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


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.

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.

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.

Download full-text


Available from: Arshan Nasir, Dec 18, 2013
43 Reads
  • Source
    • "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). "
    [Show abstract] [Hide abstract]
    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.
    Journal of biomolecular Structure & Dynamics 08/2015; DOI:10.1080/07391102.2015.1086959 · 2.92 Impact Factor
  • Source
    • "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). "
    [Show abstract] [Hide abstract]
    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.
    Frontiers in Microbiology 08/2015; 6:722. DOI:10.3389/fmicb.2015.00722 · 3.99 Impact Factor
  • Source
    • "phylogenetic analysis of these universal genes has suggested that the giant viruses did not fall into any of three domains of cellular life ( bacteria , archaea and eukaryote ) and prompted the hypothesis that these viruses evolved by reductive evolution from a hypothetical ( conceivably , extinct ) cellular domain ( Colson et al . , 2012 , 2011 ; Nasir et al . , 2012 ; Raoult et al . , 2004 ) . However , independent phylogenetic studies that employed representative sets of cellular life forms from the three domains and more advanced phylogenetic methods have effectively refuted the fourth domain hypothesis by showing that nearly all universal genes of the giant viruses were nested within the eukar -"
    [Show abstract] [Hide abstract]
    ABSTRACT: Viruses and other selfish genetic elements are dominant entities in the biosphere, with respect to both physical abundance and genetic diversity. Various selfish elements parasitize on all cellular life forms. The relative abundances of different classes of viruses are dramatically different between prokaryotes and eukaryotes. In prokaryotes, the great majority of viruses possess double-stranded (ds) DNA genomes, with a substantial minority of single-stranded (ss) DNA viruses and only limited presence of RNA viruses. In contrast, in eukaryotes, RNA viruses account for the majority of the virome diversity although ssDNA and dsDNA viruses are common as well. Phylogenomic analysis yields tangible clues for the origins of major classes of eukaryotic viruses and in particular their likely roots in prokaryotes. Specifically, the ancestral genome of positive-strand RNA viruses of eukaryotes might have been assembled de novo from genes derived from prokaryotic retroelements and bacteria although a primordial origin of this class of viruses cannot be ruled out. Different groups of double-stranded RNA viruses derive either from dsRNA bacteriophages or from positive-strand RNA viruses. The eukaryotic ssDNA viruses apparently evolved via a fusion of genes from prokaryotic rolling circle-replicating plasmids and positive-strand RNA viruses. Different families of eukaryotic dsDNA viruses appear to have originated from specific groups of bacteriophages on at least two independent occasions. Polintons, the largest known eukaryotic transposons, predicted to also form virus particles, most likely, were the evolutionary intermediates between bacterial tectiviruses and several groups of eukaryotic dsDNA viruses including the proposed order "Megavirales" that unites diverse families of large and giant viruses. Strikingly, evolution of all classes of eukaryotic viruses appears to have involved fusion between structural and replicative gene modules derived from different sources along with additional acquisitions of diverse genes. Published by Elsevier Inc.
    Virology 03/2015; 479–480:2-25. DOI:10.1016/j.virol.2015.02.039 · 3.32 Impact Factor
Show more