Sex and the eukaryotic cell cycle is consistent with a viral ancestry for the eukaryotic nucleus
Introduction
The homology between ribosomal RNA sequences of all known cellular organisms supports the premise that all life on earth descends from a common ancestor through the process of evolution. Thus despite several fundamental differences in genetic design, the relatively complex members of the eukaryotic domain, including humans, appear to share a common ancestor with the relatively simple members of the bacterial and archaeal domains. Currently, the nature of the proposed last universal common ancestor of life (LUCA) is unclear, reflecting the fact that many of the details of the early evolution of life are unknown. Theories on early life range from the progenote hypothesis (Woese and Fox, 1977) in which LUCA was a communal consortium of �pre-cells’ to hypotheses in which LUCA was a cellular organism of either eukaryotic cellular design (e.g., Forterre and Philippe, 1999; Penny and Poole, 1999) or prokaryotic cellular design (Gogarten et al., 1989; Iwabe et al., 1989).
How the eukaryotes arose is also currently unclear and the subject of much scientific debate (reviewed in Embley and Martin, 2006). According to one school of thought, the first bifurcation in the tree of life divided the bacterial and archaeal domains, and the eukaryotes somehow evolved from a prokaryotic world. This �prokaryote first’ model for the early evolution of life, in which simple life forms predate more complex life forms, is supported by both the fossil record (Schopf, 1993) and some molecular evidence (Kyrpides et al., 1999). The observation that the eukaryotic genome is apparently a chimera composed of bacterial and archeal genes (Rivera et al., 1998) has lent support to several proposals in which both archaeal and bacterial cells were directly involved in the evolution of the earliest eukaryotes (e.g., Lake and Rivera, 1994; Martin and Muller, 1998; Moreira and Lopez-Garcia, 1998).
If the eukaryotes descend from a prokaryotic ancestor or ancestors, how did the eukaryotes and their unique cell cycle arise? The universality of mitosis, and the observation that sex and meiosis are widely distributed amongst the major phylogenetic groupings of eukaryotes (Adl et al., 2005) suggest that the origin of eukaryotic cell cycle is integrally related to the origin of the eukaryotes themselves (e.g., Ramesh et al., 2005, Cavalier-Smith, 2002). Although many previous models have focussed on mathematical approaches to understanding the forces that drove the evolution of a sexual cycle and the advantages it confers on the eukaryotes (e.g., Novak et al., 1998), relatively few mechanistic models for the physical origin of the complex eukaryotic cell cycle have been proposed. One of the few models to address the origin of the cell cycle is the model proposed by Cavalier-Smith (2002) in which eukaryotes arose from a �Neomuran revolution’ some 850 million years ago. In this model, the eukaryotes arose as a result of this �revolution’, and one of the key innovations responsible for sex was the evolution of cohesins to allow the development of the two-step meiotic division.
In the paper presented here, the viral eukaryogenesis (VE) hypothesis (Bell, 2001, Bell, 2004) is extended to provide a model for the origin of the complex eukaryotic cell cycle. As previously described in the VE hypothesis it is postulated that the eukaryotic cell is a consortium derived from a lysogenic virus, an archaeon and a bacterium (Bell, 2001, Bell, 2004). In the model, a lysogenic pox-like virus evolved into the eukaryotic nucleus by acquiring genes from both the archaeon and the bacterium and taking over the role of information storage for the consortium. The archaeal host retained its function of gene translation and general metabolism but transferred its functional genome to the viral genome in the process of evolving into the cytoplasm. The bacterium retained its ability to aerobically produce ATP and transferred most of its functional genome to the virus as it evolved into the mitochondrion. Here it is proposed that mitosis, meiosis and the sexual cycle all arose from the evolutionary pressures acting upon a lysogenic virus to maintain itself at low copy number whilst developing the ability to spread horizontally through a host population.
Section snippets
Lysogeny, conjugation, immunity and compatibility are proposed as key antecedents in the evolution of the eukaryotic cell cycle
Lysogeny is observed in viruses of all three domains (Vostrov et al., 1996; Prangishvili et al., 1999; Efstathiou and Preston, 2005) and allows viral transmission through an indefinite number of cellular generations before entry into a lytic cycle. Viral lysogeny can be maintained either by integration into the host genome (e.g., bacteriophage lambda; Campbell et al., 1992), or by the establishment of a persistent presence in the host cytoplasm (e.g., P1, N15, LE1, Ď•20 and Ď•BB1; Casjens et al.,
Mitosis originates from mechanisms to maintain a pox-like virus as a low copy number lysogen
In the VE hypothesis, a pox-like virus was proposed to be the ancestor of the eukaryotic nucleus because the pox-like viruses share several fundamental features of genetic design with the eukaryotic nucleus. These features include, a linear chromosome with short telomeric repeats, a complex membrane bound capsid, the ability to produce capped mRNA, and the ability to extrude the capped mRNA across the viral membrane into the cytoplasm (Bell, 2001).
In the VE hypothesis the hypothetical pox-like
Meiosis and the sexual cycle are derived from viral conjugation and incompatibility processes
It is proposed that the loss of the ability to enter into a lytic cycle subjected the lysogenic virus to similar evolutionary pressures to those acting on non-viral plasmid lysogens. In the case of conjugative plasmids, these evolutionary pressures have resulted in the development of processes that allow the plasmids to spread horizontally within a host population. It is proposed that similar evolutionary pressures acting on the pox-like ancestor of the nucleus led to the evolution of a
Discussion
In the VE hypothesis, it is argued that the eukaryotic nucleus is descended from a pox-like DNA virus that established a permanent lysogeny in the cytoplasm of an archaeal host (Bell, 2001, Bell, 2004). As discussed in the previous papers, the descent of the nucleus from a pox-like virus provides a potential explanation for many of the unique characteristics of the eukaryotic cellular design, including the origin of linear chromosomes, telomeres, mRNA capping, and the separation of
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2017, Current BiologyCitation Excerpt :This would make it the oldest class II fusogen that we know of and thus a strong candidate as the ancestral fusogen from which other class II proteins evolved. At the same time, the existence of viruses pre-dates the evolution of eukaryotic sex [33–36], and it is equally plausible that HAP2 originated with a virus, was exapted for use in gamete cell fusion early in the course of eukaryotic evolution, and was then reacquired by modern viruses. Invasion of eukaryotic genomes by viruses is widespread [32, 37], and there is clear evidence that genes for viral fusogens have taken on new functions in the case of mammalian syncytins, which are of retroviral origin, and promote cell-cell fusion during placentation in diverse species [38, 39].
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Open Questions About Giant Viruses
2013, Advances in Virus ResearchCitation Excerpt :Interestingly, this is an important point of convergence between us and the tenants of the accretion model. This is also compatible with the notion, discussed in detail elsewhere (Claverie, 2006; Claverie & Abergel, 2010), that there might be an evolutionary link between the emergence of the cell nucleus and the origin of the large DNA viruses (Bell, 2001, 2006; Villarreal & DeFilippis, 2000; Villarreal & Witzany, 2010). Speculating further along the genome reduction scenario, we propose that the first irreversible step committing a cell-like (eventually parasitic) microorganism to the virus evolutionary pathway was the loss of its protein translation capability, for instance following a detrimental mutation in an essential ribosomal protein (or in the ribosomal RNA).
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