Virus species names have been standardized; virus names remain unchanged
ABSTRACT
Virus taxonomy, comprising classification and nomenclature, is regulated by the International Committee on Taxonomy of Viruses (ICTV). Taxon names are standardized to facilitate recognition and communication, with defined suffixes for each rank (e.g., the names of orders, families, and genera end in -virales, -viridae, and -virus, respectively). However, until recently, a standard format for species names was lacking. In 2021, following extensive discussion and community consultation, the ICTV decided to adopt a standardized binomial (Linnaean) format for virus species names, consisting of the genus name followed by a “freeform” species epithet. Previously assigned virus species names that were non-compliant with the binomial format have been fully updated. In contrast to taxon names regulated by the ICTV, the names of viruses, or “common” names, such as yellow fever virus or human immunodeficiency virus, are not under the remit of the ICTV and have not been changed.
PERSPECTIVE
The International Committee on Taxonomy of Viruses (ICTV; https://ictv.global/) is a committee of the Virology Division of the International Union of Microbiology Societies that provides oversight and codified rules for the assignment and nomenclature of taxa for viruses and certain other mobile genetic elements. The ICTV is a volunteer organization of nearly 200 members [plus approximately 900 people in Study Groups (SGs)] representing all areas of virology (1). It strives to implement a taxonomy that reflects the evolutionary relationships among viruses as accurately as possible based on current knowledge (2), which means that taxonomy is regularly updated to adopt new discoveries (3). During the last seven years, there have been major developments, including the incorporation of viruses identified in metagenomic studies into the taxonomic framework (4), expansion of the framework from a 5-rank to a 15-rank system (5), and the establishment of several virus realms as the uppermost rank, each one representing distinct clades of apparently unrelated viruses that originated independently (6, 7). Moreover, the number of ICTV-designated virus species has been increasing steadily, from 3,185 in 2014 to 14,690 in 2023. Nevertheless, this number is by several orders of magnitude lower than the currently hypothesized number of species needed to accommodate the virus diversity already deduced from metagenomic data (8). Despite differing opinions on the usefulness of middle ranks (9, 10), the system of virus classification implemented by the ICTV provides the standard taxonomic framework used by the virology and wider communities (11–13).
Classification and taxonomic codes
Although the diversity of life remains only partially described, there has been a substantial and accelerating expansion of formal phylogeny-based taxonomies for all organisms. This process is guided by the relevant taxonomic codes—the International Code of Zoological Nomenclature (ICZN; https://www.iczn.org/the-code/the-code-online/) for animals; the International Code of Nomenclature (ICNafp; https://www.iaptglobal.org/icn) for algae, fungi, and plants; and the International Code of Nomenclature of Prokaryotes (ICNP; https://the-icsp.org/code-of-nomenclatur) for bacteria and archaea (1, 14). All these codes require species names (“scientific names”) to be formatted as binomials, consisting of a capitalized and italicized genus name separated by a space from a lower case and italicized species epithet, following the principles of Latinization and typography initiated by Linnaeus in the 18th century (15). The nomenclature of virus species is similarly regulated by the ICTV, which maintains and publishes the International Code of Virus Classification and Nomenclature (ICVCN, the “Code”; https://ictv.global/about/code).
Nomenclature of taxonomic ranks
The classification framework implemented by the ICTV includes the primary ranks of realm, kingdom, phylum, class, order, family, genus, and species. For all ranks except species, a standard nomenclature has long been adopted: taxon names are single words, written in italics with the first letter capitalized, and unique suffixes are used for each rank (e.g., all order, family, and genus names end in -virales, -viridae, and -virus, respectively) (5). Thus, most virologists should recognize the names Mononegavirales, Picornaviridae, and Hepacivirus as the names of an order, a family, and a genus of viruses, respectively. However, a standard format for species names was lacking. Therefore, designations, such as Lausannevirus, Escherichia virus T4, Yellow fever virus, Potato virus X, and Autographa californica multiple nucleopolyhedrovirus were valid species names until recently. Besides being unsatisfactory (from an organizational perspective), this lack of a standard created great confusion because the only distinguishing characteristics of many species names from the corresponding virus names (“common names”) were capitalization and italicization. For example, yellow fever virus (YFV) was a member of the species Yellow fever virus, potato virus X (PVX) was a member of the species Potato virus X, and Amur virus, Hantaan virus, and Soochong virus were all members of the species Hantaan orthohantavirus. Note also that species names, such as Yellow fever virus (classified in the genus Orthoflavivirus) or Potato virus X (classified in the genus Potexvirus) provided no information on their wider taxonomic relationships, since their genus assignment was not included, as it would be in the genus + species epithet format of binomial species names used elsewhere in biology.
