Hindawi Publishing Corporation Archaea Volume 2013, Article ID 372396, 18 pages http://dx.doi.org/10.1155/2013/372396 Review Article The Common Ancestor of Archaea and Eukarya Was Not an Archaeon Patrick Forterre1,2 1 Institut Pasteur, 25 rue du Docteur Roux, 75015 Paris, France 2 Universite´ Paris-Sud, Institut de Gen´ etique´ et Microbiologie, CNRS UMR 8621, 91405 Orsay Cedex, France Correspondence should be addressed to Patrick Forterre; [email protected] Received 22 July 2013; Accepted 24 September 2013 Academic Editor: Gustavo Caetano-Anolles´ Copyright © 2013 Patrick Forterre. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. 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. 1. Introduction their bacterial homologues [7–14]. The bacterial-like fea- tures of some archaeal metabolic pathways could be mostly Archaea have been confused with bacteria, under the term due to lateral gene transfer (LGT) of bacterial genes into prokaryotes, until their originality was finally recognized by Archaea, driven by their cohabitation in various biotopes 16S rRNA cataloguing [1]. Archaea were previously “hidden [15]. Indeed, beside bacterial-like genes possibly recruited by before our eyes”, strikingly resembling bacteria under the LGT, metabolic pathways in archaea—such as the coenzyme light and electron microscopes. Archaea and bacteria are A or the isoprenoid biosynthetic pathways—also involve also quite similar at the genomic level, with small circu- a mixture of archaea-specific and eukaryotic-like enzymes lar genomes, compact gene organization, and functionally [16–18]. Archaea and eukarya share so many features in related genes organized into operons. At the same time, allaspectsoftheircellularphysiologyandmolecularfabric archaea, unlike bacteria, exhibit a lot of “eukaryotic features” that eukaryotes cannot be simply envisioned as a mosaic of at the molecular level [2–6]. It is often assumed that archaea archaeal and bacterial features. Archaea and eukarya clearly resemble eukarya when their informational systems (DNA share a more complex evolutionary relationship that remains replication, transcription, and translation) are considered but to be understood. resemble bacteria in terms of their operational systems. This Whereas many eukaryotic traits of archaea are ubiquitous is clearly not the case, since many archaeal operational sys- or widely distributed in that domain, recent discoveries tems (such as ATP production, protein secretion, cell division have identified several new eukaryotic traits that are only and vesicles formation, and protein modification machinery) present in one phylum, one order, or even in one species alsouseproteinsthathaveonlyeukaryotichomologuesor of archaea [6, 11, 14]. Phylogenetic analyses suggest that that are more similar to their eukaryotic rather than to these traits were already present in the last archaeal common 2 Archaea ancestor (LACA) since, in most cases, archaeal and eukaryal 2. The Bacterial Flavour of Archaeal Viruses sequences form two well separated monophyletic groups and Plasmids: Another Evolutionary Puzzle [12, 13, 19]. This indicates that these traits have not been sporadically acquired from eukarya by lateral gene transfer Virusesinfectingarchaeahavefascinatedforalongtime but were lost in most members of the archaeal domain after scientists that are aware of their existence by the amazing their divergence from LACA [6]. Considering this loss of morphologies of their virions that, in most cases, differ eukaryotic traits and the gain of bacterial traits by LGT,LACA drastically from those produced by bacterioviruses (formerly was probably even more “eukaryotic-like” than modern bacteriophages) or eukaryoviruses [24, 25]. Among the 13–15 archaea. However, despite their eukaryotic affinity, archaea families of archeoviruses presently known, most are unique to lack many eukaryote-specific features (ESFs) at the cellular archaea, and none of them is specifically related to a family of and/or molecular levels. These, for example, include the eukaryoviruses. The only archaeal viruses with eukaryovirus spliceosome, mRNA capping, and extensive polyadenylation relatives are the archeoviruses STIV (Sulfolobus islandicus as well as huge transcriptional machineries with unique turreted virus) (see below) and Caudovirales, which belong components, such as the mediator, endoplasmic reticulum, to major lineages of viruses infecting members from the three and derived structures such as lysosomes, the Golgi appara- cellular domains [26]. STIV is the archaeal member of the tus and the nuclear membrane, an elaborated cytoskeleton PRD1/adenovirus lineage that groups bacterial Tectiviridae andassociatedvesicletraffickingsystemwithendosomes (a group of small membrane-containing viruses resembling and ectosomes, nuclear pores, nucleolus and other nucleus- STIV) with large DNA viruses infecting eukaryotes, such specific structures, linear chromosomes with centromeres as adenoviruses and Megavirales (formerly nucleocytoplas- and telomeres, mitosis and associated chromosome segrega- miclargeDNAviruses,NCLDV)aswellastherecently tion system linked to the cytoskeleton, complex and great sex discovered satellite viruses (virophages) of giant Megavi- with meiosis derived from mitosis, an incredible machinery rales. Viruses of this lineage are characterized by major for cell division apparatus with synaptonemal complex for capsid proteins containing the so-called double jelly-roll meiosis, centrioles and midbodies for cell division, and I fold. Archaeal and bacterial Caudovirales (head and tailed probably miss some of them. Archaea not only lack all viruses) belong to the same viral lineage as eukaryoviruses these ESFs but also lack homologues of most proteins (a of the family Herpesviridae. Their virions are constructed few hundreds) that are involved in building and operating from the major capsid proteins displaying the so-called them [20]. This remains true even if a few ex-ESPs (e.g., Hong-Kong 97 fold (structurally unrelated to the jelly-roll actin, tubulin, and DNA topoisomerase IB) have recently lost fold). Strikingly, the archaeal viruses in these two lineages thisstatusfollowingthediscoveryofarchaealhomologues are much more similar in virion size and overall structure [12, 13, 19]. The number, diversity, and complexity of ESFs to their bacterial than to their eukaryotic counterparts. In areimpressiveandtheiroriginremainsamajorevolutionary particular, archaeal and bacterial Caudovirales are identical puzzle that should not be underestimated. The puzzle became in terms of virion morphology and genome organization and of even greater magnitude when it was realized during share several homologous proteins [27]. The three families the last decade from phylogenomic analyses that all ESFs of Caudovirales (Siphoviridae, Myoviridae, and Podoviridae) (and associated ESPs) were most likely already present in first described in bacteria have been now found in archaea the last common ancestor of all modern eukaryotes, (the [25, 27, 28]. Moreover, Caudovirales were recently found to last eukaryotic common ancestor)(LECA)[20]. In a recent be more widespread than previously thought among archaea, review, Martijn and Ettema called the period that experienced suggesting that Caudovirales already existed when archaea the emergence of ESFs (so before LECA): “the evolutionary and bacteria started to diverge from each other [29]. Finally, dark ages of eukaryotic cells”[21]. This denomination well a recently described family of archaeal pleomorphic viruses, illustrates the complexity of the “complexity problem” in pleolipoviruses, could be related to bacterial pleomorphic eukaryotic evolution. viruses of the family Plasmaviridae [30]. In summary, Besides lacking (by definition) all ESFs, archaea also whereas archaea and eukarya share basic molecular biology fundamentally differ from eukarya in the nature of their features for all major ancestral cellular functions, the archaeal membranes (with a unique type of lipids in archaea), and the virosphere shares