Four principles to establish a universal virus taxonomy

Abstract

A universal taxonomy of viruses is essential for a comprehensive view of the virus world and for communicating the complicated evolutionary relationships among viruses. However, there are major differences in the conceptualisation and approaches to virus classification and nomenclature among virologists, clinicians, agronomists, and other interested parties. Here, we provide recommendations to guide the construction of a coherent and comprehensive virus taxonomy, based on expert scientific consensus. Firstly, assignments of viruses should be congruent with the best attainable reconstruction of their evolutionary histories, i.e., taxa should be monophyletic. This fundamental principle for classification of viruses is currently included in the International Committee on Taxonomy of Viruses (ICTV) code only for the rank of species. Secondly, phenotypic and ecological properties of viruses may inform, but not override, evolutionary relatedness in the placement of ranks. Thirdly, alternative classifications that consider phenotypic attributes, such as being vector-borne (e.g., "arboviruses"), infecting a certain type of host (e.g., "mycoviruses," "bacteriophages") or displaying specific pathogenicity (e.g., "human immunodeficiency viruses"), may serve important clinical and regulatory purposes but often create polyphyletic categories that do not reflect evolutionary relationships. Nevertheless, such classifications ought to be maintained if they serve the needs of specific communities or play a practical clinical or regulatory role. However, they should not be considered or called taxonomies. Finally, while an evolution-based framework enables viruses discovered by metagenomics to be incorporated into the ICTV taxonomy, there are essential requirements for quality control of the sequence data used for these assignments. Combined, these four principles will enable future development and expansion of virus taxonomy as the true evolutionary diversity of viruses becomes apparent.

Fig 1. Ranks used in virus taxonomy.

Schematic depiction of the 15-rank taxonomic framework used by the ICTV. It includes the methodologies that may be used to determine virus evolutionary relationships and make assignments at each rank. The pyramid shape indicates that the number of taxa increases from the top rank (realm) to the most basal rank (species, Sp.). The names of the 15 ranks are shown on the left of the pyramid, and the methodologies are on the right (AAS, amino acid sequence similarity; NS, nucleotide sequence similarity). The pyramid includes a hypothetical example of the taxonomy of a realm, indicating the number of taxa at each rank (filled circles). The phenotypic properties of classified viruses that may inform rank placements are depicted below the pyramid.

Fig 2. Structure-based dendrogram of capsid proteins of members of the kingdom Bamfordvirae.

Structure-based phylogenetic tree inferred from major capsid protein (MCP) structures of the members of the kingdom Bamfordvirae in the Varidnaviria realm. Members of Bamfordvirae encode a vertical double-jelly roll fold MCP, which is the hallmark protein of this group of viruses. Next to each MCP structure are the virus name (top), the phylum (middle), and family (bottom), with “Faustovirus” not yet officially classified and Finnlakeviridae not yet assigned to any higher taxon. The evolutionary distances across the depicted members of the originally called PRD1-adenovirus viral lineage [67] were calculated with the Homologous Structure Finder software [50] and depicted with PHYLIP (https://evolution.genetics.washington.edu/phylip.html); the evolutionary distances are shown next to each branch. The protein data bank identifiers (PDBid) for the structures are as follows: PRD1: PDBid 1HX6; PBCV-1: 1M3Y; adenovirus: 1P2Z; STIV: 2BBD; Vaccinia D13: 2YGB; Sputnik: 3J26; Faustovirus: 5J7O; FLiP: 5OAC; ASFV p72: 6KU9; PM2: 2W0C. Adapted from [62].

Fig 3. Examples of incompatibilities between species assignments and phylogenetic groupings.

(A) Genetic relationships of HIV-1 (red dots) with simian immunodeficiency viruses infecting chimpanzees (gray dots) and gorillas (black dots). HIV-1 strains are polyphyletic and cannot be assigned to a single species taxon without incorporating nonhuman viruses within the definition. (B) Genetic relationships of louping ill virus (LIV) with tick-borne encephalitis virus (TBEV) strains isolated in Europe and Asia, with the principal groups labeled. Although LIV (red dots) is assigned to the species Louping ill virus, it lies within the phylogenetic tree created by strains of TBEV that all belong to the species Tick-borne encephalitis virus. The current assignment of LIV as a species therefore logically prevents strains of TBEV being assigned into a single species if species were to remain monophyletic. Trees were constructed from maximum composite likelihood distances between nucleotide sequences of (A) the pol gene of HIV-1/SIV and (B) the complete coding sequence of TBEV and LIV. To investigate the robustness of branches, nucleotide positions were bootstrap resampled 100 times as implemented in the MEGA7 program [91]; branches with 70% or greater support are labeled. The HIV-1/SIV tree was rooted using the HIV-2 sequence, M31113; the TBEV/LIV tree was rooted using the closely related Omsk haemorrhagic fever virus sequence, AY193805. Both trees have been annotated with a scale bar indicating substitutions per site.