Review
Open Questions on the Origin of Eukaryotes

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Trends

Eukaryotes arose from the endosymbiosis of an alphaproteobacterium in an unknown host. Eukaryogenic models diverge in the hypothetical host proposed.

Recent phylogenomic analyses and the discovery of archaea with seemingly more eukaryotic-like genes suggest that the mitochondrial host was an archaeon or had a vital archaeal contribution, excluding a third hypothetical proto-eukaryotic lineage different from archaea.

As the phylogenetic origin of eukaryotes gets clearer, mechanistic questions remain open: the type of metabolic symbioses involved, the timing of mitochondrial acquisition and, most importantly, the origin of the eukaryotic nucleus and bacterial-like membranes.

Plausible driving forces and processes for the evolution of the eukaryotic nucleus are missing.

If the mitochondrial host was an archaeon, a difficult-to-explain archaeal-to-bacterial membrane transition is required.

Despite recent progress, the origin of the eukaryotic cell remains enigmatic. It is now known that the last eukaryotic common ancestor was complex and that endosymbiosis played a crucial role in eukaryogenesis at least via the acquisition of the alphaproteobacterial ancestor of mitochondria. However, the nature of the mitochondrial host is controversial, although the recent discovery of an archaeal lineage phylogenetically close to eukaryotes reinforces models proposing archaea-derived hosts. We argue that, in addition to improved phylogenomic analyses with more comprehensive taxon sampling to pinpoint the closest prokaryotic relatives of eukaryotes, determining plausible mechanisms and selective forces at the origin of key eukaryotic features, such as the nucleus or the bacterial-like eukaryotic membrane system, is essential to constrain existing models.

Section snippets

A Long-Lasting Query

The origin of the eukaryotic cell was a major evolutionary event that led to a wide diversification of lineages displaying very different morphologies, several of which independently evolved towards multicellularity [1]. Compared to the average prokaryotic cell, the average early eukaryotic cell represented a considerable increase in structural complexity, typified by the presence of an endomembrane system delimiting a hallmark eukaryotic feature, the nucleus, and membrane-bound organelles,

Mechanistic Types of Eukaryogenesis Models

Many different hypotheses for the origin of eukaryotes have been proposed (reviewed in 5, 6, 7, 8). We briefly highlight mechanisms proposed by the two main general types of eukaryogenesis models. Many models exclusively focus on the phylogenetic ancestry of eukaryotes, looking for their closest prokaryotic relatives, or on particular mechanistic details, but only a few models provide combined phylogenetic and mechanistic frameworks.

Open Questions on the Origin of Eukaryotes

Details about the more specific nature of the symbiotic partners that originated eukaryotes remain to be specified. Which are the closest living archaeal relatives of eukaryotes? Many deep-branching archaeal lineages other than the Lokiarchaeota exist that might contain more eukaryotic-like genes [9]. What are these archaea like? Do they have eukaryotic-like features (actin cytoskeleton, vesicular-trafficking and membrane-remodeling capabilities, endocytosis and/or phagocytosis), as their

What Type of Metabolic Symbiosis Existed between Eukaryogenic Partners?

Regardless the type of eukaryogenic model considered (Figure 2), metabolic interspecies interactions must have been fundamental for the evolution of the eukaryotic cell. These are widespread in nature, and are particularly extended in anoxic environments where specialized microorganisms are most often the source and/or sink of electron donors and acceptors 43, 44. Because mitochondria are still responsible for the essential of eukaryotic cell energetics, some type of syntrophic relationship

Mitochondria: Early or Late?

Before the discovery of the Lokiarchaeota, symbiogenetic models proposing a direct endosymbiosis of the mitochondrial ancestor within one archaeon had gained popularity 24, 26, 50 (Figure 2B). They imply a triggering effect of eukaryogenesis for mitochondrial endosymbiosis. However, the fact that the newly discovered archaea possess several homologs to membrane remodeling and cytoskeleton-related eukaryotic proteins has opened the possibility for a proto-eukaryotic lineage endowed with

What Selective Forces Drove the Evolution of the Nucleus?

The origin of the nucleus remains mysterious. While it was present in LECA, and evolved as part of the endomembrane system involving many protein components of archaeal and bacterial ancestry [52], most models do not provide any (or any convincing) selective force for the evolution of this defining character. Two driving forces have been evoked by autogenous models. Cavalier-Smith proposed that the nucleus evolved to prevent DNA damage caused by cytoskeletal pulling [53], an idea adopted by

How Did The Bacterial-Like Eukaryotic Membranes Evolve?

Archaeal membranes are radically different from bacterial and eukaryotic membranes, having phospholipids of different composition and stereochemistry [57]. If currently favored models based on an archaea-derived host are correct, they entail a transition from archaeal to bacterial membranes (Figure 2A,B). However, this poses two challenges. First, the plasma membrane is not only a lipid bilayer but a dynamic cell–environment interface, and thus the driving force leading to such transition from

Concluding Remarks

The long-inscrutable quest for the origin of the eukaryotic cell has become increasingly tractable with recent progress in genome sequencing, phylogenomic analyses, and the exploration of microbial diversity in natural ecosystems. The discovery of new lineages of uncultured archaea in anoxic sediments that appear to be more related to eukaryotes than other archaea constrains existing models for the origin of eukaryotes. However, if the prokaryotic ancestry of eukaryotes begins to be refined,

Acknowledgments

We apologize for not being able to cite the work of many authors owing to space limitations. We acknowledge funding from the European Research Council (ERC) under the European Commission 7th Framework Program ERC Grant Agreement 322669 ‘ProtistWorld’.

Glossary

Alphaproteobacteria
highly diversified and metabolically versatile class of bacteria within the phylum Proteobacteria from which the ancestor of mitochondria evolved.
Archaea
one of the three classically recognized domains of life and one of the two primary phylogenetic domains. Archaea exhibit prokaryotic cell structure. They are traditionally divided into two main branches, the Euryarchaeota and the TACK (Thaumarchaeota, Aigarchaeota, Crenarchaeota, Korarchaeota) superphylum or Proteoarchaeota.

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