In collaboration with various research groups (in the US, in Sweden and in France), we have obtained sediment samples from diverse regions all around the world. We extracted and sequenced DNA from these sediments, and, using sophisticated bioinformatics approaches (“binning”), we sorted and assembled those sequences in order to reconstruct the genomes of organisms present in those samples.
Using this approach, we were able to obtain various genome sequences from uncultivated and unknonwn members of the Archaea. In particular, I have participated in the genome reconstruction and functional annotation of 69 new genomes belonging to the Asgard superphylum. A major focus of my work was then to analyze those genomes using phylogenetics and comparative genomics to (1) make inferences about the biology and metabolism of the corresponding uncultured organisms; (2) reconstruct the evolutionary relationship among those organisms, (3) pinpoint the phylogenetic placement of eukaryotes relative to those archaea; and 4) investigate the presence and evolution of ESPs in these new lineages.
MAIN RESULTS AND DISSEMINATION
1) Reassessing research priorities in the field of eukaryogenesis
We aimed to provide a historical assessment of our understanding of the tree of Life. We examined how the recent discovery of many diverse archaeal lineages has changed our understanding of the origin of eukaryotes.
Eme L, et al. Archaea and the origins of eukaryotes.
Nature Reviews in Microbiology. 15 (2017): nrmicro-2017.
2) Metabolism of Asgard archaea
We analyzed 10 Asgard genomes in order to infer the functional potential of these novel archaea. This work allowed us not only to make predictions on the metabolism of extent Asgard archaea, but also to infer the metabolic potential of the Asgard ancestor of eukaryotes, and to propose a new scenario explaining the origin of the eukaryotic cell.
Spang A, et al. "Proposal of the reverse flow model for the origin of the eukaryotic cell based on comparative analysis of Asgard archaeal metabolism".
Nature Microbiology. In press.
In parallel, our genomic investigation of more recently sequenced genomes isolated from hydrothermal deep-sea sediment allowed us to reveal the existence of a new Asgard phylum, Helarchaeota, which has the potential to metabolize hydrothermally generated hydrocarbons, a unique type of metabolism not found in any other Asgard archaea.
Seitz KW, Dombrowski N, Eme L, et al. New Asgard archaea capable of anaerobic hydrocarbon cycling.
Nature Communications. In press.
3) Investigating the phylogenetic position of eukaryotes in the tree of Life
In addition, we have used extensive and careful phylogenomic approaches to place the novel archaeal genomes in an updated tree of life and determine their relationship to eukaryotes. Our analyses show that we have uncovered 6 entirely new phyla of Asgard archaea. We have confirmed that eukaryotes originated from within the Asgard superphylum and our most recent work suggests that we have identified a novel lineage that is possibly more closely related to Eukaryotes that any other described lineage, although this remains to be confirmed (Fig. 1).
Spang A, Eme L, et al. Asgard archaea are the closest prokaryotic relatives of eukaryotes.
PLoS Genetics. 14 (3), e1007080.
4) Elucidating the origin of eukaryotic cell complexity
In addition to grouping together with eukaryotes in phylogenetic analyses, Asgard archaea encode a large number of genes that were until recently thought to be unique to eukaryotes, and that are involved in various complex cellular features in eukaryotes (ESPs) (Fig 2.). Notably, our investigations of the novel genomes revealed the presence of many genes that were previously thought to only exist in eukaryotes and, which, in eukaryotes, are involved in various aspects of the subcellular compartment (endomembrane) system (Eme et al, in prep). Our results thus further enlighten us on the order of emergence of the key features of the eukaryotic cell, and on how those have evolved among the various Asgard lineages, making this work of major importance for our understanding of the establishment of complex life forms on Earth.
Eme L, Ettema TJG. Cellular evolution: The first eukaryote shapes us. News & Views.
Nature. 2018 Oct;562(7727):352.
Over the two years of the project, I have had the opportunity to present this work at several international conferences, including 3 where I was an invited speaker (Royal Society meeting, UK; EMBO meeting, Spain; Gordon Research Conference Archaea, US) and one which I was co-organizing (Symbiosis in the microbial world, UK).
