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Report

Teaser, summary, work performed and final results

Periodic Reporting for period 1 - Gap2bridge (Bridging the gap: an evolutionary genomics approach to illuminate the prokaryote-to-eukaryote transition.)

Teaser

Summary

CONTEXT AND OVERALL OBJECTIVES OF THE PROJECT

Eukarya â€“ one of the three Domains of Life along with Archaea and Bacteria (i.e. prokaryotes) â€“ include all complex multicellular life forms, as well as a colossal diversity of unicellular microorganisms. At the cellular level, the gap between prokaryotes and eukaryotes is immense, with the latter cell types displaying a large number of complex subcellular organelles and molecular systems. The evolutionary origin of these unique features, and thus of the eukaryotic cell itself, remains one of the most fascinating enigmas in modern biology. In particular, the evolutionary origin of the building blocks of eukaryotic cellular complexity (eukaryotic-signature proteins or ESPs) remain unclear.

The major goal of this project was to illuminate the prokaryote to eukaryote transition by elucidating the origin and subsequent evolution of ESPs, as well as their order of emergence. In particular, we aimed to focus on the ESPs of archaeal origin with an emphasis on the specific contribution of the Asgard archaea to the origin of the eukaryotic cell. Indeed it is now thought that this recently described group of archaea represents the closest relatives of eukaryotes (Spang et al, 2015, Zaremba et al. 2017). In addition, we aimed to determine the placement the eukaryote lineage within the tree of Life. Finally, we aimed to infer the gene content and characteristics of the archaeal ancestors of eukaryotes.

Work performed

\"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 (â€œbinningâ€), 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 k\"

Final results

Beyond gaining scientific expertise in a new field for me, this project has allowed me to develop the leadership, mentoring, and communication skills that are essential for success as an independent researcher. Notably, the multidisciplinary nature of the project has helped me gain both independence and project management skills. In fact, those were recognized through the recent award of an ERC Starting Grant that will allow me to establish myself in France as an independent researcher. In additionn, the benefits of my stay at Uppsala University will extend beyond the period of the Marie Curie itself since I will continue to collaborate with Dr. Ettema (now established in the Netherlands), which will strengthen collaborative research within the EU. This is particularly important since environmental microbiology research has been predominant in the US and our work will continue to reinforce European competitiveness in this field. Beyond the direct contributions to the scientific goals of the European Union, this project has helped making Europe a centre of excellence for research in evolutionary molecular biology, and thus an attractive destination for researchers worldwide.