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Virus classification

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Virus classification is the process of naming viruses and placing them into a taxonomic system similar to the classification systems used for cellular organisms.

Viruses are classified by phenotypic characteristics, such as morphology, nucleic acid type, mode of replication, host organisms, and the type of disease they cause. The formal taxonomic classification of viruses is the responsibility of the International Committee on Taxonomy of Viruses (ICTV) system, although the Baltimore classification system can be used to place viruses into one of seven groups based on their manner of mRNA synthesis. Specific naming conventions and further classification guidelines are set out by the ICTV.

In 2021, the ICTV changed the International Code of Virus Classification and Nomenclature (ICVCN) to mandate a binomial format (genus|| ||species) for naming new viral species similar to that used for cellular organisms; the names of species coined prior to 2021 are gradually being converted to the new format, a process which has been stated to be planned to be completed by end 2023.

As at 2022, the ICTV taxonomy listed 11,273 named virus species (including some classed as satellite viruses and others as viroids) in 2,818 genera, 264 families, 72 orders, 40 classes, 17 phyla, 9 kingdoms and 6 realms. [1] However, the number of named viruses considerably exceeds the number of named virus species since, by contrast to the classification systems used elsewhere in biology, a virus "species" is a collective name for a group of (presumably related) viruses sharing certain common features (see below). Also, the use of the term "kingdom" in virology does not equate to its usage in other biological groups, where it reflects high level groupings that separate completely different kinds of organisms (see Kingdom (biology)).

Definitions

Virus definition

The currently accepted and formal definition of a 'virus' was accepted by the ICTV Executive Committee in November 2020 and ratified in March 2021, and is as follows:[2]

Viruses sensu stricto are defined operationally by the ICTV as a type of MGE that encodes at least one protein that is a major component of the virion encasing the nucleic acid of the respective MGE and therefore the gene encoding the major virion protein itself or MGEs that are clearly demonstrable to be members of a line of evolutionary descent of such major virion protein-encoding entities. Any monophyletic group of MGEs that originates from a virion protein-encoding ancestor should be classified as a group of viruses.

Species definition

Species form the basis for any biological classification system. Before 1982, it was thought that viruses could not be made to fit Ernst Mayr's reproductive concept of species, and so were not amenable to such treatment. In 1982, the ICTV started to define a species as "a cluster of strains" with unique identifying qualities. In 1991, the more specific principle that a virus species is a polythetic class of viruses that constitutes a replicating lineage and occupies a particular ecological niche was adopted.[3]

As at 2021 (the latest edition of the ICVCN), the ICTV definition of species states: "A species is the lowest taxonomic level in the hierarchy approved by the ICTV. A species is a monophyletic group of MGEs (mobile genetic elements) whose properties can be distinguished from those of other species by multiple criteria", with the comment "The criteria by which different species within a genus are distinguished shall be established by the appropriate Study Group. These criteria may include, but are not limited to, natural and experimental host range, cell and tissue tropism, pathogenicity, vector specificity, antigenicity, and the degree of relatedness of their genomes or genes. The criteria used should be published in the relevant section of the ICTV Report and reviewed periodically by the appropriate Study Group."[4]

Below species rank (named viruses/virus strains/isolates)

Many individually named viruses (sometimes referred to as "virus strains") exist at below the rank of virus species. The ICVCN gives the examples of blackeye cowpea mosaic virus and peanut stripe virus, which are both classified in the species Bean common mosaic virus, the latter a member of the genus Potyvirus that will in due course receive a binomial name as Potyvirus [species...]. As another example, the virus SARS-CoV-1, that causes severe acute respiratory syndrome (SARS) is different from the virus SARS-CoV-2, the cause of the COVID-19 pandemic, but both are classified within the same virus species, a member of the genus Betacoronavirus that is currently known as Severe acute respiratory syndrome-related coronavirus which, per the 2021 mandate from the ICTV, will also receive a binomial name in due course. As set out in the ICVCN, section 3.4, the names [and definitions] of taxa below the rank of species are not governed by the ICTV; "Naming of such entities is not the responsibility of the ICTV but of international specialty groups. It is the responsibility of ICTV Study Groups to consider how these entities may best be classified into species."[4] Using the example given above, the virus causing the COVID-19 pandemic was given the designation "SARS-CoV-2" by the Coronaviridae Study Group (CSG) of the International Committee on Taxonomy of Viruses in 2020; in the same publication, this Study Group recommended a naming convention for particular isolates of this virus "resembl[ing] the formats used for isolates of avian coronaviruses, filoviruses and influenza virus" in the format virus/host/location/isolate/date, with a cited example as "SARS-CoV-2/human/Wuhan/X1/2019".[5]

