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Deep eukaryotic phylogenomics : the holomycota branch

Abstract : Despite the astonishing diversity of plants, animals and macroscopic fungi, most eukaryotic diversity is actually microbial. The eukaryotic tree comprises several large monophyletic supergroups. One of these groups is the Opisthokonta, which encompasses two branches, Holozoa, including animals, and Holomycota, grouping Fungi and their unicellular relatives. While multicellular fungi are well known, knowledge on the diversity of unicellular Fungi and their phylogenetic relatives is still poor. This unicellular fraction includes several zoosporic lineages (e.g. Chytridiomycota and Blastocladiomycota) within Fungi, but also a variety of lineages related to the classical core Fungi: nucleariids, rozellids, aphelids and Microsporidia. However, the phylogenetic relationships of these lineages among them and with classical Fungi remain to be solidly established. Molecular phylogenetic trees of 18S rRNA genes retrieved from environmental studies have showed a wide diversity of unicellular holomycotans in almost all environments on Earth. However, the phylogenetic signal of this gene is limited and does not allow robustly resolving most deep phylogenetic relationships. During past years, high-throughput techniques have allowed sequencing hundreds of new genomes and transcriptomes. This has made possible to carry out multi-gene phylogenomic studies, which increase the available signal to resolve evolutionary relationships. Nevertheless, most sequenced genomes correspond to easy-to-culture fungal species, often with particular interest for humans (e.g. parasites, plant symbionts, yeast). Recently, single-cell omics has become a potential useful approach to study uncultured unicellular eukaryotes, making it possible to reconstruct robust phylogenetic analyses of a wide environmental diversity using genomic and transcriptomic data. During my PhD work, I have applied single-cell techniques to get phylogenetic information from divergent holomycotan lineages, clarify phylogenetic relationships among fungi and their close relatives and infer trait evolution. More specifically, I have used this approach to: 1) Generate genomic and transcriptomic data for nucleariids and better reconstruct inner relationships in the clade and the characters present in the nucleariid ancestor. Our results confirm that the cover-bearing unicellular genera Pompholyxophrys and Lithocolla are indeed nucleariids and branch together with Nuclearia, Parvularia and Fonticula. The reconstruction of a robust phylogeny for the group allowed us to infer the traits (e.g. no flagellum, glycocalyx, no cover) already present in their ancestor. 2) Sequence and comparatively analyze the genome of Metchnikovella incurvata, to confirm its relatively basal position within Microsporidia, and determine synapomorphies for the clade. Phylogenomic analysis of the metchnikovellid Metchnikovella incurvata confirmed that Metchnikovellidae branch at the base of Core-Microsporidia. We also confirmed their metabolic profile to be more similar to Core-microsporidia, being both similarly reduced in genes/functions. 3) Generate genomic data for Amoeboradix gromovi and Sanchytrium tribonematis, which form the newly described zoosporic fungal clade of sanchytrids, and resolve their phylogenetic position. The study of the two sanchytrid genomes clarified their placement within Fungi as a new clade sister to Blastocladiomycota. Comparative genomics showed that their metabolic composition was reduced in comparison with related lineages. This reduction was especially important in their flagellar toolkit when compared with other Holomycota, confirming 4 independent flagellum loss events in the clade.
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Luis Javier Galindo González. Deep eukaryotic phylogenomics : the holomycota branch. Populations and Evolution [q-bio.PE]. Université Paris-Saclay, 2020. English. ⟨NNT : 2020UPASS050⟩. ⟨tel-02900640⟩

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