Open Questions on the Origin of Eukaryotes

Abstract

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.

Keywords: archaea; eukaryogenesis; membrane; metabolism; origin of nucleus; symbiosis; syntrophy.

Figure 1

Schematic summary of general types of hypotheses on the phylogenetic origin of eukaryotes in the tree of life before and after the discovery of Lokiarchaeota and related deep-branching archaea. A, archaea; B, bacteria; E, eukaryotes. The schematic organelle drawing represents the mitochondrial acquisition.

Figure 2

Three hypothetical mechanisms to explain the evolution of the eukaryotic cell. Focus is made on key eukaryotic cellular structures (nucleus, mitochondria, membrane system). (A) Evolution of a proto-eukaryotic lineage before the mitochondrial acquisition event; it is compatible with the classical model proposing a third primary proto-eukaryotic lineage (Figure 1.A, B) and with models proposing that the eukaryotic host derived from within archaea (Figure 1.E). (B) Endosymbiosis of mitochondrial ancestor within one archaeon as the triggering event for eukaryogenesis (Figure 1.C, F). (C) Endosymbiotic origin of nucleus and secondary symbiosis with ancestor of mitochondria (Figure 1.D, G).