Introduction to Virus Taxonomy

Eric B. Carstens

President of the International Committee on Taxonomy of Viruses

The first internationally organized attempts to introduce some order in the bewildering variety of viruses took place at the International Congress of Microbiology held in Moscow in 1966. A committee was created, later called The International Committee on Taxonomy of Viruses (ICTV), which was given the task of developing a single, universal taxonomic scheme for all the viruses infecting animals (vertebrates, invertebrates and protozoa), plants (higher plants and algae), fungi, bacteria and archaea. ICTV was created as a committee of the Virology Division of the International Union of Microbiological Societies (IUMS) and is governed by Statutes approved by the Virology Division. These are listed in full in Part III of this Report and define the objectives of ICTV as: (i) to develop an internationally agreed taxonomy for viruses (the term “viruses” for this purpose is taken to include viroids and some important groups of satellite viruses); (ii) to develop internationally agreed names for these taxa; (iii) to communicate taxonomic decisions to the international community of virologists; and (iv) to maintain an Index of virus names. The Statutes also state that classification and nomenclature of viruses will be subject to rules set out in an International Code (the current version of which is also provided in Part III).

Virus taxonomy differs from other types of biological classification because ICTV not only regulates a Code of Nomenclature but also considers and approves the creation of virus taxa (currently orders, families, subfamilies genera and species). Priority of publication is not the determining factor. Species names are usually derived from the common (vernacular) name of the virus (usually in English) used to establish the species. The names of all recognized taxa are written in italics with an initial capital letter.

ICTV Reports

To communicate its decisions to the international community, ICTV has published a series of reports. Eight of these have been published since 1971, often following formal approval of taxonomic proposals at plenary meetings of ICTV held during International Congresses for Virology. These reports provide milestones by which the progress in virus taxonomy can be tracked.

The Reports of ICTV

* With the introduction of the current species definition and the adoption of formal species demarcation criteria in the Seventh Report (see text), many virus strains that had hitherto been listed as separate species were reorganized into new, more broadly defined, species. This explains the apparent reduction in their number between the Sixth and Seventh Reports.

The first report was published in 1971 by the then International Committee on Nomenclature of Viruses (ICNV), which had been established in 1966 (Wildy, 1971). This report, covering the period 1966 to 1970, established five Subcommittees: Bacteriophage (now Prokaryote Virus), Invertebrate Virus, Plant Virus, Vertebrate Virus and Cryptograms. The Subcommittees were responsible for approving taxonomic proposals relevant to their groups of viruses and presenting these proposals for approval by the Executive Committee (EC), the ICNV and “a sizable number of virologists working in the relevant field were to be consulted”. This report included the designations Family, Genus (Groups) and Type species, establishing and setting the foundations for viral taxonomy.

By the Second Report (Fenner, 1976), the name change to ICTV had been approved (in 1973) and a formal structure of ICTV officers was reported, consisting of the President, Vice-President, two Secretaries, Chairs of the Subcommittees, Elected Members and Life Members. There was now a Fungal Virus Subcommittee (created from the disbanded Cryptograms Subcommittee) and a Coordination Subcommittee (disbanded 1995) charged with ensuring that Study Groups included virologists with interests in particular virus groups in each class of host affected.

In the Third Report (Matthews, 1979), the viruses were listed on the basis of the kind and strandedness of the nucleic acid making up the viral genome, and the presence or absence of an envelope. It was noted that although ICTV had approved families and genera, there was no such approved “taxon equivalent to species, lying between genus and strain or variant”. The problem of defining species for viruses and naming these species was presented and an extensive discussion of the various points of view as presented by representatives of different groups of viruses was outlined for the first time. It was suggested that it might take 10–20 years to provide these taxa, and an appeal was made to Study Groups to put forward species proposals for consideration by ICTV. This was also the first ICTV report to include virus diagrams, grouped according to the major hosts (animal, bacteria or plant). There was also a list of some unclassified viruses and virus-like agents including agents of scrapie, Kuru and Creutzfeldt–Jakob diseases, viroids, and satellite viruses and satellite RNAs in plants.

The same general arrangement was followed in the Fourth (Matthews, 1982) and Fifth (Francki et al., 1991) Reports. By the time of the Sixth Report (Murphy et al., 1995) ICTV had finally accepted the controversial category of virus species based on a proposal made in 1990 (van Regenmortel, 1990). A virus species was defined as “a polythetic class of viruses that constitutes a replicating lineage and occupies a particular ecological niche”. There was also a clear description of the usage of formal taxonomic nomenclature and an attempt to explain the appropriate usage of this formal nomenclature versus informal vernacular usage. More than 15 years later, this issue continues to elicit controversy.

In the Seventh Report (van Regenmortel et al., 2000), there was an extensive discussion of the species concept in virus taxonomy, and an appeal to the virology community to establish species demarcation criteria which, when applied, could be used to discriminate between virus species within the same genus. Some but not all genera in the Seventh Report did include the criteria by which species were differentiated.

