Eocyte hypothesis

Abstract: Recent advances in phylogenomic analyses and increased genomic sampling of uncultured prokaryotic lineages have brought compelling evidence in support of the emergence of eukaryotes from within the archaeal domain of life (eocyte hypothesis)1,2. The discovery of Asgardarchaeota and its supposed position at the base of the eukaryotic tree of life3,4 provided cues about the long-awaited identity of the eocytic lineage from which the nucleated cells (Eukaryota) emerged. While it is apparent that Asgardarchaeota encode a plethora of eukaryotic-specific proteins (the highest number identified yet in prokaryotes)5, the lack of genomic information and metabolic characterization has precluded inferences about their lifestyles and the metabolic landscape that favoured the emergence of the protoeukaryote ancestor. Here, we use advanced phylogenetic analyses for inferring the deep ancestry of eukaryotes, and genome-scale metabolic reconstructions for shedding light on the metabolic milieu of Asgardarchaeota. In doing so, we: (1) show that Heimdallarchaeia (the closest eocytic lineage to eukaryotes to date) are likely to have a microoxic niche, based on their genomic potential, with aerobic metabolic pathways that are unique among Archaea (that is, the kynurenine pathway); (2) provide evidence of mixotrophy within Asgardarchaeota; and (3) describe a previously unknown family of rhodopsins encoded within the recovered genomes. A comparative analysis of Asgard archaea genomes elucidates their metabolic potential and leads to the proposal of a revised ‘aerobic protoeukaryotes’ model for the origin of the eukaryotic cell.

Abstract: Current hypotheses about the history of cellular life are mainly based on analyses of cultivated organisms, but these represent only a small fraction of extant biodiversity. The sequencing of new environmental lineages therefore provides an opportunity to test, revise, or reject existing ideas about the tree of life and the origin of eukaryotes. According to the textbook three domains hypothesis, the eukaryotes emerge as the sister group to a monophyletic Archaea. However, recent analyses incorporating better phylogenetic models and an improved sampling of the archaeal domain have generally supported the competing eocyte hypothesis, in which core genes of eukaryotic cells originated from within the Archaea, with important implications for eukaryogenesis. Given this trend, it was surprising that a recent analysis incorporating new genomes from uncultivated Archaea recovered a strongly supported three domains tree. Here, we show that this result was due in part to the use of a poorly fitting phylogenetic model and also to the inclusion by an automated pipeline of genes of putative bacterial origin rather than nucleocytosolic versions for some of the eukaryotes analyzed. When these issues were resolved, analyses including the new archaeal lineages placed core eukaryotic genes within the Archaea. These results are consistent with a number of recent studies in which improved archaeal sampling and better phylogenetic models agree in supporting the eocyte tree over the three domains hypothesis.

Abstract: In the June 1984 issue of PNAS, James Lake and colleagues (1) published a provocative article in which they proposed that eukaryotes (animals, fungi, plants, and protists) evolved from a specific group of thermophilic prokaryotes, the “eocyte” archaebacteria (,1). Few questions capture the imagination of biologists like the origin of eukaryotic (nucleus-containing) cells such as our own, and as additional support accumulated (e.g., refs. ,2–,4) Lake's eocyte hypothesis garnered considerable attention. The idea that eukaryotes could have arisen from within an already diversified archaebacterial lineage was eventually overshadowed by Woese's (,5) “three-domains” view of life in which archaebacteria (including eocytes) represent a natural (i.e., monophyletic) group to the exclusion of eukaryotes and eubacteria (,5). In this issue of PNAS, Cox et al. (6) revisit the possibility of an archaebacterial origin for eukaryotes by using expanded molecular sequence datasets and ultra-modern phylogenetic approaches. Their analyses are a model of rigor and rekindle interesting and important ideas about the prokaryotic antecedents of eukaryotic cells.