- Open Access
The origins of giant viruses, virophages and their relatives in host genomes
© Katzourakis and Aswad; licensee BioMed Central 2014
- Received: 9 June 2014
- Accepted: 24 June 2014
- Published: 30 June 2014
Giant viruses have revealed a number of surprises that challenge conventions on what constitutes a virus. The Samba virus newly isolated in Brazil expands the known distribution of giant mimiviruses to a near-global scale. These viruses, together with the transposon-related virophages that infect them, pose a number of questions about their evolutionary origins that need to be considered in the light of the complex entanglement between host, virus and virophage genomes.
See research article: http://www.virologyj.com/content/11/1/95.
- Host Genome
- Close Evolutionary Relationship
- Cellular Life
- Giant Virus
- dsDNA Virus
Giant DNA viruses are double-stranded DNA (dsDNA) viruses that have particle and genome sizes comparable to those of small bacteria, and a number of features that are uncharacteristic of viruses. These include the presence of several genes that are similar to cellular genes such as those involved in DNA repair, translation, protein folding, and polysaccharide synthesis []. Acanthamoeba polyphaga mimivirus was the first of the giant DNA viruses to be discovered, initially isolated in the search for the causative agent of pneumonia during a hospital outbreak in Bradford, UK []. Since then, related viruses have been identified in a range of environments, including the discovery last year of the morphologically and genetically distinct pandoraviruses, which are even larger than the mimiviruses []. More recently, the 30,000-year-old Pithovirus sibericum was unearthed and brought back to life from Siberian permafrost [].
Many of the giant viruses discovered to date have amoeba hosts and amoeba culture techniques have proved instrumental in identifying these giants, including the discovery last month of Samba virus, a wild mimivirus from the Amazonian Rio Negro []. Although slightly larger, Samba virus shares identity across the majority of its genome to the original Bradford mimivirus, further expanding the widespread distribution of these giant viruses. The defining feature of giant viruses is that they are an extreme outlier in terms of genome size: Acanthamoeba polyphaga mimivirus has a 1.2 Mb genome [], which was double the size of the largest virus known at the time, and pandoravirus genomes reach up to 2.5 Mb []. Giant viruses are also extreme outliers in terms of their physical size, being too large to pass through porcelain filters, a criterion historically used to define a virus. As a further challenge to the traditional definition of viruses, giant viruses have several essential protein synthesis genes that have thus far been thought to be exclusive to cellular life [].
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 []. Some virophage genes also show similarity to bacteriophages, cellular genes, and their respective viral hosts []. This compound nature of virophage genomes is evidence of extensive horizontal gene transfer, and although the precise details of this gene flow are not fully understood, perspectives from paleovirology - the study of viral remnants, or ‘fossils’, found in host genomes - may help to 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 into the host genome, thus preserving information from the distant evolutionary past []. Mimivirus EVEs have not been found, and one might suspect that their extraordinarily large genomes mean that they are unlikely to form EVEs. However, we could consider a virophage EVE to exist in the form of Mavericks; in some sense, a mimivirus that donates genes to a subsequently endogenized virophage could be thought of as a ‘vicarious EVE’. This flow of genes, from mimivirus to virophage to host genome, is therefore evident in the amoeba genome.
One proposal to explain the endogenization of virophages is that it could have been positively selected for, since the association with a virophage is beneficial to the host cell (owing to its interference with the replication of the large DNA virus) []. The survival advantage gained by an integrated virophage could conceivably be the production of virophages as a kind of antiviral response. If the viral threat were lost, then selection for the maintenance of virophage production would be relaxed, explaining the proposed loss of virophage features in Mavericks []. Because only a handful of virophages have been described, there are insufficient data to investigate the evolutionary dynamics at play. With improvements in sequencing, bioinformatics and metagenomics, viral discovery is increasing exponentially, and moving beyond studies of immediate medical and economic interest. These advances will generate more data that will be suitable for the study of these evolutionary dynamics.
The discovery of giant viruses has crossed some of the boundaries between viruses and cellular life, although ribosomes remain a distinguishing feature. The conflict between giant viruses and their hosts, with the former also infected by virophages, alongside genomic invasions with related transposons, is reminiscent of Darwin’s tangled bank, recapitulated at the microscopic scale in a droplet of water. Elucidating the role of gene flow between these microscopic entities will reveal their evolutionary dynamics and aspects of the origins of viruses and cellular life.
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