Organism or “common” names
The scientific names of cellular life codify the taxonomic assignments of all classified organisms into species and taxa of higher ranks. Species names (e.g., Felis catus, Ovis aries, and Malus domestica) coexist with common names and groupings of organisms (e.g., cats, sheep, and apples) that predate formal biological classification and which differ across languages and regions. The format and usage of common names are outside of the remits of the relevant biological codes. However, they can be used in scientific communications, provided that their reference to organisms is equated to a defined and described taxon, for example, “populations of wolves (Canis lupus) have surged in eastern Finland.” The common names of viruses are the terms that the virus community has adopted in the primary literature. In some cases, there have been notable changes towards names that better describe a virus, such as the now-universally used human immunodeficiency virus (HIV) in place of the original names “lymphadenopathy-associated virus” (LAV) (16) and “human T lymphotropic virus type 3” (HTLV-III) (17), as well as human pegivirus in place of “hepatitis G virus” or “GB virus-C” (18). However, such changes have been relatively uncommon. Despite being unregulated and outside of the remit of the ICTV, common names of viruses have been remarkably stable over many decades. Lists of virus names in common usage and the taxa to which they have been assigned have been cataloged by the ICTV for many years in the Virus Metadata Resource (https://ictv.global/vmr).
Names of virus species
The adoption of a standard format for species names was a topic of discussion within the ICTV for decades. In 2016, a large group of ICTV members, including members of several ICTV SGs, evaluated the viability of adopting a binomial (Linnaean) format for species names, consisting of genus name + species epithet, similar to the format adopted by all other taxonomies, and asserted that generating binomial names would be practical and attainable (19). The ICTV Executive Committee discussed the possibility of adopting the binomial species names during subsequent years. In 2020, a consultation to the community was published (20), inviting virologists to provide feedback in the public forum of the ICTV web page. Although the usefulness of a binomial nomenclature was recognized, opinions diverged regarding which format to adopt for the species epithet, with many virologists opposed to a fully Latinized format. In the end, as a compromise, the ICTV adopted a binomial format with a “freeform” species epithet, meaning that the epithet, as long as it is italicized, does not have to follow Latinized grammar rules that are required in other taxonomic codes and can be made up of a string of letters of the Latin alphabet with or without numbers.
The adoption of a binomial nomenclature for virus species was approved in 2021, and the work of renaming species not then conforming to the binomial format took place over the next 3 years (2021–2024). As with other proposals for changes or additions to virus taxonomy, renaming a species or other taxon follows a standard procedure that is part of the annual cycle of taxonomy proposals (TPs) submitted and evaluated by the ICTV Executive Committee and ratified by all members of the ICTV (1). Any member of the community may submit a TP, but the vast majority are submitted by or through the taxon-specific (mostly family-specific) SGs, of which there are more than 120. The renaming effort was thus assigned to the SGs. Across all subcommittees, most SGs decided to adopt Latinized epithets, often based on host, geography, symptoms or clinical manifestations, or a combination of these terms. For example, the species Japanese encephalitis virus was renamed Orthoflavivirus japonicum, and the species Allium virus X was renamed Potexvirus ecsallii. The adoption of a freeform species epithet means that names, such as Miltonvirus MAM1 (family Ackermannviridae), Pelagivirus HTVC019P (family Autographiviridae), and Bromovirus CCMV (family Bromoviridae) could also be accepted as species names.
To be clear, it is the names of species that have been changed to the binomial format used in the rest of biology. Virus “common” names are not regulated by the ICTV, and these will remain as stable as the virology community desires them to be. Thus, yellow fever virus will continue to be called yellow fever virus, potato virus X will continue to be called potato virus X, and HIV-1 will continue to be called HIV-1 until the community (not the ICTV) decides otherwise. Typically, in scientific papers, grant proposals, conference presentations, etc., the species name is referred to only once, ideally the first time the virus name is mentioned. For example, the first sentence of a paper on a plant virus could be written as “Tomato spotted wilt virus (Orthotospovirus tomatomaculae) has a wide host range and worldwide distribution, and its occurrence in lettuce (Lactuca sativa) in California was first reported in 2006.” The use of the correct species name will be particularly important and helpful in documents issued by regulatory agencies. The species name will unequivocally identify the agent in question, whereas a virus can have multiple names (for example, in different languages or in different countries where the same language is spoken). However, as in all taxonomic codes, scientific names assigned to species are unique and universal.
Changing the names of more than 14,000 species inevitably caused some controversy. Even though the ICTV advertised and invited discussion of the change, both before it was approved in 2021 and during the renaming work, some virologists were surprised by the new names and misunderstood that the “common” names of the viruses, not the names of the species to which they were assigned, were being changed. Given the scale of the renaming, it is understandable that some virologists or groups of virologists may be unhappy with individual name choices; for example, there has been criticism about the new names of the species to which HIV-1 and severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) are assigned (Lentivirus humimdef1 and Betacoronavirus pandemicum, respectively). However, there is a straightforward path to renaming species if they are thought to be inappropriate: submission of a TP to the ICTV (https://ictv.global/taxonomy/templates). All TPs submitted from any source are given full consideration by the ICTV; those from the wider virology community are particularly appreciated as they may represent widely held opinions of virologists specializing in these areas.
