in the environment of the hosts. Considering what we observed in the two previous studies, we reconstructed the metabolic capacities of four diplomonads. Using cluster analysis, we reconstructed the putative metabolism of the last Diplomonadida common ancestor. Our analyses suggested that this ancestor was, most likely, an obligate host-associated organism. However, we identified that traits associated with parasitic diplomonads evolved in a free-living ancestor. In the last study, we analyzed the genome of Hexamita inflata, a free-living, diplomonad. Our analyses showed that Trepomonas sp. PC1 and H. inflata acquired important genes for the adaptation to a secondary free-living in a common ancestor. However, our analyses also showed independent adaptations. The synthesis of glutathione and the acquisition of glutathione peroxidase, most likely, allow H. inflata to detoxify higher levels of oxygen and arsenic than other diplomonads. In conclusion, this thesis highlights the value of metabolic analyses to identify how microbial eukaryotes interact with their environment. The phylogenetic approach shows that the acquisition of genes and differential losses have been important processes in the adaptation of different hosts and environments