A symbiogenic merger enabled by oxygen initiated the evolution of eukaryotes

Recently, extensive genetic information about archaeal hosts at the basis of eukaryogenesis has come to light. Characterization of these first eukaryotic common ancestor (FECA) related organisms allows improved understanding of the enigmatic FECA to last eukaryotic common ancestor (LECA) transition. However, these gene-centered discoveries have the unfortunate side effect of entrenching erroneous ideas about early eukaryotic evolution. This is apparent in the two-Domain vision of life, with eukaryotes seen as specialized Asgard archaea, while underestimating the contribution of the endosymbiont to eukaryogenesis. Establishment of the alpha-proteobacterium as the future mitochondrion is treated as one of many such endosymbiotic occurrences, ignoring its unique evolutionary position. I will marshal evidence for symbiogenic mechanisms involved in the FECA to LECA transition, with a key role for the endosymbiont’s electron transport chain and its acceptor molecular oxygen, especially in the incarnation of reactive oxygen species occurring in the host cytoplasm. We should overcome overestimating gene determinism, while not sufficiently allowing for effects of biological hierarchies, emergent properties, and chance. Many eukaryotic properties are best understood by envisaging the crucial uptake of the future mitochondrion as a merger instead of an acquisition. This merger is characterized by a new kind of elaborate cellular entity emerging as a result of rapid coevolution, replacing a scenario in which already complex pre-eukaryotes acquired endosymbionts, accompanied by important, but limited, changes. Successful mergers are rare because they are intrinsically more difficult, but synergistically open up completely new areas of possibilities, as illustrated by incredible eukaryotic success.