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Protist evolution in suboxic worlds

Final Report Summary - PROTISTWORLD (Protist evolution in suboxic worlds)

Elusive for a long time, the origin of eukaryotes begins to be progressively solved. In recent years, it has become clear that eukaryotes resulted from the symbiosis, likely in oxygen-poor environments, of bacteria and archaea, whose ancestors are beginning to be portrayed. However, many open questions remain and the details of the eukaryogenetic process need to be elucidated. What made the eukaryogenetic symbiosis stabilize and result in new organisms with an increased level of complexity? Part of the answer may lie in the early evolutionary history of eukaryotes and in the endosymbiotic interactions that they establish with prokaryotes in oxygen-poor habitats. In addition to well-known animals, plants or fungi, eukaryotes comprise an extraordinary diversity of unicellular organisms (protists). If the use of increasingly powerful molecular tools has revealed that the extent of protist diversity is far larger than ever suspected in relatively well studied systems such as ocean plankton, less-explored ecosystems likely harbor a wealth of unstudied divergent eukaryotic lineages. Studying the genes and genomes of novel divergent lineages is essential to determine the relative order of divergence of major eukaryotic lineages, unraveling their evolutionary history and inferring the nature of the last common eukaryotic ancestor.
In ProtistWorld, we have applied interdisciplinary approaches to fill gaps in knowledge about the diversity and genomics of microbial eukaryotes in oxygen-poor environments and gain information about i) the real extent of protist diversity, identifying potential novel divergent lineages; ii) fossilization of microbial eukaryotes for potential biosignature dating ; iii) eukaryotic phylogenomics and improved reconstruction of the eukaryotic tree; and iv) the molecular bases of protist (endo)symbiosis. Our project has led to the characterization of microbial communities in many poorly studied ecosystems, including suboxic freshwater systems, microbial mats or extreme environments. Our results show a wide eukaryotic diversity in suboxic freshwater systems, including many divergent lineages related to fungi (aphelids, rozellids) or more deeply branching (e.g. apusomonads) and clades previously thought to be exclusively marine. Combining culture and single-cell approaches, we generated genomes and transcriptomes for several divergent protist lineages, including the aphelids and the hyperparasitic metchnikovellids. The phylogenomic and metabolic gene content of the first near full cell-cycle transcriptome of aphelids showed that they form the closest relatives to fungi and suggest that fungi originated from free-living (and not parasitic as some authors proposed) phagotrophic ancestors. We also studied microbial mats and microbialites (biomineralizing mats) from various locations as potential analogs of past ecosystems and to study biosignature preservation. The studied microbial mats were extremely diverse, including divergent prokaryotic and, in lesser extent, eukaryotic, lineages. We postulated that functional shifts in microbial mat metagenomes along redox gradients recapitulate early metabolic transitions in the early Earth. Applying such a space-for-time substitution approach to core metabolic genes in metagenomes suggests that anoxygenic photosynthesis largely expanded in parallel to oxygenic photosynthesis in the early Earth and that Wood-Ljungdahl was the most extended carbon fixation pathway in Precambrian ecosystems. Metagenomic analysis of living microbialites in Mexican lakes suggested that, in addition to cyanobacteria and anoxygenic photosynthesizers, photosynthetic protists contribute to the carbonate precipitation potential. Through interdisciplinary collaboration, we identified exquisitely preserved microbial cells down to the nm-scale thanks to permineralization with a newly identified poorly-crystalline hydrated silicate phase. These microbialites were also the original source of a new cyanobacterium forming intracellular carbonates that represents a novel deep-branching order of cyanobacteria (Gloeomargaritales). Phylogenomic analyses showed that this cyanobacterial order is the closest-known lineage to the chloroplast of photosynthetic eukaryotes, allowing us to formulate hypotheses about the basis and early evolution of eukaryotic photosynthesis. We obtained extensive information about inter-domain horizontal and endosymbiotic gene transfer. This, theoretical considerations on eukaryogenesis and a better understanding of microbial mat ecology led us to revise our Syntrophy hypothesis and discuss existing models for the origin of eukaryotes.