Conclusion
Principles for the naming of virus taxa are comparable to conventions used for cellular organisms in other taxonomic codes. As a universal and internationally accepted virus taxonomy was developed relatively recently (21), it possesses a purposely designed and organizationally consistent taxonomic code and can coordinate a systematic and internally consistent nomenclatural policy for taxa. Thus, its TP framework enables coordinated changes, such as the switch to a binomial format for species names during 2021–2024.
The ICTV is openly committed to the incorporation into its taxonomy viruses known only from their nucleotide sequences (4). It adopts an explicit evolution-based framework for classifying viruses (2) and possesses the bioinformatic resources and internal organization to maintain and annually update its virus Master Species List and associated ICTV-managed resources (22).
The ICTV moreover provides abundant resources with which to access virus classification, for example through the “Taxonomy Browser” tool of the ICTV web page (https://ictv.global/taxonomy) that lists all established species names and links to the complete ICTV histories of each taxon. The newly introduced “Find The Species” tool (https://ictv.global/taxonomy/find_the_species) provides the current taxonomy for a virus when the full or partial virus name is entered into a search box; for example, if “yellow fever virus” is entered, the search results in “Orthoflavivirus flavi.” It also publishes the comprehensive and citable Online Report (https://ictv.global/report) for virus families and for higher taxonomic ranks. Regularly updated content in over 100 chapters describes the structural, genome, and wider clinical and epidemiological properties of the viruses in each group and taxonomic criteria for their assignment into species and genera.
ACKNOWLEDGMENTS
The authors thank Anya Crane (Integrated Research Facility at Fort Detrick/National Institute of Allergy and Infectious Diseases/National Institutes of Health, Fort Detrick, Frederick, MD, USA) for critically editing the manuscript.
This report is the opinion of the authors and does not represent the official position of the Centers for Disease Control and Prevention. A.M. is a program director at the U.S. National Science Foundation (NSF); the statements and opinions expressed herein are made in a personal capacity and do not constitute endorsement by NSF or the government of the United States. The views and conclusions contained in this document are those of the authors and should not be interpreted as necessarily representing the official policies, either expressed or implied, of the U.S. Department of Health and Human Services or of the institutions and companies affiliated with the authors, nor does mention of trade names, commercial products, or organizations imply endorsement by the U.S. Government.
D.L.R. acknowledges funding from the UK Medical Research Council (MRC, MC_UU_00034/5). E.J.L. was supported by the National Institute of Allergy and Infectious Diseases of the National Institutes of Health under Award Number U24AI162625. E.M.A. gratefully acknowledges the support of the Biotechnology and Biological Sciences Research Council (BBSRC); this research was funded by the BBSRC Institute Strategic Programme Food, Microbiome and Health BB/X011054/1 and its constituent project BBS/E/F/000PR13631 and by the BBSRC Institute Strategic Programme Microbes and Food Safety BB/X011011/1 and its constituent projects BBS/E/F/000PR13634, BBS/E/F/000PR13635, and BBS/E/F/000PR13636. F.O.A. was supported by National Institutes of Health grant no. 1R35GM147290-01. H.M.O. was supported by the University of Helsinki and the Research Council of Finland by funding for FINStruct and Instruct Centre FI, part of Biocenter Finland and Instruct-ERIC and Horizon MSCA 101120407. J.F.-A. acknowledges financial support from Fapesp (2019/25078-9) and CNPq (312528/2020-5). This work was also supported in part through a Laulima Government Solutions, LLC, prime contract with the National Institute of Allergy and Infectious Diseases (Contract No. HHSN272201800013C). J.H.K. performed this work as an employee of Tunnell Government Services (TGS), a subcontractor of Laulima Government Solutions, LLC, under Contract No. HHSN272201800013C. L.R. acknowledges support from the European Commission–NextGenerationEU, Project SUS-MIRRI.IT "Strengthening the MIRRI Italian Research Infrastructure for Sustainable Bioscience and Bioeconomy," code n. IR0000005. The work conducted by the U.S. Department of Energy (DOE) Joint Genome Institute (https://ror.org/04xm1d337), a DOE Office of Science User Facility, is supported by the Office of Science of the U.S. Department of Energy operated under Contract No. DE-AC02-05CH11231 (S.R.). S.S. acknowledges support from the Mississippi Agricultural and Forestry Experiment Station (MAFES), USDA-ARS project 58-6066-3-044, USDA-NIFA SCRI Project 1029242, and NIFA-USDA Hatch Project 7006130.
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