ICTV classification

Comparison 1991 and 2018b virus taxonomy by ICTV

The International Committee on Taxonomy of Viruses began to devise and implement rules for the naming and classification of viruses early in the 1970s, an effort that continues to the present. The ICTV is the only body charged by the International Union of Microbiological Societies with the task of developing, refining, and maintaining a universal virus taxonomy, following the methods set out in the International Code of Virus Classification and Nomenclature.[4][6] The system shares many features with the classification system of cellular organisms, such as taxon structure. However, some differences exist, such as the universal use of italics for all taxonomic names, unlike in the International Code of Nomenclature for algae, fungi, and plants and International Code of Zoological Nomenclature.

Viral classification starts at the level of realm and continues as follows, with the taxonomic suffixes in parentheses:[4]

Realm (-viria)
Subrealm (-vira)
Kingdom (-virae)
Subkingdom (-virites)
Phylum (-viricota)
Subphylum (-viricotina)
Class (-viricetes)
Subclass (-viricetidae)
Order (-virales)
Suborder (-virineae)
Family (-viridae)
Subfamily (-virinae)
Genus (-virus)
Subgenus (-virus)
Species

In parallel to the system of binomial nomenclature adopted in cellular species, the ICTV has recently (2021) mandated that new virus species be named in a binomial format (genus|| species), and that pre-existing virus species names be progressively replaced with new names in the binomial format.[7] A mid-2023 review of the status of this changeover stated: "...a large number of proposals [concerning virus nomenclature, submitted to the ICTV Executive Committee (EC) for its consideration] renamed existing species for compliance with the recently mandated binomial nomenclature format. As a result, 8,982 out of the current 11,273 species (80%) now have binomial names. The process will be concluded in 2023, with the remaining 2,291 species being renamed."[8]

As of 2021, all levels of taxa except subrealm, subkingdom, and subclass are used. Six realms, one incertae sedis class, 22 incertae sedis families, and two incertae sedis genera are recognized:[9]

Realms:

Incertae sedis classes:

Incertae sedis families:

Incertae sedis genera:

Structure-based virus classification

It has been suggested that similarity in virion assembly and structure observed for certain viral groups infecting hosts from different domains of life (e.g., bacterial tectiviruses and eukaryotic adenoviruses or prokaryotic Caudovirales and eukaryotic herpesviruses) reflects an evolutionary relationship between these viruses.[10] Therefore, structural relationship between viruses has been suggested to be used as a basis for defining higher-level taxa – structure-based viral lineages – that could complement the ICTV classification scheme of 2010.[11]

The ICTV has gradually added many higher-level taxa using relationships in protein folds. All four realms defined in the 2019 release are defined by the presence of a protein of a certain structural family.[12]

Baltimore classification

The Baltimore Classification of viruses is based on the method of viral mRNA synthesis

Baltimore classification (first defined in 1971) is a classification system that places viruses into one of seven groups depending on a combination of their nucleic acid (DNA or RNA), strandedness (single-stranded or double-stranded), sense, and method of replication. Named after David Baltimore, a Nobel Prize-winning biologist, these groups are designated by Roman numerals. Other classifications are determined by the disease caused by the virus or its morphology, neither of which are satisfactory due to different viruses either causing the same disease or looking very similar. In addition, viral structures are often difficult to determine under the microscope. Classifying viruses according to their genome means that those in a given category will all behave in a similar fashion, offering some indication of how to proceed with further research. Viruses can be placed in one of the seven following groups:[13]

Visualization of the 7 groups of virus according to the Baltimore Classification

DNA viruses

Viruses with a DNA genome, except for the DNA reverse transcribing viruses, are members of three of the four recognized viral realms: Duplodnaviria, Monodnaviria, and Varidnaviria. But the incertae sedis order Ligamenvirales, and many other incertae sedis families and genera, are also used to classify DNA viruses. The domains Duplodnaviria and Varidnaviria consist of double-stranded DNA viruses; other double-stranded DNA viruses are incertae sedis. The domain Monodnaviria consists of single-stranded DNA viruses that generally encode a HUH endonuclease; other single-stranded DNA viruses are incertae sedis.[14]