The Eighth Report (Fauquet et al., 2005) continued this process and provided an epic compilation of virus taxonomy illustrated with 436 electron micrographs, diagrams of virus particles, diagrams of genome organization and phylogenetic trees in a total of 1259 pages. As this approached the limit for publication of a single volume book, it was becoming obvious that a different vehicle for transmission of virus taxonomy would be required in the near future to meet the needs of the ever-expanding knowledge base of viruses.

ICTV on the internet

A plan to develop a universal virus database was first discussed around 1990 and led to the development of ICTVdb. The known properties of virus isolates and species were encoded and “translated” for the user in natural language text. Enormous efforts were made to maintain and develop this database and to link with other important databases on biological taxonomy, publications, sequences etc. This was managed by the Virus Data Subcommittee of ICTV and relied heavily on the energy and commitment of Cornelia Büchen-Osmond. The database contains a wealth of important information but it has proved difficult to sustain funding and personnel at a time when taxonomic information is expanding rapidly. At the time of writing, the future of ICTVdb is uncertain.

In recent years, ICTV has also had a web presence providing lists of the currently recognized taxa and information on the Executive Committee, Subcommittees and Study Groups. Templates and other information to assist in writing and submitting taxonomic proposals have also been provided. For some years, this was hosted by Claude Fauquet at the Danforth Center, St Louis, but since 2008 the Virus Data subcommittee has overseen the development and maintenance of an official ICTV website (http://www.ictvonline.org/) that now provides a central point of reference for all ICTV matters. A separate website (http://talk.ictvonline.org/) is used to host taxonomic proposals and allows for comment and discussion to which all virologists are invited to contribute.

The working of ICTV

To date, the Executive Committee (EC) has established 76 international Study Groups (SGs) covering all major virus families and genera. The Chair of each SG is appointed by the relevant Subcommittee Chair who is a member of the EC. Chairs are responsible for (i) organizing discussions among SG members of emerging taxonomic issues in their field, (ii) for overseeing the submission of proposals for new taxonomy, and (iii) the preparation, or revision, of relevant chapter(s) in ICTV Reports.

Developing new taxonomy

ICTV welcomes taxonomic proposals from any interested individual although in practice most are prepared by the relevant SG. An all-purpose template and guidance notes are available for downloading from http://talk.ictvonline.org/. Proposals will be forwarded to all interested SGs and are also made available on the website for public comment. Authors are invited to respond to any comments made. Subcommittee Chairs (or their deputies) then present taxonomic proposals to the Executive Committee for discussion and approval. These meetings are usually held annually. Straightforward proposals to create new species in existing genera can normally be approved at a single meeting if the proposed new species clearly meet the criteria established for species demarcation. The criteria differ between genera and families but are usually specified in the relevant section of this Report. More complex or controversial proposals are made available on the ICTV website for public comment for a further year before being re-considered by the Executive Committee.

Proposals approved by the EC do not become accepted taxonomy until a final “ratification” vote by the full ICTV membership. As specified in the Statutes, this includes members of the various Subcommittees (mostly chairs of Study Groups), National Members and Life Members. Lists of members are provided in part III. Ratification is now done by an email vote after which the approved taxonomy is updated at http://www.ictvonline.org/. This site should always be consulted for the most up-to-date ICTV taxonomic information. Summaries of the voting decisions are also prepared and published in an article under the heading Virology Division News in Archives of Virology.

Virus Taxonomy

The Ninth ICTV Report lists 2284 virus and viroid species distributed amongst 349 genera, 19 subfamilies, 87 families and 6 orders. There is also a chapter of unassigned viruses that provides information on a number of viruses that have not yet been classified but which are probably representatives of new genera and/or families. The final chapters describe the satellites (and other virus-dependent nucleic acids) and prions (which include the agents of spongiform encephalopathies of humans), which are not formally classified by ICTV but simply listed for historical reasons. The Ninth Report is being published both as a book and also online. ICTV expects to make regular updates to keep the online version in step with the latest taxonomic decisions.

Each genus contains a type species (the representative used in defining the genus) and often a number of other species. For each species, authors have been asked to provide details of a single isolate, a characterized virus that is representative of the species as a whole. Some SGs are working to define official “type isolates” for each species; we believe this is a desirable goal although it has not been adopted as ICTV policy.

Most species are members of a genus. However, the code also allows for species to be created within a family (or subfamily) but unassigned to a particular genus. Similarly, most genera are now members of a family but some genera remain unassigned pending further information on their status and relationships. Wherever possible, genera and families are justified on a phylogenetic basis although we recognize that the use of phylogenetic comparisons in virus classification still has much further to go. The designation of higher levels of taxonomy (only orders are recognized in the current Code) is often made difficult by the mosaicism evident amongst the genomes of many related viruses. This poses one of the major challenges for the future. The other most obvious challenge is the vast amount of sequence data that is being generated from environmental samples through metagenomic surveys. These data are revealing the presence of many viruses that are largely uncharacterized and for which host organisms are often unknown (Suttle, 2005). The lack of biological data makes such viruses difficult to classify using current criteria so processes need to be found to integrate the phylogenetic information they provide into future taxonomic schemes.

