Abstract
It is often assumed that eukarya originated from archaea. This view has been recently supported by phylogenetic analyses in which eukarya are nested within archaea. Here, I argue that these analyses are not reliable, and I critically discuss archaeal ancestor scenarios, as well as fusion scenarios for the origin of eukaryotes. Based on recognized evolutionary trends toward reduction in archaea and toward complexity in eukarya, I suggest that their last common ancestor was more complex than modern archaea but simpler than modern eukaryotes (the bug in-between scenario). I propose that the ancestors of archaea (and bacteria) escaped protoeukaryotic predators by invading high temperature biotopes, triggering their reductive evolution toward the “prokaryotic” phenotype (the thermoreduction hypothesis). Intriguingly, whereas archaea and eukarya share many basic features at the molecular level, the archaeal mobilome resembles more the bacterial than the eukaryotic one. I suggest that selection of different parts of the ancestral virosphere at the onset of the three domains played a critical role in shaping their respective biology. Eukarya probably evolved toward complexity with the help of retroviruses and large DNA viruses, whereas similar selection pressure (thermoreduction) could explain why the archaeal and bacterial mobilomes somehow resemble each other.
Highlights
Archaea have been confused with bacteria, under the term prokaryotes, until their originality was recognized by 16S rRNA cataloguing [1]
Fusion scenarios posit a transient but extreme acceleration of protein evolutionary rates and drastic structural changes to take into account the existence of eukaryotic specific versions of universal proteins and the rapid emergence of all eukaryote-specific features (ESFs) in the period between the fusion event and LECA. They should posit a transient but extreme acceleration of evolution of viral structures and the appearance of many new viral and transposon families in that same period. This does not seem reasonable, even more so if the fusion event is assimilated to the endosymbiosis that produced mitochondria [49], since in that case, all these dramatic evolutionary changes should have occurred between the appearance of the first mitochondrial eukaryote (FME) and LECA! Such scenarios require no less than several miracles for the emergence of eukaryotes, miracles that occurred only once in 2-3 billion years of coexistence between archaea and bacteria
The Scenario I favoured in this paper for the origin and evolution of archaea is at odds with the traditional view that “prokaryotes” gave rise to “eukaryotes”
Summary
Archaea have been confused with bacteria, under the term prokaryotes, until their originality was recognized by 16S rRNA cataloguing [1]. It is often assumed that archaea resemble eukarya when their informational systems (DNA replication, transcription, and translation) are considered but resemble bacteria in terms of their operational systems This is clearly not the case, since many archaeal operational systems (such as ATP production, protein secretion, cell division and vesicles formation, and protein modification machinery) use proteins that have only eukaryotic homologues or that are more similar to their eukaryotic rather than to their bacterial homologues [7,8,9,10,11,12,13,14]. This indicates that these traits have not been sporadically acquired from eukarya by lateral gene transfer but were lost in most members of the archaeal domain after their divergence from LACA [6] Considering this loss of eukaryotic traits and the gain of bacterial traits by LGT, LACA was probably even more “eukaryotic-like” than modern archaea. This is probably because, as recently stated by Koonin and Wolf, “viruses are no part of the traditional narrative of evolutionary biology” [23]
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