A classification system for virophages and satellite viruses

Arch Virol (2016) 161:233–247 DOI 10.1007/s00705-015-2622-9 VIROLOGY DIVISION NEWS A classification system for virophages and satellite viruses Mart Krupovic1 • Jens H. Kuhn2 • Matthias G. Fischer3 Received: 23 June 2015 / Accepted: 21 September 2015 / Published online: 7 October 2015 Ó Springer-Verlag Wien 2015 Abstract Satellite viruses encode structural proteins required for the formation of infectious particles but depend on helper viruses for completing their replication cycles. Because of this unique property, satellite viruses that infect plants, arthropods, or mammals, as well as the more recently discovered satellite-like viruses that infect protists (virophages), have been grouped with other, socalled ‘‘sub-viral agents.’’ For the most part, satellite viruses are therefore not classified. We argue that This article is related to four taxonomic proposals that were approved by the Executive Committee of the ICTV in July of 2015 but have not yet been ratified. The taxonomic changes suggested/proposed/described here: (i) may differ from any new taxonomy that is ultimately approved by the ICTV and (ii) are presented for discussion only and have no official standing. The content of this publication does not necessarily reflect the views or policies of the US Department of Health and Human Services or the institutions and companies affiliated with the authors. This work was funded in part through Battelle Memorial Institute’s prime contract with the US National Institute of Allergy and Infectious Diseases (NIAID) under Contract No. HHSN272200700016I. Subcontractors to Battelle Memorial Institute who performed this work are: J.H.K., an employee of Tunnell Government Services, Inc. & Mart Krupovic & Matthias G. Fischer 1 Unité Biologie Moléculaire du Gène chez les Extrêmophiles, Department of Microbiology, Institut Pasteur, Paris, France 2 Integrated Research Facility at Fort Detrick, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Fort Detrick, Frederick, MD, USA 3 Max Planck Institute for Medical Research, Heidelberg, Germany possession of a coat-protein-encoding gene and the ability to form virions are the defining features of a bona fide virus. Accordingly, all satellite viruses and virophages should be consistently classified within appropriate taxa. We propose to create four new genera — Albetovirus, Aumaivirus, Papanivirus, and Virtovirus — for positivesense single-stranded (?) RNA satellite viruses that infect plants and the family Sarthroviridae, including the genus Macronovirus, for (?)RNA satellite viruses that infect arthopods. For double-stranded DNA virophages, we propose to establish the family Lavidaviridae, including two genera, Sputnikvirus and Mavirus. Introduction Perhaps the most astonishing feature of the virosphere is its diversity. Across the three domains of life, viruses display a stunning versatility in virion organization and genomic content [48]. Furthermore, viruses span an entire range of morphological, genomic, and functional complexity. Some viruses are organized in an extremely simple manner, whereas others are exceedingly complex, surpassing some unicellular organisms in terms of physical dimensions and the number of genome-encoded proteins. Irrespective of complexity, replication of all viruses depends on certain functions provided by the host cell, but the extent of such dependence varies from one virus to the other. Some of the most complex viruses, such as members of the family Mimiviridae, encode many of the molecular machineries required for their multiplication [3, 79], whereas viruses with short genomes, such as circoviruses, have evolved masterful host manipulation strategies that allow hijacking all necessary components from the host cell to support their 123 234 replication [25]. More generally, exploration of viral diversity has revealed a continuum of genome and virion sizes within the viral world, and any threshold between small and large viruses appears increasingly arbitrary [29]. Nevertheless, some groups of viruses appear to be discriminated against based on the level of their complexity. In particular, the classification scheme used by the International Committee on Taxonomy of Viruses (ICTV) does not extend to certain viruses, commonly known as satellite viruses, which, for successful propagation, require certain functions to be provided by other viruses. Paraphrasing George Orwell, it thus seems that ‘‘All viruses are equal, but some viruses are more equal than others’’. The ability to form infectious particles is a feature unique to classified viruses and distinguishes them from other types of (unclassified) mobile genetic elements, such as plasmids and certain transposable elements [51, 80]. It should be noted, however, that classified viruses from several taxonomic groups do not form virions (e.g., endornaviruses, hypoviruses, narnaviruses, umbraviruses [49]). Satellite viruses do encode components required for virion formation. Nevertheless, they are currently not classified into the same taxon ranks as the ‘‘full-fledged’’ viruses. Instead, satellite viruses are banished into a broad category called ‘‘sub-viral agents’’ on an equal footing with non-viral parasitic nucleic acids (satellite nucleic acids and viroids), and even prions [47]. Paradoxically, a distinct classification system has been put in place for the nonprotein-coding viroids (family names ending in ‘‘-viroidae’’, genus names ending in ‘‘-viroid’’) [47], whereas protein-coding satellite nucleic acids remain unclassified. Furthermore, the categorization of satellite viruses as ‘‘subviral’’ agents is not applied consistently. For example, adenovirus-associated satellite viruses (AAVs) that depend on members of the families Herpesviridae, Adenoviridae, Papillomaviridae or Poxviridae for replication have been assigned to the genus Dependoparvovirus, included in the family Parvoviridae, whereas satellite hepatitis delta virus (HDV), which uses hepatitis B virus (family Hepadnaviridae) as a helper virus, is classified as a member of the free-floating genus Deltavirus. Notably, although HDV uses the envelope proteins of the helper virus, it also encodes two proteins, S-HDAg and L-HDAg, which form a ribonucleocapsid [11], thereby adhering to the definition of a satellite virus. By contrast, none of the remaining satellite viruses, some of which are considerably more complex than AAVs and HDV, have undergone proper taxonomic classification. For example, as of the latest, Ninth Report of the ICTV [47] and its updates, the Sputnik virophage, a satellite virus with a complex T = 27 virion and an 18-kb dsDNA genome that encodes structural and DNA replication proteins [58, 109], is labelled a sub-viral agent. Such unsubstantiated separation of satellite viruses from the 123 M. Krupovic et al. remainder of the viral world has previously fuelled discussions on the necessity to reassess the cla (...truncated)