History of Virus Classification and Virus Nomenclature

Humans feel the need to classify natural entities and the viruses are no exception. As in other biological systems, virus classification is an approximate and imperfect exercise. Like any other type of classification, it is a totally artificial and human-driven activity without any natural base. However, science requires workable descriptions of living systems and their constituent parts, and, when achieved properly, classifications are extremely useful for showing similar characteristics and properties across populations. Unfortunately for virus taxonomy no fossil record exists and so evolutionary relationships are very speculative, meaning that only a logical and precise virus classification can provide indications of the evolution of viruses. Appropriately chosen classification criteria are also informative in the case of newly discovered viruses. In theory, nomenclature and classification are totally independent, but for viruses both issues are often considered at the same time. As a result, taxonomic names for the viruses have always been the subject of passionate discussions and the taxonomic status of viruses is a sensitive and critical issue.

Virus classification is a relatively new exercise, as the first evidence for existence of a virus was only presented at the end of the nineteenth century by Beijerinck in 1898. It was not until 1927 that Johnson, a plant virologist, drew attention to the need for a system of virus nomenclature and classification. First efforts to classify viruses utilized a range of ecological and biological criteria, including pathogenic properties in the case of human and animal viruses, and symptoms for plant viruses. For example, viruses sharing the pathogenic properties causing hepatitis (e.g. hepatitis A virus, hepatitis B virus, yellow fever virus, and Rift Valley fever virus) were grouped together as 'the hepatitis viruses'. Virology developed substantially in the 1930s and early classifications for the viruses reflected these advances. In 1939, Holmes published a classification of plant viruses dependent on host reactions and differential host species, using a binomial-trinomial nomenclature based on the name of the infected plant; however, only 89 viruses were described and classified in this way. With the development of electron microscopy and biochemical studies in the 1950s, the first virus groupings based on common virion properties emerged: like the Herpesvirus group described by Andrewes in 1954, the Myxovirus group by Andrewes et al, in 1955, and the Poxvirus group by Fenner and Burnet in 1957. During this period there was also an explosion of newly discovered viruses; in response, several individuals and committees independently proposed virus classification systems but none was widely adopted by the scientific community. It became obvious that only an international association of virologists could propose a comprehensive and universally acceptable system of virus classification.

At the 1966 International Congress for Microbiology held in Moscow, the International Committee on Nomenclature of Viruses (ICNV) was established by an international group of 43 virologists. An international organization was set up with the aim of developing a taxonomy and nomenclature system for all viruses that would be recognized worldwide. The name of the ICNV was changed in 1974 to the more appropriate International Committee on Taxonomy of Viruses (ICTV), which remains active today. ICTV, the unique official committee of the Virology Division, is now considered the international official body for all matters related to taxonomy and nomenclature of viruses.

Since the founding of the ICTV, all virologists have agreed that the hundreds of viruses isolated from different organisms should be classified together in a unique system, but separate from other microorganisms such as fungi, bacteria and mycoplasma. However, there was much controversy on the way to do it. Lwoff, Home and Tournier argued for the adoption of a system classifying viruses into subphyla, classes, orders, suborders and families. Descending hierarchical divisions would have been based on nucleic acid type (DNA or RNA), strandedness (single or double), presence or absence of an envelope, capsid symmetry, and so on. The hierarchy of this system has never been recognized by the ICTV; nevertheless, the types of criteria used became the basis of the universal taxonomy system now in place, and all ICTV reports have used this scheme. Until 1990, no hierarchical classification level higher than the family was used, however, the system has recently begun to move in this direction. A first order, Mononegavirales, was accepted in 1990, and another two, Caudovirales and Nidovirales, were adopted in 1996. In its nonlinnean structure, the scheme is quite different from that used in the taxonomy of bacteria and other organisms. Nevertheless, the usefulness of the scheme is being demonstrated by its wide application. It has replaced all competing classification schemes for all viruses and no one would now dispute with the ICTV the international mandate to name and classify viruses.