  • Group I: viruses possess double-stranded DNA. Viruses that cause chickenpox and herpes are found here.
  • Group II: viruses possess single-stranded DNA.
Examples of DNA viruses
Virus family Examples (common names) Virion
naked/enveloped
Capsid
symmetry
Nucleic acid type Group
1. Adenoviridae Canine hepatitis virus, Some types of the common cold Naked Icosahedral ds I
2. Papovaviridae JC virus, HPV Naked Icosahedral ds circular I
3. Parvoviridae Human parvovirus B19, canine parvovirus Naked Icosahedral ss II
4. Herpesviridae Herpes simplex virus, varicella-zoster virus, cytomegalovirus, Epstein–Barr virus Enveloped Icosahedral ds I
5. Poxviridae Smallpox virus, cowpox, myxoma virus, monkeypox, vaccinia virus Complex coats Complex ds I
6. Anelloviridae Torque teno virus Naked Icosahedral ss circular II
7. Pleolipoviridae HHPV1, HRPV1 Enveloped ss/ds linear/circular I/II

RNA viruses

All viruses that have an RNA genome, and that encode an RNA-dependent RNA polymerase (RdRp), are members of the kingdom Orthornavirae, within the realm Riboviria.[15]

  • Group III: viruses possess double-stranded RNA genomes, e.g. rotavirus.
  • Group IV: viruses possess positive-sense single-stranded RNA genomes. Many well known viruses are found in this group, including the picornaviruses (which is a family of viruses that includes well-known viruses like Hepatitis A virus, enteroviruses, rhinoviruses, poliovirus, and foot-and-mouth virus), SARS virus, hepatitis C virus, yellow fever virus, and rubella virus.
  • Group V: viruses possess negative-sense single-stranded RNA genomes. Ebola and Marburg viruses are well known members of this group, along with influenza virus, measles, mumps and rabies.
Examples of RNA viruses
Virus Family Examples (common names) Capsid
naked/enveloped
Capsid
Symmetry
Nucleic acid type Group
1. Reoviridae Reovirus, rotavirus Naked Icosahedral ds III
2. Picornaviridae Enterovirus, rhinovirus, hepatovirus, cardiovirus, aphthovirus, poliovirus, parechovirus, erbovirus, kobuvirus, teschovirus, coxsackie Naked Icosahedral ss IV
3. Caliciviridae Norwalk virus Naked Icosahedral ss IV
4. Togaviridae Eastern equine encephalitis Enveloped Icosahedral ss IV
5. Arenaviridae Lymphocytic choriomeningitis virus, Lassa fever Enveloped Complex ss(−) V
6. Flaviviridae Dengue virus, hepatitis C virus, yellow fever virus, Zika virus Enveloped Icosahedral ss IV
7. Orthomyxoviridae Influenzavirus A, influenzavirus B, influenzavirus C, isavirus, thogotovirus Enveloped Helical ss(−) V
8. Paramyxoviridae Measles virus, mumps virus, respiratory syncytial virus, Rinderpest virus, canine distemper virus Enveloped Helical ss(−) V
9. Bunyaviridae California encephalitis virus, Sin nombre virus Enveloped Helical ss(−) V
10. Rhabdoviridae Rabies virus, Vesicular stomatitis Enveloped Helical ss(−) V
11. Filoviridae Ebola virus, Marburg virus Enveloped Helical ss(−) V
12. Coronaviridae Human coronavirus 229E, Human coronavirus NL63, Human coronavirus OC43, Human coronavirus HKU1, Middle East respiratory syndrome-related coronavirus, Severe acute respiratory syndrome coronavirus, and Severe acute respiratory syndrome coronavirus 2 Enveloped Helical ss IV
13. Astroviridae Astrovirus Naked Icosahedral ss IV
14. Bornaviridae Borna disease virus Enveloped Helical ss(−) V
15. Arteriviridae Arterivirus, equine arteritis virus Enveloped Icosahedral ss IV
16. Hepeviridae Hepatitis E virus Naked Icosahedral ss IV

Reverse transcribing viruses

All viruses that encode a reverse transcriptase (also known as RT or RNA-dependent DNA polymerase) are members of the class Revtraviricetes, within the phylum Arterviricota, kingdom Pararnavirae, and realm Riboviria. The class Blubervirales contains the single family Hepadnaviridae of DNA RT (reverse transcribing) viruses; all other RT viruses are members of the class Ortervirales.[16]

  • Group VI: viruses possess single-stranded RNA viruses that replicate through a DNA intermediate. The retroviruses are included in this group, of which HIV is a member.
  • Group VII: viruses possess double-stranded DNA genomes and replicate using reverse transcriptase. The hepatitis B virus can be found in this group.
Examples of reverse transcribing viruses
Virus Family Examples (common names) Capsid
naked/enveloped
Capsid
Symmetry
Nucleic acid type Group
1. Retroviridae HIV Enveloped dimer RNA VI
2. Caulimoviridae Caulimovirus, Cacao swollen-shoot virus (CSSV) Naked VII
3. Hepadnaviridae Hepatitis B virus Enveloped Icosahedral circular, partially ds VII