Glossary of Abbreviations

In addition to universally accepted abbreviations such as DNA and RNA, it is common practice to use abbreviations for virological and technical words in virology. In the Report, we have adopted commonly used abbreviations (e.g. CP for capsid protein and NC for nucleocapsid). These have been approved by the Executive Committee of ICTV for use in the ICTV Report but have no official status. The abbreviations will be used without definition throughout the book, except in a few instances where Study Group conventions (e.g. C in place of CP for capsid protein) dictate different practice. In these instances, abbreviations are defined locally.

Abbreviations

aa    amino acid(s)

bp    base pair(s)

CF    complement fixing

CP    capsid/coat protein (unless otherwise defined)

CPE    cytopathic effect

D    diffusion coefficient

DI    defective interfering

DNAse    deoxyribonuclease

ds    double stranded

gRNA    genomic RNA

HE    hemagglutination esterase

Hel    helicase

HI    hemagglutination inhibition

h    hour(s)

IRES    internal ribosome entry site

kbp    kilobase pairs

kDa    kilodalton

5m⁷G    7-methylguanosine (the 5′ cap structure of many RNAs)

min    minutes(s)

MP    movement protein

Mr    relative molar mass

mRNA    messenger RNA

Mtr    methyltransferase

N    nucleoprotein

NC    nucleocapsid

NES    nuclear export signal

NLS    nuclear localization signal

nt    nucleotide(s)

NTR    non-translated region

ORF    open reading frame

PAGE    polyacrylamide gel electrophoresis

PCR    polymerase chain reaction

Pol    polymerase

Pro    protease

RdRp    RNA-dependent RNA polymerase

Rep    replication associated protein

RF    replicative form

RFLP    restriction fragment length polymorphism

RI    replicative intermediate

RNAse    ribonuclease

RNP    ribonucleoprotein

RT    reverse transcriptase

sgRNA    subgenomic RNA

ss    single stranded

T (e.g. T3)    triangulation number

T cell    T lymphocyte

UTR    untranslated region

VPg    genome-linked protein

References

Fauquet et al., 2005 C. Fauquet, M.A. Mayo, J. Maniloff, U. Desselberger, L.A. Ball, Virus Taxonomy: Eighth Report of the International Committee on Taxonomy of Viruses. In: C. Fauquet, M.A. Mayo, J. Maniloff, U. Desselberger, L.A. Ball, Virus Taxonomy: Eighth Report of the International Committee on Taxonomy of Viruses. Elsevier/Academic Press, Amsterdam2005.

Fenner, 1976 F. Fenner, Classification and nomenclature of viruses. Second report of the International Committee on Taxonomy of Viruses. Intervirol. 7 (1976) 1–115.

Francki et al., 1991 Francki, R.I.B., Fauquet, C.M., Knudson, D.L. and Brown, F. (1991). Classification and nomenclature of viruses. Fifth report of the International Committee on Taxonomy of Viruses. Arch. Virol. Suppl., 2. Vienna, Springer-Verlag.

Matthews, 1979 R.E. Matthews, Third report of the International Committee on Taxonomy of Viruses. Classification and nomenclature of viruses. Intervirol. 12 (1979) 129–296.

Matthews, 1982 R.E.F. Matthews, Classification and nomenclature of viruses. Fourth report of the international committee on taxonomy of viruses. Intervirol. 17 (1982) 1–199.

Murphy et al., 1995 Murphy, F.A., Fauquet, C.M., Bishop, D.H.L., Ghabrial, S.A., Jarvis, A.W., Martelli, G.P., Mayo, M.A. and Summers, M.D. (1995). Virus Taxonomy. Sixth Report of the International Committee on Taxonomy of Viruses. Vienna, Springer-Verlag.

Suttle, 2005 C.A. Suttle, Viruses in the sea. Nature. 437 (2005) 356–361.

van Regenmortel, 1990 M.H. van Regenmortel, Virus species, a much overlooked but essential concept in virus classification. Intervirol. 31 (1990) 241–254.

van Regenmortel et al., 2000 M.H.V. van Regenmortel, C.M. Fauquet, D.H.L. Bishop, E.B. Carstens, M.K. Estes, S.M. Lemon, J. Maniloff, M.A. Mayo, D.J. McGeoch, C.R. Pringle, R.B. Wickner, Virus TaxonomySeventh Report of the International Committee on Taxonomy of Viruses. Academic Press, San Diego2000.

Wildy, 1971 P. Wildy, Classification and nomenclature of viruses. First report of the International Committee on Nomenclature of Viruses. Monog. Virol. 5 (1971) 1–81.