Since its establishment, a total of seven virus taxonomic reports (also known by the names of the ICTV Presidents acting as Editors in Chief of the reports) have been published by the ICTV: Wildy in 1971; Fenner in 1976; Matthews in 1979; Matthews in 1982; Francki et al in 1991; Murphy et al in 1995; and van Regenmortel et al in 1999. At the first meeting in Mexico City in 1970, two families with a corresponding two genera and 24 floating genera were adopted to begin the grouping of the vertebrate, invertebrate and bacterial viruses. In addition, 16 plant virus groups were designated, as reported by Matthews in 1983. The fifth ICTV report, edited by Francki et al in 1991, described one order, 40 families, nine subfamilies, 102 genera, two floating genera and two subgenera for vertebrate, invertebrate, bacterial and fungal viruses, and 32 groups and seven subgroups for plant viruses. While most virologists shifted to placing viruses in families and genera, plant virologists retained the term 'groups' until 1993. It was only in 1995, as described in the sixth ICTV report, that the ICTV proposed a uniform system for all viruses, with two orders, 50 families, nine subfamilies, 126 genera, 23 floating genera and four subgenera encompassing 2644 assigned viruses. Most recently, at the 28th meeting of the ICTV in March 1998 in San Diego, California, the Universal Virus Classification was adopted; this comprises three orders, 56 families, nine subfamilies, 203 genera, 30 floating genera and a total of 3954 species, strains and/ or serotypes of species and tentative species. It is a general trend that the number of described taxa and the number of species of viruses is increasing steadily, easily explained by the increasing complexity of the virus classification and by the amount of data available to demarcate viruses.

With precise and complete descriptions available for a large number of virus families, this classification now constitutes a valuable source of information for new 'unknown' viruses. Therefore, the ICTV classification is not only a taxonomic exercise for virus evolutionists but also a valuable diagnostic tool and educational system for virologists, teachers, medical doctors and epidemiologists.

How does the ICTV operate?

The ICTV is a committee of the Virology Division, which is in turn part of the International Union of Microbiological Societies. The ICTV is a nonprofit-making organization composed of prominent virologists representing countries from throughout the world who work to designate virus names and taxa through a democratic process. The ICTV operates through a number of committees, subcommittees and study groups consisting of more than 492 eminent virologists with expertise in viruses infecting humans, animals, insects, protozoa, archaea, bacteria, mycoplasma, fungi, algae, yeasts and plants. Taxonomic proposals are initiated and formulated by individuals or by the study groups. These proposals are revised and accepted by the corresponding subcommittees and presented for executive committee approval. All decisions are then ratified at a plenary session (or also now by postal vote) held at each Virology Congress where all members of ICTV and more than 50 representatives of national microbiological societies are represented. At present, there are 47 study groups working in concert with six subcommittees - namely, the vertebrate, invertebrate, plant, bacteria, fungus and virus data subcommittees. The ICTV does not impose any taxonomic terms or taxa but ensures that all propositions are compatible with ICTV rules for homogeneity and consistency. The ICTV regularly publishes reports describing all existing virus taxa with a list of classified viruses as well as descriptions of virus families and genera. An Internet web site, where the most important information relative to virus taxonomy is made available, is updated regularly. The sixth report was published by Murphy et al (1995) and the seventh by van Regenmortel et al (1999).

The increasing number of virus species and virus strains being identified, together with the explosion of data on many descriptive aspects of viruses and viral diseases, and particularly sequence data, has led the ICTV to launch an international virus database project. This project, termed ICTVdB, is scheduled to be fully operational and accessible to the scientific community around the year 2000. The ICTVdB, in addition to the taxonomic descriptions of all the taxa, will comprise all the information available about each virus species, and later each virus strain, for all the descriptors necessary to identify and recognize all viruses.

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