Historical systems

Holmes classification

Holmes (1948) used a Linnaean taxonomy with binomial nomenclature to classify viruses into 3 groups under one order, Virales. They are placed as follows:

The system was not accepted by others due to its neglect of morphological similarities.[17]

Subviral agents

Infectious agents are smaller than viruses and have only some of their properties.[18][19] Since 2015, the ICTV has allowed them to be classified in a similar way as viruses are.[20]

Viroids and virus-dependent agents

Viroids

Satellites

Satellites depend on co-infection of a host cell with a helper virus for productive multiplication. Their nucleic acids have substantially distinct nucleotide sequences from either their helper virus or host. When a satellite subviral agent encodes the coat protein in which it is encapsulated, it is then called a satellite virus.

Satellite-like nucleic acids resemble satellite nucleic acids, in that they replicate with the aid of helper viruses. However they differ in that they can encode functions that can contribute to the success of their helper viruses; while they are sometimes considered to be genomic elements of their helper viruses, they are not always found within their helper viruses.[18]

Defective interfering particles

Defective interfering particles are defective viruses that have lost their ability to replicate except in the presence of a helper virus, which is normally the parental virus. They can also interfere with the helper virus.

  • Defective interfering particles (RNA)
  • Defective interfering particles (DNA)

Viriforms

Viriforms are a polyphyletic category of endogenous viral elements. Sometime in their evolution, they became "domesticated" by their host as a key part of the host's lifecycle. The prototypical example is members of the (also polyphyletic) Polydnaviriformidae, which are used by wasps to send pieces of immunity-blunting DNA into the prey by packing them into virion-like particles. Other members are so-called gene transfer agents (GTAs) found among prokaryotes. GTA particles resemble tailed phages, but are smaller and carry mostly random pieces of host DNA. GTAs are produced by the host in times of stress; releasing GTAs kills the host cell, but allows pieces of its genetic material to live on in other bacteria, usually of the same species.[24] The three known clades of GTAs, Rhodogtaviriformidae, Bartogtaviriformidae, and Brachygtaviriformidae, all arised independently from different parts of the Caudoviricetes family tree.[25]

