Jane Flint - Principles of Virology, Volume 1

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 theirshared 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:

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 thestandard 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).

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).

The mimivirus virion, the prototype member of the Mimiviridae , was the first giant virus of amoebae to be discovered. Isolated from water in a cooling tower in England in 1992, it is large enough to be visible in a light microscope and was initially thought to be an intracellular bacterium within its host. Not until publication of a brief note in 2003 did it become apparent that this giant was really a virus. The mimivirus genome of 1.2 Mbp was much larger than that of any known virus at the time, exceeding that of some bacteria. This giant encodes more than 900 proteins, many of which are components of the protein translational apparatus, a function for which other viruses rely entirely on the host.

Since reports of the first giant viruses, the use of different strains of amoebae to screen soil and water samples from diverse environments and geographic locations has yielded more than 50 isolates, assigned to nine distinct families. Among the most spectacular is a Pandoravirus isolate, discovered in saltwater off the coast of Chile in 2013. The genome of this giant is twice the size of the mimivirus genome, and contains ∼2,500 putative protein-coding sequences, most of them never seen before. Furthermore, while mimivirus has a more or less familiar icosahedral capsid, the Pandoravirus has no regular capsid. Instead, the genomes of these viruses are surrounded by an ovoid envelope, with a pore at the apex that allows delivery of the internal components into the cytoplasm of its host. The following year two additional giant amoeba viruses, a circular mollivirus and ovoid pithovirus, were discovered in a sample of Siberian permafrost more than 30,000 years old.

The unusual properties of the giant viruses of amoebae have prompted the somewhat controversial speculation that they might represent a separate branch in the tree of life, or that they arose by reductive evolution from the nucleus of a primitive cellular life form. However, the discovery in 2017 of another group of these viruses, by metagenomic analysis of samples from a sewer in Klosterneuburg, Austria, has suggested a more pedestrian origin. While the new group, called Klosneuviruses, encode numerous components of translational machinery, comprehensive phylogenetic analyses indicate that these genes were captured from a cellular host by a smaller, precursor virus during evolution of Klosneuviruses. If this is a general phenomenon, the 2018 description of tailed mimivirus relatives, isolated from the extreme environments of an alkaline soda lake in Brazil and from deep in the Atlantic Ocean, must be considered an extraordinary example of such capture. The genomes of these odd-looking isolates, called Tupanviruses, contain nearly all of the necessary translation-associated genes, lacking only ribosomes for protein synthesis. It would seem that there is still much to ponder concerning the evolution of these giant viruses.