In a recent article published in PLOS Biology, a team of 45 virologists, evolutionary biologists, bioinformaticians, and structural biologists from around the world arrived at a consensus on virus classification methodologies and presented an integrated taxonomical framework for the systematics and taxonomy of viruses.
Like all taxonomic fields associated with classifying lifeforms, virus taxonomy has undergone multiple revisions and updates based on novel methods and discoveries. Early virus classification and nomenclature were based on characteristics such as morphology, nucleic acid type, and the susceptibility of the virus to inactivation using low pH, high temperature, and organic solvents. The advent of genomics and technologies such as high-throughput and next-generation sequencing has resulted in the inclusion of genomic-level classification as a requirement for virus taxonomy.
Given that the estimation of viral diversity based on phenotypic classifications, in vitro cultures, and strain isolation estimates viral species diversity at a much lower scale than diversity estimates based on genomic data, the topic of contention among virologists is whether phenotypic properties of viruses such as host range, viral isolation in cell cultures, pathogenicity, morphology, etc., should be required criteria for virus taxonomy.
A 2016 committee convened by the International Committee on Taxonomy of Viruses (ICTV) allowed viruses that were known only based on their genomic data to be included in virus taxonomy, which resulted in the identification of a large number of new viral taxa. Similar to the trend seen in the taxonomy of larger lifeforms, this has highlighted the need for a unified, integrated taxonomic approach that includes the traditional, morphology-based classification, as well as a metagenomics-based evolutionary taxonomy.
With a unified taxonomic framework in mind, 45 virologists, structural and evolutionary biologists, and bioinformaticians attended a meeting in April 2022 in Oxford, United Kingdom, to discuss methodologies and arrive at a consensus for a unified viral taxonomic framework. They discussed the reconciliation of the newly developed classification methods based on genetic data and the phenetic classification methods developed by virologists over decades, which include, apart from morphology, a range of properties such as epidemiology and virus-host ecology.
The recommendations proposed by the team were in the form of four principles of virus taxonomy. The first principle states that the taxonomy of viruses should reflect their evolutionary history, which means that taxonomic assignments must be based on monophyly in the evolutionary relationships. Based on the evolutionary patterns of hallmark genes, which are generally modules in the viral genome associated with virion formation and replication, viruses can be assigned to independent realms that reflect separate evolutionary origins.
The second principle discusses using viral properties to guide the assignment of ranks within the larger taxonomic groups determined based on evolutionary relationships. There are about 15 taxonomic ranks, including realms and species at opposite ends, the assignment of viruses to these ranks should follow the order of evolutionary patterns, genomic properties, and phenotypic characters. Species-level classifications can use characteristics such as host range, epidemiology, or disease associations as long as these categories also result in monophyly.
However, according to the third principle, while the proposed integrated taxonomic approach provides a framework for the evolutionary classification of viruses, alternate methods of classification based on epidemiology or other regulatory properties are valuable in specific circumstances. These methods, such as the Baltimore classification, may not follow evolutionary patterns and may include polyphyletic groups, but have clinical and epidemiological value, as in the case of the human immunodeficiency virus and arboviruses.
The last principle states that in the case of viruses with only genomic data and no other properties for the characterization of the virus, the metagenomic data will undergo strict quality control for sequence completion and accuracy. While the ICTV does not stipulate the need for multiple sequences for the taxonomic assignment of the new virus, although multiple sequences will provide information on the complete genome and genetic diversity, a set of guidelines is being developed to guide the submission of metagenomic data into publicly accessible databases for taxonomic classification.
Overall, the four principles for virus taxonomy outlined in this article provide the ICTV with a roadmap for integrating new technologies and discoveries into the development and expansion of viral classification systems. These principles also provide clarity, consistency, and a standardized method for viral classification to the wider community of virologists.