Principles of Virology, Volume 1. Jane Flint

http://www.virology.ws/are-viruses-alive/.

       Forterre P. 2016. To be or not to be alive: how recent discoveries challenge the traditional definitions of viruses and life. Stud Hist Philos Biol Biomed Sci 59:100–108.

       van Regenmortel MHV. 2016. The metaphor that viruses are living is alive and well, but it is no more than a metaphor. Stud Hist Philos Biol Biomed Sci 59:117–124.

Cataloging Animal Viruses

As new viruses were being discovered and studied by electron microscopy, the virus world was seen to be a veritable zoo of particles with different sizes, shapes, and compositions. With no standard rules for naming isolates, the viral lexicon was, and still is, idiosyncratic (Box 1.9). Constructing a rational scheme by which these agents could be classified became a subject of colorful and quite heated controversy. A traditionalist camp argued that it was impossible to infer, from the known properties of viruses, anything about their evolutionary origin or their relationships to one another—the major goal of classical taxonomy. Others maintained that despite such limitations, there were significant practical advantages in grouping viruses with similar properties. A major sticking point, however, was finding agreement on which properties should be considered most important in constructing a scheme for virus classification.

The Classical System

      Lwoff, Robert Horne, and Paul Tournier, in 1962, advanced a comprehensive scheme for the classification of all viruses under the classical Linnaean hierarchical system consisting of phylum, class, order, family, genus, and species. Although a subsequently formed international committee on the nomenclature of viruses did not adopt this system in toto, its designation of orders, families, genera, and species is used for the classification of animal viruses.

      One of the most important principles embodied in the system advanced by Lwoff and his colleagues was that viruses should be grouped according to their shared properties rather than those of the cells or organisms they infect. A second principle was a focus on the nature of the nucleic acid genome as the primary criterion for classification. The importance of the genome had become clear when it was inferred from the Hershey-Chase experiment that viral nucleic acid alone can be infectious (Box 1.5). Four characteristics are used in the taxonomic classification of all viruses:

BOX 1.9

      TERMINOLOGY

       Complexities of viral nomenclature

No consistent system for naming viral isolates has been established by their discoverers. For example, among the vertebrate viruses, some are named for the associated diseases (e.g., poliovirus, rabies virus), for the specific type of disease they cause (e.g., murine leukemia virus), or for the sites in the body that are affected or from which they were first isolated (e.g., rhinovirus and adenovirus). Others are named for the geographic locations from which they were first isolated (e.g., Sendai virus [Sendai, Japan] and Coxsackievirus [Coxsackie, NY]) or for the scientists who first discovered them (e.g., Epstein-Barr virus). In these cases, the virus names are capitalized. Some viruses are even named for the way in which people imagined they were contracted (e.g., influenza, for the “influence” of bad air), how they were first perceived (e.g., the giant mimiviruses [Box 1.10], for the fact that they “mimic” bacteria), or totally by whimsy (e.g., Pandoravirus, after Pandora’s jar [later box] of Greek mythology). Finally, combinations of the above designations are also used (e.g., Rous sarcoma virus).

      1 Nature of the nucleic acid in the virus particle (DNA or RNA)

      2 Symmetry of the protein shell (capsid)

      3 Presence or absence of a lipid membrane (envelope)

      4 Dimensions of the virion and capsid

      The elucidation of evolutionary relationships by analyses of nucleic acid and protein sequence similarities is now the standard method for assigning viruses to a particular family and ordering members within a family. For example, hepatitis C virus was classified as a member of the family Flaviviridae and MERS was assigned to the Coronaviridae based on their genome sequences. However, as our knowledge of molecular properties of viruses and their reproduction has increased, other relationships have become apparent. Hepadnaviridae, Retroviridae, and some plant viruses are classified as different families on the basis of the nature of their genomes. Nevertheless, they are all related by the fact that reverse transcription is an essential step in their reproductive cycles, and the viral polymerases that perform this task exhibit important similarities in amino acid sequence. Another example is the classification of the giant protozoan Mimiviridae as members of a related group called nucleocytoplasmic large DNA viruses (NCLDVs), which includes the Poxviridae that infect vertebrates (Box 1.10).

      The International Committee on Taxonomy of Viruses (ICTV), founded by André Lwoff, authorizes and organizes the classification and establishes nomenclature for all viruses. Freely available as a periodically updated, online resource (https://ictv.global/taxonomy), the 2018 report lists orders, families, genera, and species for all known viruses. In addition, it describes numerous viruses that are not yet classified and probably representatives of new genera and/ or families. The ICTV catalog also includes descriptions of subviral agents (satellites, viroids, and prions) and a list of viruses for which information is still insufficient to make assignments. The pace of discovery of new viruses has been accelerated greatly with the application of metagenomic analyses, direct sequencing of genomes from environmental samples, suggesting that we have barely begun to chart the viral universe.

      The ICTV nomenclature has been applied widely in both the scientific and medical literature, and therefore we adopt it in this text. In this nomenclature, the Latinized virus family names are recognized as starting with capital letters and ending with -viridae, as, for example, in the family name Parvo-viridae. These names are used interchangeably with their common derivatives, as, for example, parvoviruses (see additional examples in the Appendix).

Classification by Genome Type: the Baltimore System

      Francis Crick conceptualized the central dogma for flow of information from the DNA genome in all living cells:

      DNA → mRNA → protein

As intracellular parasites that depend on the host cell’s translational machinery for protein production, all viruses must direct the synthesis of mRNAs. But viral genomes comprise both DNA and RNA in a variety of conformations. Appreciation of the essential role of the translational machinery in virus reproduction inspired David Baltimore, in 1971, to devise a classification scheme for viruses, based on the steps that would be required to produce mRNA from their diverse genomes (Fig. 1.12).

BOX 1.10

      DISCUSSION

       Giant viruses discovered in amoebae

      The