See also

Notes

  1. ^ "Virus Taxonomy: 2022 v3 Release". ictv.global. International Committee on Taxonomy of Viruses. Retrieved 5 January 2024.
  2. ^ Koonin, Eugene V.; Dolja, Valerian V.; Krupovic, Mart; Kuhn, Jens H. (2021-09-01). "Viruses Defined by the Position of the Virosphere within the Replicator Space". Microbiology and Molecular Biology Reviews. 85 (4): e0019320. doi:10.1128/MMBR.00193-20. PMC 8483706. PMID 34468181.
  3. ^ Alimpiev, Egor (March 15, 2019). Rethinking the Virus Species Concept (PDF). Archived (PDF) from the original on 2020-09-22.
  4. ^ a b c d "The International Code of Virus Classification and Nomenclature (ICVCN), March 2021 edition". International Committee on Taxonomy of Viruses. Retrieved 6 January 2024.
  5. ^ Coronaviridae Study Group of the International Committee on Taxonomy of Viruses (April 2020). "The species Severe acute respiratory syndrome-related coronavirus: classifying 2019-nCoV and naming it SARS-CoV-2". Nature Microbiology. 5 (4): 536–544. doi:10.1038/s41564-020-0695-z. PMC 7095448. PMID 32123347.
  6. ^ Lefkowitz EJ, Dempsey DM, Hendrickson RC, Orton RJ, Siddell SG, Smith DB (January 2018). "Virus taxonomy: the database of the International Committee on Taxonomy of Viruses (ICTV)". Nucleic Acids Research. 46 (D1): D708–D717. doi:10.1093/nar/gkx932. PMC 5753373. PMID 29040670.
  7. ^ Walker, Peter J.; Siddell, Stuart G.; Lefkowitz, Elliot J.; et al. (6 July 2021). "Changes to virus taxonomy and to the International Code of Virus Classification and Nomenclature ratified by the International Committee on Taxonomy of Viruses (2021)". Archives of Virology. 168: 2633–2648. doi:10.1007/s00705-021-05156-1.
  8. ^ Zerbini, F.M.; Siddell, S.G.; Lefkowitz, E.J.; et al. (10 June 2023). "Changes to virus taxonomy and the ICTV Statutes ratified by the International Committee on Taxonomy of Viruses (2023)". Archives of Virology. 168 (article no. 175): 1–11. doi:10.1007/s00705-023-05797-4.
  9. ^ "Virus Taxonomy: 2021 Release". ictv.global. International Committee on Taxonomy of Viruses. Retrieved 26 January 2023.
  10. ^ Bamford DH (May 2003). "Do viruses form lineages across different domains of life?". Research in Microbiology. 154 (4): 231–6. doi:10.1016/S0923-2508(03)00065-2. PMID 12798226.
  11. ^ Krupovič M, Bamford DH (December 2010). "Order to the viral universe". Journal of Virology. 84 (24): 12476–9. doi:10.1128/JVI.01489-10. PMC 3004316. PMID 20926569.
  12. ^ "Virus Taxonomy: 2019 Release". talk.ictvonline.org. International Committee on Taxonomy of Viruses. Retrieved 26 April 2020.
  13. ^ "Baltimore Classification of Viruses". www.web-books.com. Retrieved 2023-01-02.
  14. ^ "Virus Taxonomy: 2019 Release". talk.ictvonline.org. International Committee on Taxonomy of Viruses. Retrieved 26 April 2020.
  15. ^ "Virus Taxonomy: 2019 Release". talk.ictvonline.org. International Committee on Taxonomy of Viruses. Retrieved 25 April 2020.
  16. ^ Koonin EV, Dolja VV, Krupovic M, Varsani A, Wolf YI, Yutin N, Zerbini M, Kuhn JH. "Proposal: Create a megataxonomic framework, filling all principal taxonomic ranks, for realm Riboviria". International Committee on Taxonomy of Viruses (ICTV). Retrieved 2020-05-21.{{cite web}}: CS1 maint: multiple names: authors list (link)
  17. ^ Kuhn, Jens H. (2020). "Virus Taxonomy". Reference Module in Life Sciences. Encyclopedia of Virology. pp. 28–37. doi:10.1016/B978-0-12-809633-8.21231-4. ISBN 978-0-12-809633-8. PMC 7157452. Archived from the original on Nov 18, 2023.
  18. ^ a b "Subviral Agents". ICTV 9th Report (2011). International Committee on Taxonomy of Viruses. Archived from the original on Jul 7, 2022. Retrieved 2020-06-15. Updated version in sync with current release: "Subviral Agents". 10th Report. International Committee on Taxonomy of Viruses. Archived from the original on Jul 2, 2022.
  19. ^ Strauss, James H.; Strauss, Ellen G. (2008). "Subviral Agents". Viruses and Human Disease. Elsevier. pp. 345–368. doi:10.1016/b978-0-12-373741-0.50012-x. ISBN 978-0-12-373741-0. S2CID 80872659. Archived from the original on Nov 29, 2023.
  20. ^ TaxoProp 2015.002aG
  21. ^ Di Serio, Francesco; Li, Shi-Fang; Matoušek, Jaroslav; Owens, Robert A.; Pallás, Vicente; Randles, John W.; Sano, Teruo; Verhoeven, Jacobus Th. J.; Vidalakis, Georgios; Flores, Ricardo (June 2020). "Family: Avsunviroidae". The 10th ICTV Report on Virus Classification and Taxon Nomenclature. ICTV. Retrieved 16 January 2023.
  22. ^ Di Serio, Francesco; Owens, Robert A.; Li, Shi-Fang; Matoušek, Jaroslav; Pallás, Vicente; Randles, John W.; Sano, Teruo; Verhoeven, Jacobus Th. J.; Vidalakis, Georgios; Flores, Ricardo (November 2020). "Family: Pospiviroidae". The 10th ICTV Report on Virus Classification and Taxon Nomenclature. ICTV. Retrieved 16 January 2023.
  23. ^ Krupovic, Mart; Kuhn, Jens H.; Fischer, Matthias G. (7 October 2015). "A classification system for virophages and satellite viruses". Archives of Virology. 161 (1): 233–247. doi:10.1007/s00705-015-2622-9. hdl:11858/00-001M-0000-0028-DC34-F. PMID 26446887.
  24. ^ Kuhn, JH; Koonin, EV (3 February 2023). "Viriforms-A New Category of Classifiable Virus-Derived Genetic Elements". Biomolecules. 13 (2). doi:10.3390/biom13020289. PMC 9953437. PMID 36830658.
  25. ^ Kogay, R; Koppenhöfer, S; Beatty, JT; Kuhn, JH; Lang, AS; Zhaxybayeva, O (2022). "Formal recognition and classification of gene transfer agents as viriforms". Virus evolution. 8 (2): veac100. doi:10.1093/ve/veac100. PMC 9662315. PMID 36381234.