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      Eukaryogenesis: The Rise of an Emergent Superorganism

      research-article
      * ,
      Frontiers in Microbiology
      Frontiers Media S.A.
      evolution, viruses, emergent complexity, eukaryotes, Tree of Life, virocell

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          Abstract

          Although it is widely taught that all modern life descended via modification from a last universal common ancestor (LUCA), this dominant paradigm is yet to provide a generally accepted explanation for the chasm in design between prokaryotic and eukaryotic cells. Counter to this dominant paradigm, the viral eukaryogenesis (VE) hypothesis proposes that the eukaryotes originated as an emergent superorganism and thus did not evolve from LUCA via descent with incremental modification. According to the VE hypothesis, the eukaryotic nucleus descends from a viral factory, the mitochondrion descends from an enslaved alpha-proteobacteria and the cytoplasm and plasma membrane descend from an archaeal host. A virus initiated the eukaryogenesis process by colonising an archaeal host to create a virocell that had its metabolism reprogrammed to support the viral factory. Subsequently, viral processes facilitated the entry of a bacterium into the archaeal cytoplasm which was also eventually reprogrammed to support the viral factory. As the viral factory increased control of the consortium, the archaeal genome was lost, the bacterial genome was greatly reduced and the viral factory eventually evolved into the nucleus. It is proposed that the interaction between these three simple components generated a superorganism whose emergent properties allowed the evolution of eukaryotic complexity. If the radical tenets of the VE hypothesis are ultimately accepted, current biological paradigms regarding viruses, cell theory, LUCA and the universal Tree of Life (ToL) should be fundamentally altered or completely abandoned.

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          Most cited references94

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          Marine viruses--major players in the global ecosystem.

          Viruses are by far the most abundant 'lifeforms' in the oceans and are the reservoir of most of the genetic diversity in the sea. The estimated 10(30) viruses in the ocean, if stretched end to end, would span farther than the nearest 60 galaxies. Every second, approximately 10(23) viral infections occur in the ocean. These infections are a major source of mortality, and cause disease in a range of organisms, from shrimp to whales. As a result, viruses influence the composition of marine communities and are a major force behind biogeochemical cycles. Each infection has the potential to introduce new genetic information into an organism or progeny virus, thereby driving the evolution of both host and viral assemblages. Probing this vast reservoir of genetic and biological diversity continues to yield exciting discoveries.
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            Estimating the timing of early eukaryotic diversification with multigene molecular clocks.

            Although macroscopic plants, animals, and fungi are the most familiar eukaryotes, the bulk of eukaryotic diversity is microbial. Elucidating the timing of diversification among the more than 70 lineages is key to understanding the evolution of eukaryotes. Here, we use taxon-rich multigene data combined with diverse fossils and a relaxed molecular clock framework to estimate the timing of the last common ancestor of extant eukaryotes and the divergence of major clades. Overall, these analyses suggest that the last common ancestor lived between 1866 and 1679 Ma, consistent with the earliest microfossils interpreted with confidence as eukaryotic. During this interval, the Earth's surface differed markedly from today; for example, the oceans were incompletely ventilated, with ferruginous and, after about 1800 Ma, sulfidic water masses commonly lying beneath moderately oxygenated surface waters. Our time estimates also indicate that the major clades of eukaryotes diverged before 1000 Ma, with most or all probably diverging before 1200 Ma. Fossils, however, suggest that diversity within major extant clades expanded later, beginning about 800 Ma, when the oceans began their transition to a more modern chemical state. In combination, paleontological and molecular approaches indicate that long stems preceded diversification in the major eukaryotic lineages.
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              A giant virus in amoebae.

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                Author and article information

                Contributors
                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                11 May 2022
                2022
                : 13
                : 858064
                Affiliations
                Microbiogen Pty Ltd. , Sydney, NSW, Australia
                Author notes

                Edited by: Jean-Michel Claverie, Aix-Marseille Université, France

                Reviewed by: Hiroyuki Ogata, Kyoto University, Japan; Juliana Cortines, Federal University of Rio de Janeiro, Brazil

                *Correspondence: Philip J. L. Bell, philip.bell@ 123456microbiogen.com

                This article was submitted to Virology, a section of the journal Frontiers in Microbiology

                Article
                10.3389/fmicb.2022.858064
                9130767
                35633668
                7802d9b0-d601-4e31-8f86-86c561337242
                Copyright © 2022 Bell.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 19 January 2022
                : 15 April 2022
                Page count
                Figures: 7, Tables: 0, Equations: 0, References: 94, Pages: 13, Words: 11057
                Categories
                Microbiology
                Hypothesis and Theory

                Microbiology & Virology
                evolution,viruses,emergent complexity,eukaryotes,tree of life,virocell
                Microbiology & Virology
                evolution, viruses, emergent complexity, eukaryotes, tree of life, virocell

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