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The Origins of Giant Viruses, Virophages and Their Relatives in Host Genomes Aris Katzourakis* and Amr Aswad

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The Origins of Giant Viruses, Virophages and Their Relatives in Host Genomes Aris Katzourakis* and Amr Aswad Katzourakis A and Aswad A BMC Biology 2014, 12:51 http://www.biomedcentral.com/1741-7007/12/51 COMMENTARY The origins of giant viruses, virophages and their relatives in host genomes Aris Katzourakis* and Amr Aswad Abstract including the discovery last month of Samba virus, a wild mimivirus from the Amazonian Rio Negro [4]. Al- Giant viruses have revealed a number of surprises that though slightly larger, Samba virus shares identity across challenge conventions on what constitutes a virus. the majority of its genome to the original Bradford The Samba virus newly isolated in Brazil expands the mimivirus, further expanding the widespread distribu- known distribution of giant mimiviruses to a near- tion of these giant viruses. The defining feature of giant global scale. These viruses, together with the viruses is that they are an extreme outlier in terms of transposon-related virophages that infect them, pose a genome size: Acanthamoeba polyphaga mimivirus has a number of questions about their evolutionary origins 1.2 Mb genome [1], which was double the size of the lar- that need to be considered in the light of the gest virus known at the time, and pandoravirus genomes complex entanglement between host, virus and reach up to 2.5 Mb [2]. Giant viruses are also extreme virophage genomes. outliers in terms of their physical size, being too large to pass through porcelain filters, a criterion historically See research article: used to define a virus. As a further challenge to the trad- http://www.virologyj.com/content/11/1/95. itional definition of viruses, giant viruses have several es- sential protein synthesis genes that have thus far been The discovery of giant viruses thought to be exclusive to cellular life [1]. Giant DNA viruses are double-stranded DNA (dsDNA) viruses that have particle and genome sizes comparable Evolutionary origins of viral giantry to those of small bacteria, and a number of features that Determining the evolutionary relationships among vi- are uncharacteristic of viruses. These include the pres- ruses is crucial to investigating the origins of features ence of several genes that are similar to cellular genes such as their size, but is complicated by the absence of such as those involved in DNA repair, translation, pro- universally conserved viral genes. The Baltimore system tein folding, and polysaccharide synthesis [1]. Acanth- classifies viruses according to genome type and replica- amoeba polyphaga mimivirus was the first of the giant tion strategy, therefore placing giant viruses among DNA viruses to be discovered, initially isolated in the others with dsDNA genomes. They are also considered search for the causative agent of pneumonia during a hos- on the basis of distinguishing biological features to be- pital outbreak in Bradford, UK [1]. Since then, related vi- long within the nucleocytoplasmic large DNA viruses ruses have been identified in a range of environments, (NCLDVs) alongside viral families such as poxviruses including the discovery last year of the morphologically and iridoviruses [5]. While dsDNA viruses in general do and genetically distinct pandoraviruses, which are even not appear to have a single evolutionary origin, the larger than the mimiviruses [2]. More recently, the NCLDVs all contain five core genes and tend to share a 30,000-year-old Pithovirus sibericum was unearthed and suite of 50 or so likely ancestral genes [5] that partition brought back to life from Siberian permafrost [3]. them from other large eukaryotic dsDNA viruses such as Many of the giant viruses discovered to date have nudiviruses, herpesviruses and baculoviruses. NCLDVs amoeba hosts and amoeba culture techniques have do share some genes with these other large DNA viruses, proved instrumental in identifying these giants, but are additionally distinguished by an either com- pletely or largely cytoplasmic replication cycle [5]. * Correspondence: [email protected] Although the low levels of genetic similarity among Department of Zoology, University of Oxford, Oxford OX1 3PS, UK NCLDVs complicate the precise phylogenetic placement © 2014 Katzourakis and Aswad; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Katzourakis A and Aswad A BMC Biology 2014, 12:51 Page 2 of 4 http://www.biomedcentral.com/1741-7007/12/51 of giant viruses, the relationships between NCLDV fam- ovoid rather than icosahedral morphology [3]. Moreover, ilies have been reconstructed using multiple conserved of the more than 1,000 pandoravirus genes, 93% are pre- genes [5]. The phylogenetic relationships of DNA poly- viously unknown to biologists [2]. Many viruses contain merase genes from NCLDVs reveal that the Mimiviridae some of these so-called orphan genes, but