Genome evolution and radical lifestyle changes in eukaryotic microbes

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Changes in evolutionary trajectories entail deep alterations in the biology of organisms, often at the level of genomic organization. A key example is genomic reduction after acquisition of an intracellular parasitic lifestyle, a phenomenon that has been investigated in bacterial endosymbionts. Eukaryotic genomes are larger and more complex than their bacterial counterparts, and the consequences of lifestyle changes on their genomes are poorly known. My research program has the long-term goal of improving our understanding of the evolution of eukaryotic genomes, with emphasis on the relationships between life history (e.g. symbiosis, parasitism) and genome form/function. To this aim, I focus my study on members of ALVEOLATA, a diverse group of eukaryotic microbes composed by apicomplexan, dinoflagellate and ciliate protozoa. This lineage is particularly well suited to investigate these questions. On one side, the apicomplexans evolved from free-living unicellular algae into highly specialized obligate intracellular parasites, some of which are very dangerous human pathogens such as the agents of malaria and toxoplasmosis. The closest relatives of apicomplexans are dinoflagellates, which collectively exhibit a bewildering array of unusual genomic features that appear to have played a major role in the evolution of these organisms. This proposal builds on our previous work advancing on our goals through the following specific topics: 1) we are exploring the genomic architecture of the dinoflagellate model species Oxyrrhis marina, whose genome is 8 times larger than human’s. Our analysis focuses on describing and analyzing genomic elements that are hypothetically involved in the size expansion and other unusual features of these genomes. We will also use biochemical and molecular biology approaches to unravel the secrets of the unique organization of their chromosomes. 2) Our second focus is on apicomplexans. So far we have been working on elucidating the relationships among the various apicomplexans lineages in order to have a solid phylogenetic framework to explore the cellular and genomic correlates of the transition from free-living and predatory organisms to highly specialized intracellular parasites. As part of this goal, we will investigate an organism called Nephromyces, whose life cycle uniquely deviates from the standard apicomplexan lifestyle: instead of growing intracellularly, Nephromyces invades a peculiar organ in their animal host where it completes its life cycle, which includes many coexisting cell types. In stark contrast to other apicomplexans, there is no evidence that it is pathogenic for its host, and some evidence points to metabolic exchanges between host and symbiont. We expect this unique microbe will shed substantial light on the origins of parasitism and its consequences.