Article

Giant viruses coexisted with the cellular ancestors and represent a distinct supergroup along with superkingdoms Archaea, Bacteria and Eukarya

BMC Evolutionary Biology (Impact Factor: 3.37). 08/2012; 12(1):156. DOI: 10.1186/1471-2148-12-156
Source: PubMed

ABSTRACT

Background
The discovery of giant viruses with genome and physical size comparable to cellular organisms, remnants of protein translation machinery and virus-specific parasites (virophages) have raised intriguing questions about their origin. Evidence advocates for their inclusion into global phylogenomic studies and their consideration as a distinct and ancient form of life.

Results
Here we reconstruct phylogenies describing the evolution of proteomes and protein domain structures of cellular organisms and double-stranded DNA viruses with medium-to-very-large proteomes (giant viruses). Trees of proteomes define viruses as a ‘fourth supergroup’ along with superkingdoms Archaea, Bacteria, and Eukarya. Trees of domains indicate they have evolved via massive and primordial reductive evolutionary processes. The distribution of domain structures suggests giant viruses harbor a significant number of protein domains including those with no cellular representation. The genomic and structural diversity embedded in the viral proteomes is comparable to the cellular proteomes of organisms with parasitic lifestyles. Since viral domains are widespread among cellular species, we propose that viruses mediate gene transfer between cells and crucially enhance biodiversity.

Conclusions
Results call for a change in the way viruses are perceived. They likely represent a distinct form of life that either predated or coexisted with the last universal common ancestor (LUCA) and constitute a very crucial part of our planet’s biosphere.

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Available from: Arshan Nasir, Dec 18, 2013
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    • "Since RNA viruses have small genomes and diverse strategies of replication, it has been suggested they have their roots in the early stages of evolution that preceded the appearance of cellular DNA genomes (Forterre, 2006; Koonin et al., 2006; Agol, 2010; Koonin and Dolja, 2013). On the other extreme are the so-called nucleocytoplasm large DNA viruses (NCLDV) endowed with the largest viral genomes reported so far, which in some cases may be even larger than some small prokaryotic genomes, have been considered by some as a fourth domain of life comparable to the Bacteria, the Archaea and the Eucarya (Raoult et al., 2004; Boyer et al., 2009; Nasir et al., 2012). "
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    ABSTRACT: It has been suggested that RNA viruses and other subcellular entities endowed with RNA genomes are relicts from an ancient RNA/protein World which is believed to have preceded extant DNA/RNA/protein-based cells. According to their proponents, this possibility is supported by the small-genome sizes of RNA viruses and their manifold replication strategies, which have been interpreted as the result of an evolutionary exploration of different alternative genome organizations and replication strategies during early evolutionary stages. At the other extreme are the giant DNA viruses, whose genome sizes can be as large as those of some prokaryotes, and which have been grouped by some authors into a fourth domain of life. As argued here, the comparative analysis of the chemical nature and sizes of the viral genomes reported in GenBank does not reveal any obvious correlation with the phylogenetic history of their hosts. Accordingly, it is somewhat difficult to reconcile the proposal of the putative pre-DNA antiquity of RNA viruses, with their extraordinary diversity in plant hosts and their apparent absence among the Archaea. Other issues related to the genome size of all known viruses and subviral agents and the relationship with their hosts are discussed.
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    • "Recently discovered giant viruses like Mimivirus or Megavirus (belonging to the Megaviridae), that possess genomes of a size comparable to the genomes of bacteria (containing few tRNA genes, translation initiation and elongation factors and even some simple repeats), blur the established frontiers between viruses and cellular organisms (Raoult et al., 2004). Giant viruses coexisted with the cellular ancestors (Nasir et al., 2012). Such findings support our view that various acellular forms deserve to be added to the existing broadly accepted six-kingdom system of life (Cavalier-Smith, 2004). "
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    ABSTRACT: There is a huge variety of RNA- and DNA-containing entities that multiply within and propagate between cells across all kingdoms of life, having no cells of their own. Apart from cellular organisms these entities (viroids, plasmids, mobile elements and viruses among others) are the only ones with distinct genetic identities but which are not included in any traditional tree of life. We suggest to introduce or, rather, revive the distinct category of acellular organisms, Acytota, as an additional, undeservedly ignored full-fledged kingdom of life. Acytota are indispensable players in cellular life and its evolution. The six traditional kingdoms (Cytota) and Acytota together complete the classification of the biological world (Biota), leaving nothing beyond.
    Full-text · Article · Aug 2015 · Journal of biomolecular Structure & Dynamics
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    • "Using two of them, which are universal and encode DNA-dependent RNA polymerase subunits, recent phylogenetic analyses with a comprehensive sequence set further supported the four branches of life hypothesis (Sharma et al., 2014). In addition, other research groups strengthened this hypothesis using different methodological approaches or datasets (Wu et al., 2011; Nasir et al., 2012). Eventually, the term " TRUC " (an acronym for Things Resisting Uncompleted Classifications) was introduced for a new classification of life that includes a fourth TRUC, consisting of Megavirales, standing out from the ribosome-based three domain classification (Raoult, 2013, 2014), and we recently described pandoraviruses as new members of a " Fourth TRUC " club (Sharma et al., 2015). "
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    ABSTRACT: Nucleocytoplasmic large DNA viruses, or representatives of the proposed order Megavirales, include giant viruses of Acanthamoeba that were discovered over the last 12 years and are bona fide microbes. Phylogenies based on a few genes conserved amongst these megaviruses and shared by microbes classified as Eukarya, Bacteria, and Archaea, allowed for delineation of a fourth monophylogenetic group or "TRUC" (Things Resisting Uncompleted Classification) composed of the Megavirales representatives. A new Megavirales member named Pithovirus sibericum was isolated from a >30,000-year-old dated Siberian permafrost sample. This virion is as large as recently described pandoraviruses but has a genome that is approximately three to four times shorter. Our objective was to update the classification of P. sibericum as a new member of the "Fourth TRUC" club. Phylogenetic trees were constructed based on four conserved ancient genes and a phyletic analysis was concurrently conducted based on the presence/absence patterns of a set of informational genes from members of Megavirales, Bacteria, Archaea, and Eukarya. Phylogenetic analyses based on the four conserved genes revealed that P. sibericum is part of the fourth TRUC composed of Megavirales members, and is closely related to the families Marseilleviridae and Ascoviridae/Iridoviridae. Additionally, hierarchical clustering delineated four branches, and showed that P. sibericum is part of this fourth TRUC. Overall, phylogenetic and phyletic analyses using informational genes clearly indicate that P. sibericum is a new bona fide member of the "Fourth TRUC" club composed of representatives of Megavirales, alongside Bacteria, Archaea, and Eukarya.
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