the high per- family, one of the larger members of which is the Samba centage of orphans in a single virus highlights how lim- virus [4], groups with the Marseilleviridae and Iridoviri- ited our sampling of the diversity of viral genes is. dae that are 1.2 Mb, 350 kbp and 200 kbp in size, re- spectively (Figure 1). Pandoraviruses are most closely Giant viruses are susceptible to viral infection by related to Emiliana huxleyi virus, which has a genome relatives of eukaryotic DNA transposons that is 0.41 Mb in size. Thus, pandoraviruses are derived Giant viruses reproduce in ‘viral factories’, which are members of Phycodnaviridae and therefore phylogenet- cytoplasmic compartments of the host cell that can be ically distinct from the rest of the giant viruses [2,5]. as large as the nucleus (Figure 2). Accompanying the While it has been argued that the large genomes of these surprise of discovering giant viruses was the discovery of giants suggest a large and complex ancestor, the most a group of associated viruses that are not capable of rep- parsimonious interpretation of the phylogenetic evidence lication in their absence, and instead exploit the viral is that viral giantry evolved independently on at least factory for replication. Other viruses are known to re- two occasions from ancestors with much smaller ge- quire helper viruses for replication, but these ‘viro- nomes [5] (Figure 1). phages’ result in the formation of defective mimiviruses, The genome sizes of the NCLDVs vary greatly, from implying a parasitic relationship [6]; they make the giant the 150 kb genomes of the poxviruses to the 2.5 Mb ge- viruses ill. For example, the infection of Samba virus by nomes of pandoraviruses [2,5]. This hints at the possibil- its virophage results in a reduction of viral titer of over ity that viruses with intermediate genome sizes may 80%, as well as partial recovery of the host amoebae [4]. exist. While many lineages may be extinct, it seems This parasitism is therefore part of a complex relation- likely that at least some will eventually be found through ship between giant viruses, their hosts and the viro- metagenomic sampling. It would be premature to con- phages [6]. Virophage genomes are dwarfed by the clude that mimivirus and pandoravirus represent the lar- mimiviruses that they infect, being approximately 20 gest DNA viruses that will be found. Interestingly, the kbp in length, and have been identified in association recently uncovered pithoviruses are phylogenetically with several members of Mimiviridae [6,7]. There are closer to the mimivirus/marseillevirus group despite a now multiple strains of the first virophage, named Sput- morphological resemblance to pandoraviruses that have nik [6], including the Rio Negro isolate from the Samba Figure 1. Stylized figure depicting the phylogenetic relationships, genome length and virion size of various nucleocytoplasmic large DNA viruses (NCLDVs). The maximum likelihood tree shown is a simplified version of the NCLDV subtree for DNA polymerase adapted from [6], where collapsed clades in the original tree are represented by single branches. Numbers at each node are expected likelihood weights from 1,000 rearrangements. The scale throughout the figure is approximate. Katzourakis A and Aswad A BMC Biology 2014, 12:51 Page 3 of 4 http://www.biomedcentral.com/1741-7007/12/51 The fact that Mavericks are widespread in the animal kingdom indicates that a number of virophages, and therefore NCLDVs, are yet to be discovered in associ- ation with these hosts. A question of gene flow and its evolutionary consequences Gene flow has played a central role in the evolutionary history of virophages. Integrated virophages have been found in a mimivirus genome, and virophage genes also share similarity to genes in other DNA transposons, such as a class of linear plasmids called transpovirons that are also found in mimiviruses [9]. Some virophage genes also show similarity to bacteriophages, cellular genes, and their respective viral hosts [7]. This com- pound nature of virophage genomes is evidence of ex- tensive horizontal gene transfer, and although the Figure 2. Scanning electron microscope image of Samba virus precise details of this gene flow are not fully understood, and Rio Negro virophage adapted from [4]. The figure depicts perspectives from paleovirology - the study of viral rem- Samba virus morphogenesis within the viral factory that is formed in nants, or ‘fossils’, found in host genomes - may help to Acanthamoeba castellanii, as well as the parasitic virophage particles interspersed among the giant virions. clarify them. Analysis of these viral remnants, known as endogenous viral elements (EVEs), has revealed that all viruses can in principle integrate in a heritable fashion virus [4] and more distantly related virophages such as into the host genome, thus preserving information from Mavirus, identified from the Cafeteria roenbergensis the distant evolutionary past [10].
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