Evidence supporting a viral origin of the eukaryotic nucleus

Abstract

29The defining feature of the eukaryotic cell is the possession of a nucleus that uncouples transcription 30 from translation. This uncoupling of transcription from translation depends on a complex process 31 employing hundreds of eukaryotic specific genes acting in concert and requires the 7-32 methylguanylate (m7G) cap to prime eukaryotic mRNA for splicing, nuclear export, and cytoplasmic 33 translation. The origin of this complex system is currently a paradox since it is not found or needed 34 in prokaryotic cells which lack nuclei, yet it was apparently present and fully functional in the Last 35Eukaryotic Common Ancestor (LECA). According to the Viral Eukaryogenesis (VE) hypothesis the 36 abrupt appearance of the nucleus in the eukaryotic lineage occurred because the nucleus descends 37 from the viral factory of a DNA phage that infected the archaeal ancestor of the eukaryotes. 38 Consequently, the system for uncoupling of transcription from translation in eukaryotes is predicted 39 by the VE hypothesis to be viral in origin. In support of this hypothesis it is shown here that m7G 40 capping apparatus that primes the uncoupling of transcription from translation in eukaryotes is 41 present in viruses of the Mimiviridae but absent from bona-fide archaeal relatives of the eukaryotes 42 such as Lokiarchaeota. Furthermore, phylogenetic analysis of the m7G capping pathway indicates 43 that eukaryotic nuclei and Mimiviridae obtained this pathway from a common ancestral source that 44 predated the origin of LECA. These results support the VE hypothesis and suggest the eukaryotic 45 nucleus and the Mimiviridae descend from a common First Eukaryotic Nuclear Ancestor (FENA). 46 47 48 49 50 51 52 53 54 55 A membrane-bound nucleus defines the eukaryotic domain, and all cellular organisms without nuclei 56 are prokaryotic (Sapp 2005; Stanier and Van Niel 1962). Its presence contributes to a great divide 57 between eukaryotes and prokaryotes defined by features such as linear chromosomes, telomeres, 58 nuclear pores, the spliceosome, mitosis, meiosis, the sexual cycle, and the endoplasmic reticulum. 59 Since the nucleus separates the eukaryotic genome from the ribosomal apparatus, its presence also 60 introduces an uncoupling of transcription from translation unique to the eukaryotic domain. 61 62 Lokiarchaeota reportedly 'bridges the gap between prokaryotes and eukaryotes' and are proposed 63 to be bona-fide archaeal relative of the eukaryotes (Spang et al. 2015). Lokiarchaeota and related 64 Asgardians encode Crenactins, the ESCRT-III complex, a family of small Ras-like GTPases and a 65 ubiquitin system, making them a plausible direct descendent of an archaeal ancestor of the 66 eukaryotes (Koonin 2015). This discovery supports the Eocyte tree of life where eukaryotes evolved 67 from a specific archaeon rather than representing a sister group to the archaea (Riviera and Lake 68 1992). If Lokiarchaeota are bona-fide archaeal relatives of the eukaryotes, the last common 69 ancestor of the Asgard archaea and the eukaryotes ...

Giant viruses encode novel types of actins possibly related to the origin of eukaryotic actin: the viractins

“…Additional viractin sequences and an improved understanding of the phylogeny of eukaryotes are now needed to refine the model of evolution regarding the origin of actin. Different authors previously emphasized a possible evolutionary relationship between the eukaryotic nucleus and NCLDV viral factories 22,23 . In this context, it is interesting to note that actin is present in both the cytoplasm and nucleus of eukaryotic cells and that, in collaboration with nuclear ARPs, seems to be involved in several nuclear-related processes 24 .…”