Viral eukaryogenesis

Viral eukaryogenesis is the hypothesis that the cell nucleus of eukaryotic life forms evolved from a large DNA virus in a form of endosymbiosis within a methanogenicarchaeon or a bacterium. The virus later evolved into the eukaryotic nucleus by acquiring genes from the hostgenome and eventually usurping its role. The hypothesis was proposed by Philip Bell in 2001[1] and was further popularized with the discovery of large, complex DNA viruses (such as Mimivirus) that are capable of protein biosynthesis. Recent supporting evidence includes the discovery that, upon the infection of a bacterialcell, the giant bacteriophage201Phi2-1 (of genus Phikzvirus) assembles a nucleus-like structure that segregates proteins according to function.[2] This nucleus-like structure and its key properties have been found conserved in the related phages.[3]

The viral eukaryogenesis hypothesis has inflamed the longstanding debate over whether viruses are livingorganisms. Many biologists do not consider viruses to be alive, but the hypothesis posits that viruses are the originators of the DNA genetic mechanism shared by all eukaryotes alive today (and possibly that of prokaryotes as well).[4]

Critics of the theory point out that the similarities between DNA viruses and nuclei can be taken as evidence either of viral eukaryogenesis or of its converse, nuclear virogenesis: that complex eukaryotic DNA viruses could have originated from infectious nuclei.[4]

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The viral eukaryogenesis hypothesis posits that eukaryotes are composed of three ancestral elements: a viral component that became the modern nucleus; a prokaryotic cell (an archaeon according to the eocyte hypothesis) which donated the cytoplasm and cell membrane of modern cells; and another prokaryotic cell (here bacterium) that, by endocytosis, became the modern mitochondrion or chloroplast.

In 2006, researchers suggested that the transition from RNA to DNA genomes first occurred in the viral world.[5] A DNA-based virus may have provided storage for an ancient host that had previously used RNA to store its genetic information (such host is called ribocell or ribocyte).[4] Viruses may initially have adopted DNA as a way to resist RNA-degradingenzymes in the host cells. Hence, the contribution from such a new component may have been as significant as the contribution from chloroplasts or mitochondria. Following this hypothesis, archaea, bacteria, and eukaryotes each obtained their DNA informational system from a different virus.[5] In the original paper it was also an RNA cell at the origin of eukaryotes, but eventually more complex, featuring RNA processing. Although this is in contrast to nowadays more probable eocyte hypothesis, viruses seem to have contributed to the origin of all three domains of life (‘out of virus hypothesis’). It has also been suggested that telomerase and telomeres, key aspects of eukaryotic cell replication, have viral origins. Further, the viral origins of the modern eukaryotic nucleus may have relied on multiple infections of archaeal cells carrying bacterial mitochondrial precursors with lysogenic viruses.[6] The viral eukaryogenesis hypothesis depicts a model of eukaryotic evolution in which a virus, similar to a modern pox virus, evolved into a nucleus via gene acquisition from existing bacterial and archaeal species.[7] The lysogenic virus then became the information storage center for the cell, while the cell retained its capacities for gene translation and general function despite the viral genome’s entry. Similarly, the bacterial species involved in this eukaryogenesis retained its capacity to produce energy in the form of ATP while also passing much of its genetic information into this new virus-nucleus organelle. It is hypothesized that the modern cell cycle, whereby mitosis, meiosis, and sex occur in all eukaryotes, evolved because of the balances struck by viruses, which characteristically follow a pattern of tradeoff between infecting as many hosts as possible and killing an individual host through viral proliferation. Hypothetically, viral replication cycles may mirror those of plasmids and viral lysogens. However, this theory is controversial, and additional experimentation involving archaeal viruses is necessary, as they are probably the most evolutionarily similar to modern eukaryotic nuclei.[8][9]

The viral eukaryogenesis hypothesis points to the cell cycle of eukaryotes, particularly sex and meiosis, as evidence.[8] Little is known about the origins of DNA or reproduction in prokaryotic or eukaryotic cells. It is thus possible that viruses were involved in the creation of Earth’s first cells.[10] The eukaryotic nucleus contains linear DNA with specialized end sequences, like that of viruses (and in contrast to bacterial genomes, which have a circular topology); it uses mRNA capping, and separates transcription from translation. Eukaryotic nuclei are also capable of cytoplasmic replication. Some large viruses have their own DNA-directed RNA polymerase.[4] Transfers of “infectious” nuclei have been documented in many parasiticred algae.[11] Another supporting evidence is that the m7G capping apparatus (involved in uncoupling of transcription from translation) is present in both Eukarya and Mimiviridae but not in Lokiarchaeota that are considered the nearest archaeal relatives of Eukarya according to the Eocyte hypothesis (also supported by the phylogenetic analysis of the m7G capping pathway).[9]

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