From archaeon to eukaryote: the evolutionary dark ages of the eukaryotic cell

Abstract

The evolutionary origin of the eukaryotic cell represents an enigmatic, yet largely incomplete, puzzle. Several mutually incompatible scenarios have been proposed to explain how the eukaryotic domain of life could have emerged. To date, convincing evidence for these scenarios in the form of intermediate stages of the proposed eukaryogenesis trajectories is lacking, presenting the emergence of the complex features of the eukaryotic cell as an evolutionary deus ex machina. However, recent advances in the field of phylogenomics have started to lend support for a model that places a cellular fusion event at the basis of the origin of eukaryotes (symbiogenesis), involving the merger of an as yet unknown archaeal lineage that most probably belongs to the recently proposed 'TACK superphylum' (comprising Thaumarchaeota, Aigarchaeota, Crenarchaeota and Korarchaeota) with an alphaproteobacterium (the protomitochondrion). Interestingly, an increasing number of so-called ESPs (eukaryotic signature proteins) is being discovered in recently sequenced archaeal genomes, indicating that the archaeal ancestor of the eukaryotic cell might have been more eukaryotic in nature than presumed previously, and might, for example, have comprised primitive phagocytotic capabilities. In the present paper, we review the evolutionary transition from archaeon to eukaryote, and propose a new model for the emergence of the eukaryotic cell, the 'PhAT (phagocytosing archaeon theory)', which explains the emergence of the cellular and genomic features of eukaryotes in the light of a transiently complex phagocytosing archaeon.

The role of archaea in the origin of eukaryotes

“…Открытым для размышлений в этой гипотезе осталось предположение о фагоцитар-ном механизме приобретения эндосимбионтов. У прока-риот отсутствует способность к фагоцитозу, и предполо-жения о возможности использования такого механизма в эукариогенезе недостаточно убедительны [54,55]. По другой гипотезе [56], получившей название «во-дородной» и поддержанной многими исследователя-ми, LECA образовался в результате синтрофного эн-досимбиотического процесса, где клеткой-хозяином была архея.…”

Eukaryogenesis, how special really?

“…Coincidentally, there is mounting evidence supporting something like James Lake's long discounted "eocyte hypothesis," in which the eukaryotic nucleocytoplasmic lineage emerged from within or near the Crenarchaeota rather than before any divergence within what we call Archaea (23). If this hypothesis holds up, then we might expect to find closer and closer homologs of components of the several eukaryotespecific cellular machineries [now called eukaryotic signature proteins (24)] as we explore inferred proteomes of such archaea [the group of phyla comprising Thaumarchaeota, Aigarchaeota, Crenarchaeota, and Korarchaeota (TACK)].…”

“…Phagotrophic predation as an early eukaryotic or late archaeal invention [by Martijn and Ettema's phAT (24), or earlier such schemes] has several entailments, which might be taken as defining eukaryotic features. The need to maintain genes enabling the use of a variety of substrates and oxidants is reduced when metabolites are present in prey.…”

Eukaryotes first: how could that be?

“…Ettema and co-workers [13,32] would be in the former camp. Their 'phagocytosing archaean theory' (PhAT), seemingly now well supported by the discovery of the Lokiarchaeota [13] is of the former type, and envisions that an archaean of the TACK superphylum lost its cell wall, 'allowing for the evolution of a more flexible actin-based cytoskeleton', this 'matured into a primitive phagocytosis machinery' which encouraged 'rampant' LGT, to protect against which 'a protective membrane [was] formed via invagination events, giving rise to a primitive karyotic cell type' [32].…”

“…Such streamlining meant to Forterre that prokaryotes, though simpler than eukaryotes, are more highly evolved: the 'pro' in prokaryotes is a misnomer. In a recent and more richly elaborated formulation of this hypothesis [31], Forterre accepts the 'classical' rooted three-domain tree in which Archaea and Eukarya are sisters, and takes on board the findings of homologues of several ESPs in one or another newly discovered archaeal lineage [32,33]. He proposes that the last archael/eukaryal common ancestor (LAECA) was more complex than any contemporary archaeon and that Archaea, independently from Bacteria, underwent 'thermoreduction'.…”